Desert Malaria: An Emerging Malaria Paradigm and Its Global Impact on Disease Elimination 9811976929, 9789811976926

Table of contents :
Foreword
Preface
Acknowledgements
Contents
1: `Desert Malaria´: An Emerging New Paradigm
1.1 Introduction
1.1.1 Definition
1.1.2 Malaria Symptoms
1.1.3 Parasites
1.1.4 Malaria Vectors
1.1.4.1 The Americas
1.1.4.2 Africa
1.1.4.3 Asia-Pacific
1.2 Deserts, Arid Environments, and Malaria
1.3 Ecotypes of Malaria in the Desert Environments
1.4 Desert-Based Malaria
1.4.1 The Problem
1.4.2 Types of Desert-Based Malaria Paradigms
1.4.2.1 Desert Oasis Malaria
1.4.2.2 Desert Fringe Malaria
1.4.2.3 Desert Malaria
2: Global vis-à-vis Desert-Driven Malaria
2.1 Global Malaria Scenario
2.2 Desert-Driven Malaria
2.2.1 Malaria in African Sahara Desert
2.2.2 Malaria in Arabian Peninsula Desert
2.2.3 Malaria in the Middle East/Central and West Asian Deserts
2.2.4 Malaria in the Great Indian Thar Desert
2.2.4.1 Brief History of Malaria in India
2.2.4.2 Malaria Situation in Rajasthan State
Malaria Situation During Pre-1966 Period
Malaria Situation During 1967-1976
Malaria Situation During 1977-1995
Malaria Situation During 1996-2020
Malaria Situation in the Great Indian Thar Desert
Milestones on Malaria Research in the Thar Desert
3: World Deserts: Environments and Malaria Potential
3.1 Introduction
3.2 Desert Environments, Man, and Malaria
3.3 Deserts with Potential to Exacerbate Malaria
3.3.1 Sahara Desert and Malaria
3.3.2 Arabian Peninsula Desert and Malaria
3.3.3 The Great Indian Thar Desert and Malaria
4: Desert Water Sources and Vector Adaptation
4.1 Introduction
4.2 Traditional Sources of Water in Deserts
4.2.1 Lakes
4.2.2 Oases
4.2.3 Desert Fringes
4.2.4 Springs, Well, and Seasonal Streams
4.2.5 Wadi
4.2.6 Fossil Water
4.2.7 Mines
4.2.8 Petro Products
4.2.9 Aquifers
4.2.10 Canals
4.2.11 Snowfall in the Sahara Desert: A New and Rare Source for Water
5: `TANKA´ and `BERI´: The Most Crucial Habitats for Breeding of Anopheles stephensi and Emergence of ``DESERT MALARIA´´ in th...
5.1 Introduction
5.2 Wetlands and Sources of Potable Water
5.3 `Tanka and `Beri´: Most Significant Malariogenic Habitats in the Thar Desert
5.3.1 `Tanka´
5.3.1.1 Benefits of Tanka
5.3.1.2 Present Status of Tankas
5.3.1.3 Size of Tanka and Construction Materials
5.3.1.4 Volume of Water per Tanka Required
5.3.2 Beri
5.4 Microclimates of `Tanka´ and `Beri´
6: Extensive Canalization and Its Impact on Transformation of the Thar Desert and Malaria Exacerbation
6.1 Introduction
6.2 Canalized Irrigation in the Sahara Desert
6.2.1 Ziway´s Canalized Irrigation
6.3 Canalized Irrigation in the Thar Desert of India
6.3.1 The IGNP Command Area Characteristics and Malaria Exacerbation
6.3.2 Transformation in the Thar´s Physiography
6.4 Salutogenesis, Canalized Irrigation in Desert Environment, and Mosquitoes
7: Anopheline Fauna and Major Malaria Vectors of Deserts
7.1 Introduction
7.2 Deserts´ Most Dangerous Malaria Vectors
7.2.1 The Sahara Desert
7.2.2 The Arabian Peninsula Desert
7.2.3 The Middle East/West Asia/Central Asia Deserts
7.2.4 The Great Indian Desert, the Thar Desert
7.3 Bio-Ecology of Anopheline Mosquitoes
7.4 Dispersal
7.5 Succession and Replacement of Taxa
7.6 Density of Anopheline Mosquitoes
7.7 Biting Behaviour and Host Preference of the Anopheline Mosquitoes
7.8 Age Structure of Vector Mosquitoes
7.9 Vector Incrimination Studies
7.10 Major Breeding Habitats of Different Anopheline Species
7.11 Correlation of Canalized Irrigation under National Five-Year Plan of Economy Development with the Malaria Escalation in t...
7.12 Insecticide Usage in Health and Agricultural Programmes and Development of Insecticide Resistance in Vector Species
7.13 Species Complexes in Vectors of the Thar Desert
7.14 Anopheles stephensi-Anopheles culicifacies Distribution-Based Classification of the Thar Desert
8: Anophelenization of the Deserts
8.1 Introduction
8.2 The Phenomenon of Anophelenization
8.3 Chorogeography of Anopheline Mosquitoes
9: Sibling Species Complexes of Malaria Vectors in Major Deserts
9.1 Introduction
9.2 Species Complexes in Deserts
9.2.1 The Sahara Desert
9.2.2 The Middle East/West Asia/Central Asia Deserts
9.2.3 The Thar Desert in India
9.3 The Enigmatic Status of Anopheles stephensi
10: Anopheles stephensi Liston 1901: Origin and Chorogeography-A New Hypothesis
10.1 Introduction
10.2 Classification
10.3 Etymology of Anopheles stephensi
10.4 Distribution
10.5 The New `Out of Range´ Occurrence of An. stephensi Since Early Twenty-First Century
10.5.1 Gulf Countries
10.5.2 Africa
10.5.3 Middle East and West Asia
10.5.4 The Thar Desert
10.6 The Original Desert Mosquito: Anopheles stephensi
10.7 A New Hypothesis on the Origin and Evolution of Anopheles stephensi
10.7.1 The Hypothesis Based on the Rule of Reinig (1938, 1939)
10.7.2 The Basis
10.7.3 The Evolution and Migration Pathways of New Species or Subspecies to Other Regions
10.7.4 Test of Bergmann´s Rule on the Origin of Anopheles stephensi
11: Invasive Vector Species of Malaria in Desert Environments
11.1 Introduction
11.2 What Makes a Vector Species `Invasive´
11.3 Interplay Between Vector-Pathogen Interaction Dynamics and the Climate Change
11.4 Invasion of Anopheles stephensi Within India
11.5 Invasion of Anopheles stephensi in Sri Lanka
11.6 Invasion of An. stephensi in West Asia/Middle East
11.7 Invasion of An. stephensi in Arabian Peninsula
11.8 Invasion of An. stephensi in Africa
12: Epidemiology of Desert Malaria
12.1 Introduction
12.2 Ecological, Biological and Social Aspects of Malaria Disease in Major Deserts
12.3 Dynamics of Malaria Prevalence in Major Deserts
12.3.1 The Sahara Desert
12.3.2 The Arabian Peninsula
12.3.3 Middle East/West Asia/Central Asia Deserts
12.3.4 The Thar Desert
12.4 Review of Malaria Situation for Individual District Under the Thar Desert
12.5 Possible Factors Responsible for Conflagration of Malaria, Particularly P. Falciparum-Dominated Malaria
12.6 Malaria-Associated Complications or Malaria Syndromes
13: Epidemics of Malaria in Major Deserts
13.1 Introduction
13.2 Malaria Epidemic Modelling
13.2.1 The P. falciparum Infection Model
13.2.2 The Liverpool Malaria Model (LMM)
13.3 Epidemics in Saharan Countries
13.4 Epidemics in the Thar Desert
13.5 Possible Pathways of Evolution of Malaria Epidemics in the Thar Desert
13.6 Early Warning Systems for Epidemic Malaria in the Thar Desert
14: Urban Malaria in the Desert
14.1 Introduction
14.2 Factors Responsible
14.3 Vectors
14.4 Urban Malaria
14.4.1 Sahara Desert
14.4.2 Middle East/Central and West Asia
14.4.3 Thar Desert
14.4.4 Quarry Mine Malaria
14.4.5 Construction Site-Water Storage Pits
14.4.6 Roadside Water Tanks for Cattle/Animal Drinking
14.4.7 Overhead Water Tanks
15: Clinical Scenario of Desert Malaria
15.1 Introduction
15.2 Malaria Clinical Spectrum
15.2.1 Symptoms
15.2.2 Splenomegaly
16: Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts
16.1 Introduction
16.2 Agroeconomical and Social Impacts of Malaria: Paradox about Rice Cultivation in the Irrigated Desert Region and Malaria
16.3 Health Impact of Malaria
16.4 Knowledge, Attitude and Practice of the Rural Population about Malaria in the Thar Desert
17: Vector Identification and Malaria Diagnosis in Major Deserts
17.1 Introduction
17.2 Dichotomous Keys for Identification of Vectors of Malaria in India
17.2.1 Fourth Instar Larvae of Malaria Vectors
17.2.2 Adults of Vector Mosquitoes
17.3 Distinctive Taxonomic Characters of the World´s Two Major Malaria Vectors in Desert Environments, Anopheles stephensi Lis...
17.3.1 Morphological
17.3.2 Chromosomal
17.3.3 Polymerase Chain Reaction (PCR)
17.4 Parasite Diagnosis
17.4.1 Microscopic
17.4.2 Rapid Diagnostic Test
17.5 Clinical Diagnosis
18: Malaria Immunity in Desert Populations and Development of Resistance in Parasites against Antimalarials
18.1 Introduction
18.2 Malaria Endemicity and Immunity Development
18.3 Biology of Malaria Parasites
18.4 Clinical Symptoms and Treatments
18.5 Parasite Resistance against Antimalarials
18.6 Malaria Treatment and Immunity
19: Malaria and Climate Change
19.1 Introduction
19.2 The Sahara Desert
19.3 The Thar Desert
19.3.1 Physical Transformation in the Thar Desert Climate
19.3.1.1 Rainfall
19.3.1.2 Air Temperature
19.3.1.3 Relative Humidity
19.3.2 Malariological Transformation in the Thar Desert Climate
19.3.2.1 Entomological Investigations
19.3.2.2 Parasitological Investigations
19.4 Where Is the Thar Desert Heading to Malariologically under Climate Change
20: Anopheles stephensi: The First Vector to Show an Evolutionary Response to Rapid Climate Change
20.1 Introduction
20.2 The Principle
20.3 The Basis
20.4 Population, Urbanization, Anthropization and Climate Change in the Thar Desert
20.5 Urbanization-Driven Climate Change and Effluxes of Anopheles stephensi from the Thar Desert to In-Country and Extraterrit...
20.6 Conclusion
21: Trans-Border Migration and Malaria in Desert Populations
21.1 Introduction
21.2 Human Movement in Search of Fodder for Cattle
21.3 Malaria Transmission across International Borders
21.3.1 The Saudi-Yemeni Border
21.3.2 The Jordan-Iraq Border
21.3.3 Malaria Status of Countries Bordering India
21.3.4 Ethiopia and Sudan
21.3.5 Border Malaria in the Thar Desert
22: Malaria Management Including Vector Control in Major Deserts
22.1 Introduction
22.2 Malaria Control in the Desert
22.2.1 Sahara and Arab Peninsula Deserts
22.2.2 Malaria Control in the Desert
22.2.2.1 Malaria Control Policy
22.2.2.2 Diagnosis and Treatment
22.2.2.3 Vector Control through Insecticides
22.2.2.4 Biological Control of Mosquitoes
22.3 Research on Phytochemicals as Repellents against Anopheles stephensi from the Thar Desert
22.4 Role of Community and Future Scenario of Malaria Control in the Thar Desert
23: Inventions, Innovations and Discoveries in Malaria in Desert Environments
23.1 Introduction
23.2 Discovery of the First Human Malaria Parasite
23.3 Discovery of Entry of Anopheles stephensi in Africa´s Sahara Desert
23.4 Discovery of `Tanka´ and `Beri´ as the Main Breeding Habitats for Anopheles stephensi in the Thar Desert
23.5 Invention of a `Tanka Lid´
23.6 Invention of a Mechanical Mosquito Sampler (Tyagi Sampler)
23.7 Coining a New Classification System of the Thar Desert Based on the Distribution of Malaria Vectors (Anopheles stephensi ...
23.8 Hypothesis on the Cradle of Anopheles stephensi in the Thar Desert
23.9 Discovery of the Phenomenon of `Self-Immobilization´ in Anopheles stephensi
23.10 Hypothesis on Anopheles stephensi: A Sibling Species Complex
23.11 Discovery of Cerebral Malaria Caused by Plasmodium vivax in Adults
23.12 New Theory on Epidemics in the Thar Desert
24: Future Implications of Desert Malaria in Global Elimination Campaign
24.1 Introduction
24.2 Anthropization and Climate Change: The Major Triggers for Malaria Exacerbation in the Desert
24.3 Excessive Rainfall and Malaria Epidemics in the Thar Desert
24.4 Climate Variability: Impact of El Nino Southern Oscillation on Malaria Conflagration
24.5 The Phenomenon of `Inundative Vectorism´
24.6 Malaria Control in Deserts
25: Conclusion: Will Deserts Transform into Malaria Hotspots Tomorrow?
Glossary
References

Citation preview

B. K. Tyagi

Desert Malaria

An Emerging Malaria Paradigm and Its Global Impact on Disease Elimination

Desert Malaria

B. K. Tyagi

Desert Malaria An Emerging Malaria Paradigm and Its Global Impact on Disease Elimination

B. K. Tyagi VIT University Vellore, India

ISBN 978-981-19-7692-6 ISBN 978-981-19-7693-3 https://doi.org/10.1007/978-981-19-7693-3

(eBook)

# The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Singapore Pte Ltd. The registered company address is: 152 Beach Road, #21-01/04 Gateway East, Singapore 189721, Singapore

Dedicated to My parents and teachers who have always taught me to follow the principle of work:

Transliteration: Karmanye vadhika raste, Ma phaleshu kadachana Ma karma phala he tur bhuh, ma te sangotsva karmanye Translation: You have a right to ‘Karma’ (actions) but never to any Fruits thereof. You should never be motivated by the results of your actions, nor should there be any attachment in not doing your prescribed activities.

Foreword

Taking cognizance of the World Malaria Report 2021 it looks like malaria will be knocked off from most parts of world very soon. There are, however, certain ecotypes where malariated mobile and hard-to-approach populations need special attention, such as those in the malaria-prone deserts of the world, especially the Sahara, the Middle East/West Asia, and the Great Indian Thar Desert whose malariogenic scenario is fast changing under the impact of climate change as well as anthropization, and can affect the neighbouring regions where successful malaria elimination campaigns have been in progress. The global data on morbimortality is a big alert sign in this direction: there were an estimated 241 million cases in 2020, compared to 227 million cases in 2019, with malaria deaths in 2020 having increased to 6,27,000 globally—a 12% increase over that in 2019! After African continent, it is the South-East Asian region, including India which shoulders the heaviest burden of malaria incidence, that poses the greatest threat of malaria burden to people in the region which has recently witnessed some countries having been declared malaria-free by the World Health Organization. India, too, has made a great progress in reducing the malaria cases and resolutely developed ‘the National Framework for Malaria Elimination in India 2016–2030’ which will need to take into consideration with equal alacrity all the various different malaria ecotypes or paradigms including the distantly malariogenic Thar Desert. Accordingly, the future elimination roadmaps will also need to factor in contemporary challenges, including the impact of climate change on vector chorogeography, human migration, rapid urbanization, and expansion of irrigated agriculture. Leveraging advanced control technologies aided by a robust surveillance system to intensify malaria elimination, the time seems to be just ripe to tackle malaria; from grassroot action to holistic policy interventions and effective delivery of services, without letting emerging malaria paradigms such as, for example, ‘the Desert Malaria ’ disappear from the sight while executing the ‘National Strategic Plan for Malaria Elimination’ (2017–22). During the past one decade India has succeeded in reducing the malaria burden a great deal (69%). India was also the only high-endemic nation to see a decrease of 17.6% in 2019 compared to 2018. Further, when numbers of malaria cases are compared between 2019 and 2020 it was revealed that the overall number of malaria cases recorded in 2020 was 1,57,284 as compared to the number of cases in 2019 vii

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being 2,86,091, which is a year-on-year decrease of approximately 45%. Yet, there is no reason for ecstatic celebration for there are many challenges ahead, not to mention the ongoing pandemic which has apparently disrupted other health programmes across the world, and India is no exception; the reduction in malaria cases during the past several months could be potentially correlated with the underreporting of cases, on one hand, and the inability to timely address ‘mobile and hard to approach populations’ in regions such as, for example, the arid environments of the Thar Desert, on the other. Eventually, grassroot action involving as significantly indiscernible risk as that of the desert malaria is critical to combat a disease like malaria. Tackling the desert malaria, in addition to holistic policy interventions and effective delivery of services in endemic areas, would be vital in helping achieve the goal of a malaria-free India by 2030. On the global front, due cognizance should be taken of the fact that desert malaria has immense potential to impact the successful disease elimination campaigns in the bordering areas/regions or countries, and under the irreversible Climate Change the situation will only worsen with the expanding geographical reach of the dangerous invasive mosquito, like Anopheles stephensi, and the parasite, Plasmodium falciparum. Currently desert environments intervened by Climate Change and anthropization are becoming conducive to malaria exacerbation. I wish Prof. B.K. Tyagi’s book, Desert Malaria a great success. The book is an innovative and unique treatment, and yet so vital for our understanding about the complexities associated with the malaria elimination in future. I further wish that all those who are personally or institutionally involved in the drive against malaria, such as policy makers, programme implementers, disease managers, academicians, and researchers alike, will find this book a useful reference in their endeavours to eliminate the disease from the face of the Earth once for all! Parasitology Department, Universiti Malaya Kuala Lumpur, Malaysia 28th April, 2022

Indra Vythilingam

Preface

The decision to write a book on malaria in deserts, however innovative, exigent, and thought-provoking, was highly challenging and unconventional. The disease is inherently associated with water—in variety and abundance—as a prerequisite, and deserts are but chronically water-deficient, besides other environmental features generally inimical to the development, growth, and survival of both the Plasmodium parasites of human malaria and their anopheline mosquito vectors. The fact, however, is that deserts’ inhospitable and inimical arid environments the world over are fast transforming under the impact of climate change and/or anthropization, and becoming home for continued malaria exacerbation and epidemics so much that antimalaria campaigns elsewhere could be put to danger of reversal by increased malaria cases. The threat of ‘Desert Malaria’ (Tyagi 1995) is indeed very real. Therefore, highlighting malariological significance of deserts has proved a pathbreaking endeavour, to say the least! It is, of course, common thinking that deserts are not the places where malaria exists. If not seriously attended, the ‘Desert Malaria’ may become a good reason to ultimately undermine the global efforts to eliminate malaria in a timebound manner in the near future. Globally, according to the World Malaria Report 2021, there were an estimated 241 million cases in 2020, increasing from 227 million in 2019. During the same time malaria deaths increased by 12% globally in 2020, in comparison to 2019, to an estimated 6,27,000. For India, the numbers are grim. In 2020, the South-East Asia Region (SEAR) had 5 million estimated cases. Three countries accounted for 99.7% of the estimated cases in the region, with India being the largest contributor (82.5%). India also accounted for 82% of all malaria deaths in the SEAR. Malaria control is a global issue and the World Health Organization through its member states is committed to eliminate the disease from the face of the Earth. The WHO Global Malaria Programme (GMP) is responsible for coordinating WHO's global efforts to control and eliminate malaria. Its work is guided by the ‘Global Technical Strategy for Malaria 2016–2030’ adopted by the World Health Assembly in May 2015 and updated in 2021. As far as the WHO SEA Region, in which India is also included, it is noteworthy that the island nation of Sri Lanka was recently certified malaria-free in 2015, and another country Timor-Leste is in the line of WHO Certification for malaria-free having reported consistently zero malaria cases in 2018 and 2019. Outside the WHO SEA Region, China was also most recently declared malariaix

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free in 2021. India has recently prepared a National Strategic Framework of Malaria Elimination 2016–2030 wherein the northwestern xeric region of the Thar Desert is also included on the basis of recent experiences. Thus, it is more than crystal clear that the desert/xeric environments bearing countries with potential for malaria conflagration, like those in the African Continent and India, face rather greater challenges to eliminate malaria due largely to a continuous reinforcement of cases from a less or infrequently surveyed region for reasons apparent. The real potential of the desert malaria is so far not fully comprehended, and it is doubted if any great success in eliminating malaria would be achievable without growing au fait in this crucial ecosystem. ‘Desert Malaria’, a new coinage in the realms of malariology, is an emerging malaria paradigm, having been reported for the first time in the Thar Desert, northwestern India. Its global impact on disease elimination carries a unique, yet most significant epidemiological, value at a time when the malaria endemic countries across the world are struggling to the skin of their teeth against the man's oldest and deadliest predator, the mosquito, and the centuries-old infection it transmits, i.e. malaria, which is woefully neglected in deserts due to their hostile physiography and inclement environment, on one hand, and, more importantly, the traditional belief that the desert ecosystem has only very low and unstable potential to exacerbate malaria! Generally it is witnessed that countries with endemic malaria invariably lay their entire focus for vector and disease control/elimination on the wellknown epidemiological paradigms such as, for example, tribal malaria, rural malaria, urban malaria, industrial malaria, irrigation malaria, forest malaria, border malaria, etc., and the desertic, xeric, and/or arid environments are often neglected epidemiologically, albeit high potential for outbreaks conflagratory enough to escalate disease burden all over again in the neighbouring areas! Desert environments (including desertic/xeric and arid lands) constitute the most widespread terrestrial biome on Earth covering about 33% of the land areas of the world, and are home to over 20% of the world's population. The book brings up the significance of the emerging new malaria paradigm—The Desert Malaria, in totality, that is, also by highlighting the significance of both the ‘desert fringe’ and the ‘desert oasis’. Malariologically, if not appreciated for their epidemiological potential, these deserts can become difficult habitats for malaria management. The desert malaria is, therefore, an integral constituent of the global disease epidemiology and control. The book unfolds the history of malaria vis-à-vis desert ecosystems, followed by disease exacerbation due to multiple factors chiefly comprising anthropogenic interference. The book reveals how in recent times increase in trade, transportation (of all kinds), and migration as well as the cyclic droughts in the world’s xeric ecosystems, on one hand, and the impending climate change and anthropization, on the other hand, have led to wide and distant spread of both the vectors and the disease into the vast stretches of deserts. It also informs on reasons behind the emergence of the deadly malaria parasite, Plasmodium falciparum, in the desert ecosystem following faulty canalized irrigation. This is for the first time that all the three different types of disease paradigms, viz., (1) Desert Malaria per se, (2) Desert Oasis Malaria,

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and (3) Desert Fringe Malaria, have been treated in one volume, with fundamental differences in their eco-bio-social impacts in conjunction with malariological significance. It is hoped that this book, written authoritatively, on Desert Malaria: an emerging malaria paradigm and its global impact on disease elimination, will add new knowledge on malaria, and deserts would be given their due share of thinking about eliminating malaria in India and the world alike. Vellore, India 30th April, 2022

B. K. Tyagi

Acknowledgements

A book on malaria in desert or arid environments may appear quixotic but the reality is that it is the most burning topic today in the realms of malariological science, enshrined with a multidisciplinary treatment. My research work on ‘Desert Malaria’, a theory propounded in 1995, is a fabulous journey of perseverance and application chronicled in a series of approximately 200 research publications in national and international journals like The Lancet, Journal of Arid Environments, Phytomedicine, Indian Journal of Medical Research etc. Many colleagues from the ICMR-Desert Medicine Research Centre, Jodhpur, Regional Remote Sensing Centre, Central Arid Zone Research Institute, Arid Forest Research Institute, and Zoological Survey of India facilitated my malariological explorations in the highly challenging, and yet so mesmerizing, Thar Desert. To colleagues particularly such as, for example, Dr S.P. Yadav, Dr K.V. Singh Verma, Dr S.K. Bansal, Dr Raman Sachdev, Dr Ramnath Takiar, and Dr P.K. Dam I remain ever so indebted for assisting me in both the laboratory and the field. For permission to use figures from their publications my heartfelt gratitude goes to a large number of friends and colleagues particularly Dr Vas Dev, Ex-Scientist 'G', ICMR-National Institute of Malaria Research, New Delhi, India; Dr Solomon Kibret, Ecosystem Management, School of Environmental and Rural Science, University of New England, Armidale NSW 2351, Australia; Dr Marianne Sinka, Department of Zoology, University of Oxford, Zoology @ Plant Sciences, South Parks Road, Oxford, OX1 3RB, United Kingdom; Dr Farah Ishtiaq, Principal Scientist, Tata Institute of Genetics and Society (TIGS), Bangalore, India; Dr Natacha Protopopoff, Department of Parasitology, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium; and Prof. Dr S.N. Surendran, Department of Zoology, Faculty of Science, University of Jaffna, Jaffna, Sri Lanka—who have all generously permitted in writing. Further, I am also deeply indebted to the universal policy of organizations like the World Health Organization, Geneva, Switzerland, to use their material with due acknowledgement which I am respectfully doing herewith. They are all duly cited on appropriate legend of the figure(s) or other places in the book. Above all, my cordial remembrances with heartfelt thanks go to the world-famous malariologist and friend, the late Professor Dr Felix P. Amerasinghe of International Water Management, Colombo, Sri Lanka, who appreciated my malaria research in xiii

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the Thar Desert, remarking, ‘Tyagi is best known internationally among malaria and medical entomology circles for his long years of research into mosquitoes, malaria and irrigated agriculture in the Thar Desert of Rajasthan, India’. His appreciation was my motivation for writing this book on ‘Desert Malaria’. I am extremely grateful to Professor Dr Indra Vythilingam (Parasitology Department, University Malaya, Kuala Lumpur, Malaysia) for writing the Foreword in the book and giving encouragement to me in all my undertakings such as this book. As always in the past, here too, I wish to thank my wife, Ajita, who gave me full freedom of time and discussion so that I could put my whole attention to the accomplishment of this long and meandering journey of characterizing ‘Desert Malaria’. Last but not least I duly thank the publisher Springer Nature, specifically the editorial team for guidance throughout the course of processing this book for publication.

Contents

1

‘Desert Malaria’: An Emerging New Paradigm . . . . . . . . . . . . . . . . 1.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.1 Definition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.2 Malaria Symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.3 Parasites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1.4 Malaria Vectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.2 Deserts, Arid Environments, and Malaria . . . . . . . . . . . . . . . . 1.3 Ecotypes of Malaria in the Desert Environments . . . . . . . . . . . 1.4 Desert-Based Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4.1 The Problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.4.2 Types of Desert-Based Malaria Paradigms . . . . . . . . .

1 1 2 3 3 4 7 9 11 11 13

2

Global vis-à-vis Desert-Driven Malaria . . . . . . . . . . . . . . . . . . . . . 2.1 Global Malaria Scenario . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2 Desert-Driven Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1 Malaria in African Sahara Desert . . . . . . . . . . . . . . . 2.2.2 Malaria in Arabian Peninsula Desert . . . . . . . . . . . . 2.2.3 Malaria in the Middle East/Central and West Asian Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4 Malaria in the Great Indian Thar Desert . . . . . . . . . .

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19 19 20 20 21

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21 22

3

World Deserts: Environments and Malaria Potential . . . . . . . . . . 3.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2 Desert Environments, Man, and Malaria . . . . . . . . . . . . . . . . 3.3 Deserts with Potential to Exacerbate Malaria . . . . . . . . . . . . . 3.3.1 Sahara Desert and Malaria . . . . . . . . . . . . . . . . . . . 3.3.2 Arabian Peninsula Desert and Malaria . . . . . . . . . . . 3.3.3 The Great Indian Thar Desert and Malaria . . . . . . . .

. . . . . . .

41 41 42 47 49 49 51

4

Desert Water Sources and Vector Adaptation . . . . . . . . . . . . . . . . . 4.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2 Traditional Sources of Water in Deserts . . . . . . . . . . . . . . . . . 4.2.1 Lakes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2.2 Oases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

75 75 76 76 76 xv

xvi

Contents

4.2.3 4.2.4 4.2.5 4.2.6 4.2.7 4.2.8 4.2.9 4.2.10 4.2.11

Desert Fringes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Springs, Well, and Seasonal Streams . . . . . . . . . . . . . Wadi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Fossil Water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Petro Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Aquifers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Canals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Snowfall in the Sahara Desert: A New and Rare Source for Water . . . . . . . . . . . . . . . . . . . . . . . . . . .

80 81 83 83 83 84 85 85 86

5

‘TANKA’ and ‘BERI’: The Most Crucial Habitats for Breeding of Anopheles stephensi and Emergence of “DESERT MALARIA” in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 5.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 5.2 Wetlands and Sources of Potable Water . . . . . . . . . . . . . . . . . 90 5.3 ‘Tanka and ‘Beri’: Most Significant Malariogenic Habitats in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 5.3.1 ‘Tanka’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 5.3.2 Beri . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99 5.4 Microclimates of ‘Tanka’ and ‘Beri’ . . . . . . . . . . . . . . . . . . . . 101

6

Extensive Canalization and Its Impact on Transformation of the Thar Desert and Malaria Exacerbation . . . . . . . . . . . . . . . . . . . . . . 6.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6.2 Canalized Irrigation in the Sahara Desert . . . . . . . . . . . . . . . . 6.2.1 Ziway’s Canalized Irrigation . . . . . . . . . . . . . . . . . . . 6.3 Canalized Irrigation in the Thar Desert of India . . . . . . . . . . . . 6.3.1 The IGNP Command Area Characteristics and Malaria Exacerbation . . . . . . . . . . . . . . . . . . . . . 6.3.2 Transformation in the Thar’s Physiography . . . . . . . . 6.4 Salutogenesis, Canalized Irrigation in Desert Environment, and Mosquitoes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

7

Anopheline Fauna and Major Malaria Vectors of Deserts . . . . . . . . 7.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2 Deserts’ Most Dangerous Malaria Vectors . . . . . . . . . . . . . . . 7.2.1 The Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . . 7.2.2 The Arabian Peninsula Desert . . . . . . . . . . . . . . . . . . 7.2.3 The Middle East/West Asia/Central Asia Deserts . . . . 7.2.4 The Great Indian Desert, the Thar Desert . . . . . . . . . . 7.3 Bio-Ecology of Anopheline Mosquitoes . . . . . . . . . . . . . . . . . 7.4 Dispersal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7.5 Succession and Replacement of Taxa . . . . . . . . . . . . . . . . . . . 7.6 Density of Anopheline Mosquitoes . . . . . . . . . . . . . . . . . . . . .

103 103 103 103 105 108 109 114 115 115 116 116 118 119 120 123 133 134 135

Contents

7.7 7.8 7.9 7.10 7.11

7.12

7.13 7.14

xvii

Biting Behaviour and Host Preference of the Anopheline Mosquitoes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Age Structure of Vector Mosquitoes . . . . . . . . . . . . . . . . . . . . Vector Incrimination Studies . . . . . . . . . . . . . . . . . . . . . . . . . Major Breeding Habitats of Different Anopheline Species . . . . Correlation of Canalized Irrigation under National Five-Year Plan of Economy Development with the Malaria Escalation in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . Insecticide Usage in Health and Agricultural Programmes and Development of Insecticide Resistance in Vector Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Species Complexes in Vectors of the Thar Desert . . . . . . . . . . Anopheles stephensi-Anopheles culicifacies Distribution-Based Classification of the Thar Desert . . . . . . . .

138 139 141 141

142

145 146 146

8

Anophelenization of the Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . 8.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8.2 The Phenomenon of Anophelenization . . . . . . . . . . . . . . . . . 8.3 Chorogeography of Anopheline Mosquitoes . . . . . . . . . . . . .

. . . .

149 149 149 150

9

Sibling Species Complexes of Malaria Vectors in Major Deserts . . 9.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9.2 Species Complexes in Deserts . . . . . . . . . . . . . . . . . . . . . . . 9.2.1 The Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . 9.2.2 The Middle East/West Asia/Central Asia Deserts . . . 9.2.3 The Thar Desert in India . . . . . . . . . . . . . . . . . . . . . 9.3 The Enigmatic Status of Anopheles stephensi . . . . . . . . . . . .

. . . . . . .

157 157 158 158 158 160 165

10

Anopheles stephensi Liston 1901: Origin and Chorogeography—A New Hypothesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.2 Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.3 Etymology of Anopheles stephensi . . . . . . . . . . . . . . . . . . . . . 10.4 Distribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.5 The New ‘Out of Range’ Occurrence of An. stephensi Since Early Twenty-First Century . . . . . . . . . . . . . . . . . . . . . . . . . . 10.5.1 Gulf Countries . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.5.2 Africa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.5.3 Middle East and West Asia . . . . . . . . . . . . . . . . . . . . 10.5.4 The Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.6 The Original Desert Mosquito: Anopheles stephensi . . . . . . . . 10.7 A New Hypothesis on the Origin and Evolution of Anopheles stephensi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10.7.1 The Hypothesis Based on the Rule of Reinig (1938, 1939) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

169 169 171 172 172 173 174 174 174 175 178 179 179

xviii

Contents

10.7.2 10.7.3 10.7.4 11

12

13

The Basis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179 The Evolution and Migration Pathways of New Species or Subspecies to Other Regions . . . . . . . . . . . 181 Test of Bergmann’s Rule on the Origin of Anopheles stephensi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 184

Invasive Vector Species of Malaria in Desert Environments . . . . . . 11.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.2 What Makes a Vector Species ‘Invasive’ . . . . . . . . . . . . . . . . 11.3 Interplay Between Vector-Pathogen Interaction Dynamics and the Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11.4 Invasion of Anopheles stephensi Within India . . . . . . . . . . . . . 11.5 Invasion of Anopheles stephensi in Sri Lanka . . . . . . . . . . . . . 11.6 Invasion of An. stephensi in West Asia/Middle East . . . . . . . . 11.7 Invasion of An. stephensi in Arabian Peninsula . . . . . . . . . . . . 11.8 Invasion of An. stephensi in Africa . . . . . . . . . . . . . . . . . . . . . Epidemiology of Desert Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.2 Ecological, Biological and Social Aspects of Malaria Disease in Major Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.3 Dynamics of Malaria Prevalence in Major Deserts . . . . . . . . . . 12.3.1 The Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . . 12.3.2 The Arabian Peninsula . . . . . . . . . . . . . . . . . . . . . . . 12.3.3 Middle East/West Asia/Central Asia Deserts . . . . . . . 12.3.4 The Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.4 Review of Malaria Situation for Individual District Under the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12.5 Possible Factors Responsible for Conflagration of Malaria, Particularly P. Falciparum-Dominated Malaria . . . . . . . . . . . . 12.6 Malaria-Associated Complications or Malaria Syndromes . . . . Epidemics of Malaria in Major Deserts . . . . . . . . . . . . . . . . . . . . . . 13.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.2 Malaria Epidemic Modelling . . . . . . . . . . . . . . . . . . . . . . . . . 13.2.1 The P. falciparum Infection Model . . . . . . . . . . . . . . 13.2.2 The Liverpool Malaria Model (LMM) . . . . . . . . . . . . 13.3 Epidemics in Saharan Countries . . . . . . . . . . . . . . . . . . . . . . . 13.4 Epidemics in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . 13.5 Possible Pathways of Evolution of Malaria Epidemics in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13.6 Early Warning Systems for Epidemic Malaria in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

187 187 188 189 191 192 193 194 194 197 197 198 198 199 205 206 206 212 224 228 233 233 234 234 235 236 238 248 249

Contents

xix

14

Urban Malaria in the Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.2 Factors Responsible . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.3 Vectors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.4 Urban Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.4.1 Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.4.2 Middle East/Central and West Asia . . . . . . . . . . . . . . 14.4.3 Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14.4.4 Quarry Mine Malaria . . . . . . . . . . . . . . . . . . . . . . . . 14.4.5 Construction Site-Water Storage Pits . . . . . . . . . . . . . 14.4.6 Roadside Water Tanks for Cattle/Animal Drinking . . . 14.4.7 Overhead Water Tanks . . . . . . . . . . . . . . . . . . . . . . .

255 255 255 256 256 256 257 257 258 260 261 261

15

Clinical Scenario of Desert Malaria . . . . . . . . . . . . . . . . . . . . . . . . . 15.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15.2 Malaria Clinical Spectrum . . . . . . . . . . . . . . . . . . . . . . . . . . . 15.2.1 Symptoms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15.2.2 Splenomegaly . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

263 263 264 264 265

16

Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16.2 Agroeconomical and Social Impacts of Malaria: Paradox about Rice Cultivation in the Irrigated Desert Region and Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16.3 Health Impact of Malaria . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16.4 Knowledge, Attitude and Practice of the Rural Population about Malaria in the Thar Desert . . . . . . . . . . . . . . . . . . . . . .

17

Vector Identification and Malaria Diagnosis in Major Deserts . . . . 17.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.2 Dichotomous Keys for Identification of Vectors of Malaria in India . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.2.1 Fourth Instar Larvae of Malaria Vectors . . . . . . . . . . . 17.2.2 Adults of Vector Mosquitoes . . . . . . . . . . . . . . . . . . . 17.3 Distinctive Taxonomic Characters of the World’s Two Major Malaria Vectors in Desert Environments, Anopheles stephensi Liston (1901) and Anopheles arabiensis Patton (1905) . . . . . . . 17.3.1 Morphological . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.3.2 Chromosomal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.3.3 Polymerase Chain Reaction (PCR) . . . . . . . . . . . . . . . 17.4 Parasite Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.4.1 Microscopic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17.4.2 Rapid Diagnostic Test . . . . . . . . . . . . . . . . . . . . . . . . 17.5 Clinical Diagnosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

271 271

271 273 280 285 285 285 286 291

296 297 297 298 299 299 299 299

xx

18

19

20

Contents

Malaria Immunity in Desert Populations and Development of Resistance in Parasites against Antimalarials . . . . . . . . . . . . . . . . . 18.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18.2 Malaria Endemicity and Immunity Development . . . . . . . . . . . 18.3 Biology of Malaria Parasites . . . . . . . . . . . . . . . . . . . . . . . . . 18.4 Clinical Symptoms and Treatments . . . . . . . . . . . . . . . . . . . . . 18.5 Parasite Resistance against Antimalarials . . . . . . . . . . . . . . . . 18.6 Malaria Treatment and Immunity . . . . . . . . . . . . . . . . . . . . . . Malaria and Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.2 The Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.3 The Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.3.1 Physical Transformation in the Thar Desert Climate . . . 19.3.2 Malariological Transformation in the Thar Desert Climate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19.4 Where Is the Thar Desert Heading to Malariologically under Climate Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Anopheles stephensi: The First Vector to Show an Evolutionary Response to Rapid Climate Change . . . . . . . . . . . . . . . . . . . . . . . . 20.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20.2 The Principle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20.3 The Basis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20.4 Population, Urbanization, Anthropization and Climate Change in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20.5 Urbanization-Driven Climate Change and Effluxes of Anopheles stephensi from the Thar Desert to In-Country and Extraterritorial Regions . . . . . . . . . . . . . . . . . . . . . . . . . 20.6 Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. . . .

301 301 302 302 304 304 306 307 307 309 310 310 311 320 323 323 324 325

. 327

. 329 . 331

21

Trans-Border Migration and Malaria in Desert Populations . . . . . . 21.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.2 Human Movement in Search of Fodder for Cattle . . . . . . . . . . 21.3 Malaria Transmission across International Borders . . . . . . . . . 21.3.1 The Saudi-Yemeni Border . . . . . . . . . . . . . . . . . . . . . 21.3.2 The Jordan-Iraq Border . . . . . . . . . . . . . . . . . . . . . . . 21.3.3 Malaria Status of Countries Bordering India . . . . . . . . 21.3.4 Ethiopia and Sudan . . . . . . . . . . . . . . . . . . . . . . . . . 21.3.5 Border Malaria in the Thar Desert . . . . . . . . . . . . . . .

333 333 334 334 336 336 337 337 337

22

Malaria Management Including Vector Control in Major Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22.2 Malaria Control in the Desert . . . . . . . . . . . . . . . . . . . . . . . . . 22.2.1 Sahara and Arab Peninsula Deserts . . . . . . . . . . . . . . 22.2.2 Malaria Control in the Desert . . . . . . . . . . . . . . . . . .

345 345 347 347 347

Contents

22.3 22.4 23

24

25

xxi

Research on Phytochemicals as Repellents against Anopheles stephensi from the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . 352 Role of Community and Future Scenario of Malaria Control in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354

Inventions, Innovations and Discoveries in Malaria in Desert Environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.2 Discovery of the First Human Malaria Parasite . . . . . . . . . . . . 23.3 Discovery of Entry of Anopheles stephensi in Africa’s Sahara Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.4 Discovery of ‘Tanka’ and ‘Beri’ as the Main Breeding Habitats for Anopheles stephensi in the Thar Desert . . . . . . . . . . . . . . . 23.5 Invention of a ‘Tanka Lid’ . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.6 Invention of a Mechanical Mosquito Sampler (Tyagi Sampler) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.7 Coining a New Classification System of the Thar Desert Based on the Distribution of Malaria Vectors (Anopheles stephensi and An. culicifacies) . . . . . . . . . . . . . . . 23.8 Hypothesis on the Cradle of Anopheles stephensi in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.9 Discovery of the Phenomenon of ‘Self-Immobilization’ in Anopheles stephensi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.10 Hypothesis on Anopheles stephensi: A Sibling Species Complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.11 Discovery of Cerebral Malaria Caused by Plasmodium vivax in Adults . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23.12 New Theory on Epidemics in the Thar Desert . . . . . . . . . . . . . Future Implications of Desert Malaria in Global Elimination Campaign . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24.2 Anthropization and Climate Change: The Major Triggers for Malaria Exacerbation in the Desert . . . . . . . . . . . . . . . . . . . . . 24.3 Excessive Rainfall and Malaria Epidemics in the Thar Desert . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24.4 Climate Variability: Impact of El Nino Southern Oscillation on Malaria Conflagration . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24.5 The Phenomenon of ‘Inundative Vectorism’ . . . . . . . . . . . . . . 24.6 Malaria Control in Deserts . . . . . . . . . . . . . . . . . . . . . . . . . . .

355 355 355 357 357 358 358

360 361 362 362 362 363 365 365 366 368 369 370 371

Conclusion: Will Deserts Transform into Malaria Hotspots Tomorrow? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 373

Glossary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 381 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 389

‘Desert Malaria’: An Emerging New Paradigm

1.1

1

Introduction

Malaria is an age-old vector-borne disease that is transmitted to humans by mosquitoes belonging to the genus Anopheles (Bruce-Chwatt 1985; Sharma et al. 2020). It is numero uno among all the nearly 400 infections transmitted by the arthropod vectors in terms of morbimortality as well as its social, psychological, and economic impacts (Tyagi 2003a, b, 2004a, b). It not only affects health but also emaciates economy, enfeebles communities, and saps off affected nations’ intelligentsia (Sinton 1936; Tyagi 1992a, b; Hay et al. 2004). Malaria’s ferocity in both time and space is widely regarded to be responsible for changing the course of human history, for example, deciding the fate of nations in war (e.g., Panama, which still belonged to Colombia until the late nineteenth century, raged a war for independence following which a bitter Civil War erupted between 1900 and 1903 whereafter it finally won the independence) (Spielman and D’Antonio 2001; Tyagi 2020); for felling the great leaders (e.g., Alexander the Great, is believed to have succumbed to the infection by Plasmodium falciparum while returning after the fateful battle against the Indian King, Porus, in Punjab); for terminating ruthless and much dreaded invaders on the Indian soil (e.g., Mohammed Bin Tughluk contracted malaria in 1351 while on a military campaign against rebels and died shortly thereafter. A similar fate is believed to have meted out to Mahmud Ghaznavi who invaded and plundered the Indian temples in Somnath and Mathura, and he too died en route to Ghazni through the Great Indian Thar Desert); for decimating armies (e.g., malaria, together with Yellow Fever and dengue, is regarded to have taken its toll on thousands of US soldiers engaged in an ephemeral Cuban independence war between Spain and the United States of America during the late nineteenth century, and that death from the disease among American troops was much more common than death in war per se from bullets); and for indecisive wars (e.g., the infamous and indecisive US-Vietnam war in the mid-twentieth century, between 1955 and 1975, during which malaria pitched the foreign troops in dire consequences of the

# The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_1

1

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‘Desert Malaria’: An Emerging New Paradigm

One or more indigenous cases Zero cases in 2018–2019 Zero cases in 2019 Zero cases (³3 years) in 2019

Certified malaria free after 2000 No malaria Not applicable

Fig. 1.1 World map showing countries with indigenous cases in 2000 and their status by 2019. Countries with zero indigenous cases over at least the past 3 consecutive years are considered to have eliminated malaria. In 2019, China and El Salvador reported zero indigenous cases for the third consecutive year and have applied for WHO certification of malaria elimination; also, the Islamic Republic of Iran, Malaysia, and Timor-Leste reported zero indigenous cases for the second time. (Source: WHO 2020, auto-permitted with due acknowledgement in the book)

infection, and even singularly stood responsible for aborting the war with total withdrawal of the US soldiers from Vietnam). Malaria is currently vastly limited to tropical and subtropical countries, but more prominently in Africa, South Asia, and Latin America (Maurice and Pearce 1987; Greenwood 1999; WHO 2020) (Fig. 1.1). Malaria is a global disease but the poorest countries of the world have been suffering from it most, with Sub-Saharan African (SSA) nations bearing the highest burden of both disease prevalence and deaths (90%), followed by the South-East Asian countries (May 1951; MAP 2020). Though initially malaria remained predominantly a rural problem, it has recently begun impacting the urban agglomerations with equally serious repercussions. Interestingly, malaria has recently extended its occurrence even in a least expected, water scarce and inimical environment such as that of the desert, which is a new paradigm for malaria as well as a serious issue in our efforts to eliminate malaria globally (Baeza et al. 2011, 2013; Tyagi 2002).

1.1.1

Definition

Malaria (məˈlɛːrɪə) is defined as an intermittent and remittent infectious disease caused by protozoan parasites from the Plasmodium family, which is mainly transmitted by the bite of the Anopheles mosquito, besides by way of contaminated needles or blood transfusion, mostly in tropical and subtropical countries.

1.1 Introduction

1.1.2

3

Malaria Symptoms

Malaria is characterized by high fever, chills, and other flu-like symptoms. The infection can eventually lead to kidney failure, seizures, confusion, coma, and, in the worst cases, death. Symptoms of malaria primarily include the classic cycles of high fever, followed by sweat and finally chills that recur every few days, which may be joined by nausea and vomiting, abdominal pain, fatigue, rapid breathing, rapid heart rate, cough, general feeling of discomfort or muscle or joint pain, and headache. People who fall sick due to malaria usually feel very weak with a high fever and shaking chills. The sickened people may also experience coughing, vomiting, diarrhoea, and yellowing (jaundice) of the skin and eyes. On the other hand, those persons who are affected with severe falciparum-malaria can develop bleeding or haemorrhagic manifestations, shock, kidney and liver failure, central nervous system problems, coma, and, if not timely attended medically, even die. After an infected mosquito bite to a healthy man, signs and symptoms of the malaria disease typically begin within a few weeks. In some types of malaria parasites such as Plasmodium vivax, or more particularly P. malariae, however, the pathogen can lie dormant in the body for months to a year or even more. Among the many names for malaria are ague, jungle fever, marsh or swamp fever, paludism, and, in Hindi, ‘durvāta’ (= दरवात) or ‘sheet-jwar’ (शीत-जवर). Indian literature of yore has several irrefutable references to both malaria and various different types of mosquitoes involved in the transmission of malaria and other maladies to man (Satvalekar 1958; Rao 1984; Kaur and Singh 2017; Tyagi 2020).

1.1.3

Parasites

Although there are over 200 species known under the genus Plasmodium Marchiafava and Celli, 1885, and as many as 11 are known to infect humans (Igweh 2012), only five of the following species of Plasmodium are responsible for human malaria (Cox Francis 2010), viz., 1. 2. 3. 4. 5.

Plasmodium falciparum (Welch 1897) Plasmodium vivax (Grassi and Feletti 1890) Plasmodium ovale (Stephens 1922) Plasmodium malariae (Feletti and Grassi 1889) Plasmodium knowlesi (Sinton and Mulligan 1932)

Of all these parasites, P. vivax and P. falciparum are more common; the former being more dominant in Asia and the latter in Africa where it inflicts about 90% of the population, most of them children below 5 years and pregnant women. Plasmodium falciparum, also known as malignant malaria parasite, differs from the rest of the parasites mainly in the fact that it affects human brain or nervous system, with eventual death if not treated medically in time (Guerra et al. 2008). Plasmodium vivax, too, is dangerous since the benign fever caused by it usually relapses, with

4

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‘Desert Malaria’: An Emerging New Paradigm

severe complications to follow. Both these malaria forms are, however, treatable through a range of antimalarials under strict medical advice. The malaria parasite completes its asexual phase of life cycle in the human host and sexual phase in the anopheline mosquito. Fundamental details about malariology have been explained by Bruce-Chwatt (1985). To reduce malaria infections, the national health programmes across the world distribute preventive drugs and insecticide-treated bed nets to protect people from mosquito bites. Personal, self, or private medication as presumptive treatment without a proper prescription must be avoided. A reasonably effective vaccine, RTS,S/AS01 (RTS,S), world’s first malaria vaccine, after being piloted for several years in a few African countries, is now available for vaccination on a limited scale. Further, in October 2021, the WHO for the first time recommended the large-scale use of a malaria vaccine for children living in areas with moderate-to-high malaria transmission in certain endemic countries in Africa. There is no vaccine for travellers yet. Therefore, travellers to areas with malaria are advised to take medications to prevent infection, if exposed. The treatment of malaria is with oral or intravenous medications, under strict medical care.

1.1.4

Malaria Vectors

Tropical countries are typically characterized by both richness and endemism of the anopheline taxa, with preponderance of species diversity ever growing toward the equator (Foley et al. 2007). Therefore the countries like Brazil, Indonesia, Malaysia, and Thailand surpass others in the species quantum and densities, although Brazil tops the list of the countries in exhibiting the highest taxonomic output and number of type locations. Further, countries like Brazil, Australia, the Philippines, Indonesia, Panama, French Guiana, Malaysia, and Costa Rica do not only boast of the highest numbers of endemic mosquito species but also the highest densities of total species and endemic species. Interestingly, 50% of mosquito species occurring worldwide, i.e., approximately 2000 species, are endemic to these countries. Among all the nations with highest species densities as well as when compared to the continental mainland countries of similar size, the island nations have characteristically both the higher total number of species and higher endemic species. As far as deserts are concerned, very low number of mosquito species and fragmentary publications have been brought on record, possibly due to lesser sampling efforts and/or species abundance. This is probably the reason that the taxonomic output was lowest for some desertic countries, such as those located in Africa, Arabian Peninsula, and the Middle East desertic regions; the Thar Desert in the north-western State of Rajasthan (India) being the only possible exception (Tyagi 2002; Anon. 2006). Of the nearly 3600 species of mosquitoes worldwide (precisely 3606 extant taxa of Culicidae as of now on July 6, 2022) in the three subfamilies: Toxorhynchitinae (Toxorhynchites), Culicinae (Aedes, Culex, Mansonia, Armigeres), and Anophelinae (Anopheles), there exists a total of 465 formally recognized Anopheles species in addition to more than 50 unnamed members of species complexes such as Anopheles

1.1 Introduction

5

Fig. 1.2 Zoogeography of vector species for malaria across the world’s different regions. (Source: Available in public domain at http://www.cdc.gov/malaria/about/biology/mosquitoes/map.html)

culicifacies, An. subpictus, An. fluviatilis, and An. annularis (Sinka 2013; Manguin 2013). Of the many species included in these subfamilies, only a subset of approximately 70 species have been confirmed to have the capacity to transmit parasites of human malaria (Service and Townson 2002), and 41 are considered to be primary or dominant vector species (DVS)/species complexes, capable of transmitting malaria at a level of major concern to public health (Hay et al. 2010a, b). They are present in all regions of the world, mostly in the tropics and the subtropics. Maximum vector species occur in Asia. Region-wise dominant vector species (DVS) are discussed below (Sinka 2013), albeit actual quantum of potential vector species might be much higher for each of the regions (Fig. 1.2).

1.1.4.1 The Americas The American continent nations have the lowest P. falciparum morbidity (PfPR210 ≤ 5%) when compared with the nations of other regions. High quality of vector control/management throughout the entire region for a long time has been the major factor behind the decreased morbidity and mortality in the North American nations, in particular. There are nine dominant vector species in the Americas: (i) (ii) (iii) (iv) (v)

An. albimanus An. albitarsis complex An. aquasalis An. darlingi An. freeborni

6

(vi) (vii) (viii) (ix)

1

‘Desert Malaria’: An Emerging New Paradigm

An. marajoara An. nuneztovari complex An. pseudopunctipennis An. quadrimaculatus complex

1.1.4.2 Africa Considering Africa’s gargantuan and variable landscape and ecosystem, there is a corresponding variability in the intensity of malaria transmission (Hay et al. 2000, 2005). The Sub-Saharan region is not only the world’s most malarious area with highest morbidity and mortality but also the home for highest global P. falciparummalaria transmission levels (Fontenille and Simard 2004; Hay et al. 2010a, b). Anopheles gambiae, the deadliest mosquito on our planet, is a member of the An. gambiae complex, which also contains other dominant vector species such as An. arabiensis, An. Merus, and An. melas. In addition, and importantly enough, An. funestus subgroup consisting of another highly effective vector An. funestus is also widely found in Africa. It is of course worth mentioning here that An. funestus is possibly the first species in the subgroup to adapt to make use of humans as a food/ blood source. Still, An. moucheti, a vector much limited in both density and distribution but highly anthropophilic in nature, and An. nili complex of comparatively more widespread species further reinforce the strength of vectors within Africa. All these vectors, primary or secondary in nature, are highly efficient in malaria transmission. Their control is equally difficult primarily owing to the yet unnamed species under complexes, on the one hand, and varying behavioural attributes, on the other. Following are the more dominant vectors in Africa: (i) (ii) (iii) (iv) (v) (vi) (vii)

An. arabiensis An. funestus An. gambiae An. melas An. merus An. moucheti An. nili complex

1.1.4.3 Asia-Pacific The Asia-Pacific is one of the most prosperous regions in the world as far as the biodiversity of vector species, species complexes, and suspected species complexes is concerned. Many of these species complexes occur sympatrically (i.e., species occurring in the same geographical range without loss of identity from interbreeding sympatric species or the taxa occurring between populations that are not geographically separated sympatric speciation) and manifest a great degree of fluctuation in behaviour or behavioural plasticity (Sinka et al. 2011). This complexity, and the taxonomic ambiguity of many of the dominant vector species (DVS) of the region, is a major contributing factor to the continuing impact of malaria in this area. With 39% of the global malaria burden (estimated clinical cases of P. falciparum malaria only), southeastern Asia is second only to Africa in suffering with malaria, with

1.2 Deserts, Arid Environments, and Malaria

7

pockets of medium to high endemicity found in Orissa and some of the seven-sister States in the northeast India, western Myanmar, and the lowlands of New Guinea. India alone shares 41.9% of the global population at risk of P. vivax transmission which is quite worrisome. The Asia-Pacific region harbours 19 DVSs (i.e., 46.4% of totally 41 Dominant Vector Species recognized globally). Of these at least 10 are now considered as species complexes. The phenotypic and genotypic complexities of the vector biology in the Asian-Pacific region escalates the problems associated with our understanding of the vector/disease transmission environment which is integral to control programmes. The Asia-Pacific region outnumbers DVSs in all other regions in the world. The region houses far greater number of species complexes and taxonomic complexities than anywhere else (vide infra). (i) (ii) (iii) (iv) (v) (vi) (vii) (viii) (ix) (x) (xi) (xii) (xiii) (xiv) (xv) (xvi) (xvii) (xviii) (xix)

1.2

An. aconitus An. annularis An. balabacensis An. barbirostris complex An. culicifacies complex An. dirus complex An. farauti complex An. flavirostris An. fluviatilis complex An. koliensis An lesteri An. leucospyrus/latens An. maculatus (group) An. minimus complex An. punctulatus complex An. sinensis complex An. stephensi An. subpictus complex An. sundaicus complex

Deserts, Arid Environments, and Malaria

Malaria is still the deadliest vector-borne disease of great public health significance transmitted by infected female Anopheles mosquitoes which breed in aquatic habitats, stagnant or slowly streaming fresh or salty water which is a prerequisite for the development of the larval stages (Shayo et al. 2021; Getachew et al. 2020; Mwakalinga et al. 2018). Therefore, the billion dollar question that springs up naturally is: “Can malaria occur in the desert environments?” Zahar (1990a, b) first highlighted the significance of “Desert Fringes” and “Desert Oases” in the transmission of malaria among local desert populations, and also the neighbouring

8

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‘Desert Malaria’: An Emerging New Paradigm

areas. Long-term investigations into risk of malaria exacerbation in the light of extensive canalized irrigation in the Thar Desert by Tyagi (1995a, b, 1996a, b, c, d, e, f, g, 2002, 2003a, b, 2004a, b, 2020, 2021), Tyagi et al. (1995), and Tyagi and Chaudhary (1997) founded for the first time an irrefutable malariological significance of the desert ecosystems and their impact on exacerbation of the disease in the neighbouring areas where malaria control campaigns were in progress and the risk of resurgence of disease transmission occurred. In general, people associate malaria with the regions where surface water is abundantly present in some form. However, in addition to surface water, prevalence of malaria depends mainly on climatic factors such as temperature, humidity, and rainfall. Factors such as temperature and humidity are particularly critical, though significance of rainfall cannot be underestimated especially in Desert Fringe areas where wide epidemics of malaria generally follow heavy downpour. Malaria, particularly Plasmodium falciparum (a deadly parasite which causes severe malaria)malaria, thrives in tropical and subtropical countries because the environment there is highly favourable for the development of both the vector and the parasite, implying that (1) Anopheles mosquitoes, which must live for a minimum of 7 days on an average, can survive and multiply prodigiously, and (2) malaria parasites can complete their growth cycle in the mosquitoes (“extrinsic incubation period”). It is noteworthy here that the deadly malaria parasite, Plasmodium falciparum, is unable to complete its growth cycle in the Anopheles mosquito below 20 °C or 68 °F. On the other hand, Plasmodium vivax, which is more tolerant of lower ambient temperatures may be prevalent seasonally in cooler regions. Besides temperature, humidity and rainfall, factors such as the altitude may also impact transmission. It is for this reason that malaria is generally not reported in high altitude areas for the want of any anopheline, leave aside a vector, mosquito. Thus, even within tropical and subtropical areas, transmission will not occur (1) in colder seasons in some areas, (2) frozen lands, (3) in deserts (save for the Sahara, the Thar, etc.), and (4) in many temperate areas, such as western Europe and the United States, economic development, improved housing conditions, and public health measures through successful control/elimination programmes have succeeded in interrupting transmission and thereby eliminating malaria. However, most of these areas, parts of which existing as buffer zone for both malaria vectors and parasites, have Anopheles mosquitoes that can transmit malaria, and reintroduction of the disease is a constant risk. It is a well-known fact that malaria is more intense and transmitted year-round in warmer regions closer to the equator, and the most glittering examples to this rule are (1) the Sub-Sahara Desert where the highest perennial transmission occurs in Africa, and (2) in parts of Oceania such as Papua New Guinea where following a steady decline in cases till 2014, the scenario almost catapulted and cases increased over tenfold from 50,309 in 2014 to 646,648 in 2019. In cooler regions, transmission will be less intense and more seasonal. As far as deserts are concerned, one naturally does not associate malaria with a water-deficient habitat. Common sense dictates that mosquitoes, which breed only in stagnant and/or slowly flowing ground water, would give arid environments a wide

1.3 Ecotypes of Malaria in the Desert Environments

9

go-by. But that is not the case with some hot deserts in Asia and Africa where malaria vectors abundantly breed due largely to the long-time impacts of climate change, anthropization (human-driven environmental changes), and, above all, canalized irrigation in an attempt to develop agro-economy and general living standards of the local folks. However, these interventional vicissitudes transformed deserts into the lands of persistent malaria due mostly to water mismanagement (Tyagi 2002)! Some deserts present a highly precarious and transitional stage of evolution such as the Namib where the biological diversity apparently is in a clash of sea and land, and fog and dust (Barnard 1998). Deserts constitute a unique ecosystem in our planet, the Earth. Though much of the various different hot deserts still continue to preserve the antiquitous nature, i.e., deficient precipitation, high temperature, low humidity, sand storms, and fauna and flora with features adapted to hostile xeric conditions, yet at least some of these or their parts have undergone a major change in their physiography and transformed into a semiarid environment conducive enough to cultivate new and high-yielding agriculture due largely to canalized irrigation with a humongous network such as the world famous Indira Gandhi Nahar Pariyojana (IGNP) running across the Thar Desert in the northwestern India (Bhandari 1978; Malhotra 1988). Resultantly, in the Thar Desert, malaria drifted from an autochthonous nature in the penetralium of the leveed xeric ecosystem to a persistently fulminating epidemic malaria in the irrigated desert and neighbouring non-desert lands.

1.3

Ecotypes of Malaria in the Desert Environments

Malaria being local and focal in character, control programmes need to stratify their malaria problem into a number of smaller units, keeping in mind the variability of malaria. Such stratification may be based on the epidemiology of malaria or on its determinants such as ecology and disease transmission capacity of vectors (Schapira and Boutsika 2012a, b). An ecotypic classification comprising eight major malaria paradigms to categorize typical disease transmission settings was developed by the World Health Organization around 1990 (WHO 1993a, b), as follows: 1. 2. 3. 4. 5. 6. 7. 8.

Malaria of the African Savannah Forest malaria Malaria associated with irrigated malaria Highland fringe malaria Desert fringe and oasis malaria Urban malaria Plains malaria Seashore malaria

Malaria being local and focal infection in nature, the type of ecosystem (e.g., physiographically clearly earmarked, in transitional or mixed zones) determines a lot of its attributions, e.g., distribution over a biogeographical region or even subregion.

10

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‘Desert Malaria’: An Emerging New Paradigm

Globally malaria is associated with a melange of ecotypes, and the intensity of occurrence of the disease can be high or low or fluctuating depending on a particular set of few or all of these ecotypes. The first-hand local information on ecology, topography, physiography, bio-socio-cultural, anthropic, and health system processes, including malaria control, is essential to comprehend the nature of malaria epidemiology for a specific ecotype or set of ecotypes. Ecotyping malaria is of paramount significance and needs to be executed in the outset to determine desired control interventions. Therefore, ecotyping of a malarious area should be done for early weaving of a framework, rather than used as a shortcut, to supplement available epidemiological and entomological data so as to assess malaria situations at the local level, think through the particular risks and opportunities, and reinforce intersectoral action. Cognizance of these facts implies that several biogeographic regions’ ecotypic distinctions are not only well defined but also serve as a guiding force for implementing control campaigns with a certain degree of certitude and success. For example, forest environments in the Indo-Myanmar, Indo-Malay, and the Neotropics are, with a few exceptions, associated with much higher malaria risk than in adjacent areas. Within India, Dev (2022) has recently highlighted high risk of malaria transmission in the North-East states rife with sylvatic environments where the vectors are difficult to control, affected populations are difficult to approach, and the anthropic factors, such as population movements across the state as well as international borders, also often converge to impose constraints in delivering primary and/or emergency health care whichever necessary. Another burning example in India is the emerging urban malaria which is a serious risk, along with rural malaria intruding deeper into ecosystems hitherto known to be terra incognito for malaria (e.g., Thar Desert). In Africa, on the other hand, the malaria scenarios presented by urban agglomerations in both the Sahara Desert (SD) and the Sub-Saharan Desert (SSD) regions has so far been associated with lower risk. Urban malaria is, however, more rampart in the savannas south of the Sahara Desert. While in Africa no specific vector control is defined save for the facultative larval control on ad hoc basis, in the Indian subcontinent, in contrast, where urban malaria transmitted by An. stephensi is associated with higher risks than most adjacent rural areas, malaria vector control is implemented by a well-defined, though not exclusive, larval control methodology using chemical, biological, and/or environmental methods. Since all ecotypes do not pose the same set of challenges in controlling malaria, the field research on malaria and ecology should be interdisciplinary, especially with geography, and pay more attention to juxtapositions and to anthropic elements, especially migration (Schapira and Boutsika 2012a, b). As far as deserts are regarded, three major malaria paradigms exist currently: (1) Desert Fringe Malaria, (2) Desert Oasis Malaria, and (3) Desert Malaria per se. Malaria transmission in the desert is dependent on availability of surface water and associated increase in humidity. Anopheles arabaiensis is the main vector in the Sahara and the Arabian Peninsula deserts, while in the Great Indian Thar Desert and the Middle East it is An. stephensi which is the predominant desert species for malaria transmission. Although, both these vectors are highly adaptable to dry conditions, An. stephensi has recently invaded many countries which were hitherto

1.4 Desert-Based Malaria

11

a terra incognito for the mosquito (e.g., Sri Lanka and some nations in African Sahara)! Following are the identified characteristics associated with each of the three ecotypes: (i) Desert Fringes—These areas are located on warm low land areas, and experience abnormally heavy rainfall causing flooding which almost always gives rise to malaria epidemics. (ii) Desert Oasis—Malaria in oases is characterized by transmission of malaria limited to spring and autumn seasons when both temperature and humidity are suitable, and the transmission usually occurs in abnormal years with very long periods or heavy rain fall. (iii) Desert Malaria—This is a very peculiar state of affairs, i.e., ‘The Desert Malaria’, which has emerged in the traditionally water-deficient arid environment characterized by two different types of underground water conservation and/or harvesting processes, i.e., ‘Tanka’ and ‘Beri’—the sole factors behind indigenous and/or autochthonous round-the-year malaria mediated by An. stephensi, at the penetralium of the Thar Desert, though at a low ebb. The ‘Desert Malaria’ paradigm was explained for the first time by Tyagi (1995a; also see Tyagi 2002, 2020) and Tyagi et al. (1995). Thus, the list of malaria ecotypes earlier offered by the WHO (1993a, b) now extends to nine with the inclusion of ‘Desert Malaria’. It is emphasized here that arid environments in the Thar Desert of northwestern India are associated with unstable malaria with potential for occasional epidemics; the principal and original vector An. stephensi is difficult to control owing largely to its combined phenotypic and genotypic plasticity (Chakraborty et al. 2021), and the anthropic factors such as highly preferred water storage habit due to shortage of water supply which clearly pose operational constraints (Tyagi and Yadav 1996a, b, c; Tyagi 2002).

1.4

Desert-Based Malaria

1.4.1

The Problem

Since the early times of the Global Malaria Eradication Programme (GMEP), it had been understood that malaria, unlike several other vector-borne diseases, was essentially a local and focal problem, and a single panacea of “one size fits all” for the selection of appropriate interventions would not work in all the highly varying paradigms. A good deal of emphasis was, however, laid on developing a reconnaissance of their malaria epidemiology supported with maps on the intensity of parasite transmission, dominant vectors’ distribution, population settlements, rivers, dams, and agricultural areas and practices, etc. (WHO 1956; Pampana 1969). Although national malaria control agencies of different endemic countries independently followed different plans and developed their own maps and templets without uniform set of information, the information secured on the basis of the association between rainfall duration and malaria seasons, altitude, proximity to breeding sites,

12

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‘Desert Malaria’: An Emerging New Paradigm

and occasionally supported by empirical observations of incidence and prevalence of malaria provide a solid foundation to frame a roadmap for future action (Gemperli et al. 2006; Craig et al. 2007). Coupled with this, risk maps prepared in course helped the national control agencies grow au fait in their knowledge toward malaria epidemiology and generated important national atlases, with particular context to malaria cartography across much of Africa and India, to guide disease control (Languillon 1957; Christophers and Sinton 1926; Covell 1949). When the regional control agenda shifted from one of preventing infection to treating fevers in the 1970s, the map developing science and effort was brought to back-bench. This is for this reason that thereafter malaria risk maps were rarely developed for desert regions and tailored to address national control programme ambitions. The result was as catastrophic as the devastating resurgence of malaria in India between 1965 and 1976, following a phenomenal success in bringing down the malaria cases below one million and no death in mid-1960s (Akhtar et al. 1977). However, the eradication campaign faltered and malaria seemed to have diffused from the less cared low endemic areas as well as hard to reach populations such as the areas normally arid (Desert Malaria), semi-arid (Desert Oasis Malaria), or only moderately humid (Desert Fringe Malaria) which seemed to have played a crucial role in diffusing with those hyperendemic where control process had been focused. The much disquieting increase was from over five million in 1976 to ten million in the first 9 months of 1977. Therefore, malaria associated to desert environments carries a great epidemiological significance particularly to retain benefits of disease control in neighbouring hyperendemic zones or regions since malaria is a focal disease whose epidemiology is affected by human, vector, parasite, and environment (Ranjha and Sharma 2021). Deserts being considered generally as regions harbouring low malaria intensity are at risk of exclusion from the national focus to eliminate the disease with the same force of attention as practiced in hot malaria zones. However, such negligence might prove costly soon after achieving success in the hyperendemic and epidemic prone hot regions as possibly occurred in mid-1960s when India had reported less than one million cases without any death due to malaria (Sharma and Mehrotra 1986). It is noteworthy that soon after the spectacular, though ephemeral, success malaria had resurged with a vengeance and by 1970s hit an unbelievable mark of 10 million cases with several hundreds of people succumbing to the savagery of the infection. With this catastrophe a set of new operational constraints also emerged prominent among which was development of resistance in Anopheles vector species against insecticides used in antimalaria programme, e.g. DDT, HCH, and malathion, and in Plasmodium parasites against antimalarials of choice such as chloroquine. That a low endemic region like the Thar Desert could threaten to generate new malaria cases across far off states like Punjab, Haryana, Gujarat, Madhya Pradesh, Delhi, and Uttar Pradesh was not understood and valued significantly until Tyagi (1995a, b) and Tyagi et al. (1995) exposed its vulnerability to malaria exacerbation with potential to cyclic epidemics due to irreversible and gargantuan anthropization (human-driven environmental changes), including an extensive canalized irrigation system—one of the world’s largest of its kind in a xeric ecosystem, and the changing climate (Bouma

1.4 Desert-Based Malaria

13

and van der Kaay 1995). All the Desert Malaria ecotypes (i.e., Desert Malaria, Desert Oasis Malaria, and Desert Fringe Malaria) have been regularly threatening to stall, or even revert, the progress in eliminating malaria by nations and the world alike. It is, therefore, important to understand the characteristics of each of these ecotypes harbouring potential for malaria conflagration.

1.4.2

Types of Desert-Based Malaria Paradigms

To date only three ecotypes of malaria have been identified. Each of these three ecotypes make a different malaria paradigm being evolved in altogether different sets of eco-bio-social settings. Each of the ecotype is associated with a kind of malaria with different intensity and periodicity. Their vector composition is also more or less specific.

1.4.2.1 Desert Oasis Malaria The Sahara Desert, lying between Sub-Saharan Africa (where Plasmodium falciparum malaria is highly endemic and causes major morbimortality) and the northernmost zone along the Mediterranean Sea (where malaria was eliminated decades ago, except intermittent exotic cases), is acknowledged as the greatest of all deserts in the world rife with oases of variety. Desert oases are usually not considered when one thinks of major malarious areas (Bogreau et al. 2019). In contrast, oases in the Sahara Desert are the main agro-ecologic environments suitable for malaria transmission. In fact, oases may offer excellent conditions for the transmission of malaria in hot deserts where malaria vectors such as An. arabiensis (in Africa) and the Thar Desert (in India) exist. There are many factors for malaria transmission in the oases, which is generally low, but the essential factors, i.e., man, mosquito and parasite always exist. Extrafactorial characteristics in oases like geographical, climatological and epidemiological conditions, which differ from other localities, permit malaria to occur in desert oases which are on the increase in deserts to meet with the ever growing vital needs for human sustenance. For example, the number of oases in the Adrar region of Mauritania alone grew from 31 in 1984 to 75, which is 140%, in 2012, due mainly to the development of hydroagricultural projects. Unfortunately only fragmentary and grossly incomplete information is available on oasis malaria in the Sahara, despite the potential risk for malaria transmission projected by these special water reservoirs in the desert (Bernabeu et al. 2012; Deida et al. 2019). It has been, therefore, often advocated that regular monitoring of malaria in the Saharan zone, including in other oases, should be implemented. The oases consist of isolated areas of vegetation, normally palm trees, generally arranged in long, relatively narrow, broken lines with a well-defined orientation, e.g., eastwestern direction in Libya’s Fezzan Province oasis in the Sahara Desert. Oases are generally most thickly inhabited (Goodwin and Paltrinieri 1959). The houses of the oases, being largely of rural character (i.e., social and economic patterns), are of two types;

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‘Desert Malaria’: An Emerging New Paradigm

(i) Houses in Large Oases: Therein adobe bricks and palm branches are respectively used to make walls and roof, covered in mud plaster. (ii) Houses in Outlying Oases: Only palm branches are generally used to construct these. Oases occur where the water table is sufficiently near to the surface to support the growth of date palms, and to permit digging of shallow wells to supply water for consumption by man and his domestic animals. The wells also supply water for irrigation of barley, alfalfa, and a few vegetables. The climate of oases is generally arid with rain falling at rare intervals. As in the case of Fezzan of Libya where the rainy season is from March to May with variation in rainfall from 0.5 inch to 4.0 inch over a period of 5 years, it varies in most other cases of the deserts. The relative humidity ranges from 10 to 45%. Temperature range is very wide from -9 °C to 55 °C. Oases’ inhabitants, drawn by the better opportunities of commerce and business, often migrate periodically to the coastal cities. Many of these oases have been important trade centres, and, though motorable passages are often noticed currently (four-wheel drive vehicles fitted with special equipment), the old system of transportation through camel (‘the desert ship’) caravans is still much in vogue due to their availability round the clock. Some oases, particularly those celebrating the harvesting season of date palm fruit every year during June–August in the Sahara Desert, are also the site of increasing tourism by thousands of Mauritanians. In recent past even long distance movers such as thousands of migrants from Sub-Saharan Africa on their way to Maghreb countries (countries in North Africa bordering the Mediterranean Sea) and Europe have been using these oases as a transit zone. Evidences from oases in African Sahara and Indian Thar deserts show occurrence of the two most important human malaria parasites, viz., Plasmodium vivax and P. falciparum; the latter being more common in approximately 3:1 ratio in the Sahara Desert’s Libya and 2:3 ratio in the Thar Desert. In a study carried out in the oasis city in Mauritania, Plasmodium ovale was microscopically detected in 10/154 patients (6.5%), although subsequent PCR results discarded as wrongly identified instead of P. vivax infections (Deida et al. 2019). Plasmodium malariae, P. ovale, and P. knowlesi have never been reported from the Thar Desert, although they are occasionally encountered in the Sahara desert. In the past, incidence of malaria has not been high and epidemics have been rare. Malaria in the oases would probably increase if some type of control was not in effect. When the farmers of oases had abandoned their farms and migrated to other greener areas for the benefit of their cattle, the abandoned dug wells and other sources of irrigation resulted in an increase of suitable breeding sources for anopheline mosquitoes and a probable increase in the transmission of malaria, even epidemics. The anopheline fauna may differ from oases of one region to those in others. Thus, while Anopheles multicolor and An. sergenti are prevalent in Libya’s oasis, it is feared that the deadly desert mosquito, An. arabiensis, possibly along with several others, might get introduced in Mauritania sheerly on account of the recently constructed national highway that connects Rachid oasis to Atar. In India the

1.4 Desert-Based Malaria

15

major malaria vector perennially present is An. stephensi, although other species, including An. culicifacies and An. subpictus among others, are also present in some parts of the year (Tyagi 1995a, b, 2002, 2020).

1.4.2.2 Desert Fringe Malaria Of all the three malaria paradigms or ecotypes known to the world, i.e., desert fringe, desert oasis and desert per se, the largest surface area is occupied by the desert fringes which are the home for millions of people around the tropics in Africa, Asia, and South America. Desert fringes are best known for seasonal and epidemic malaria under the impact of marginal environmental conditions in which both the development of the parasite and the population dynamics of the Anopheles mosquito vector are favoured (Roy et al. 2015). Due to heavy seasonal rains in the desert fringe areas both humidity and temperature are almost optimum and good enough to trigger malaria epidemics in warm semi-arid (desert-fringe) and high altitude (highlandfringe) epidemic risk areas. As such there is no rainfall in the desert fringe areas for most part of the year, which, aided by the temperature limit, tends to preclude the population growth of the vector and the parasite’s development within the vector, but the sudden onset of climate variability brought about by heavy downpour renders the ecotype the highest potential to strongly impact disease dynamics. 1.4.2.3 Desert Malaria ‘Desert Malaria’, a new malaria paradigm, originated in the Thar Desert (Tyagi 1995a, b; Tyagi and Chaudhary 1996; Tyagi et al. 1995). The emerging ecotype is of immense epidemiological significance, especially when focus for control of malaria is put on high endemic ecotypes in close approximation, both in context with national malaria elimination campaign and other countries particularly in Middle East/West Asia, Arabian Peninsula, and the African continent with deserts where ‘Tanka’, etc., exist and either a species like An. stephensi is already occurring there or has in recent years made incursions to exacerbate malaria situation (Zahar 1985, 1990b; Tyagi 1995a, b, 1996a, b, c, d, e, f, 2002, 2004a, b, 2020; Tyagi et al. 1995; Sinka et al. 2010, 2012, 2020, Sinka 2013; Manguin 2013). The Thar Desert is comparatively a young desert. It ranks 20th among deserts in the world as far as size is concerned and ninth largest hot subtropical desert when weather conditions dominated by temperature is regarded. During the integrated and undivided times it was wholly limited within the Indian mainland; however, after the partition of the country in 1947 about 90% of the Thar Desert is located in India, while only less than 10% falls in Pakistan. The Thar Desert is about 4.56% of the total geographic area of India. It originally comprised 11 desert districts which later increased to 12 in the 1990s. Known for unstable malaria with potential for occasional outbreaks of malaria, the Thar Desert did not have any canal-based irrigation system nor there was a perennial river, albeit seasonal Ghaggar river which however disappears halfway into the desert. The only long-time water resources were the man-made ‘Tanka’ and “Beri’, the underground engineering feats to conserve water for meeting out vital needs for sustenance as well as limited agriculture, with the help of seasonal ponds and tube-wells.

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Anopheles stephensi, the only desert mosquito specialized to breed in these underground water storing systems, was adapted to the Thar Desert’s inclement environment and continued multivoltine life throughout the year. Malaria among desert folks was P. vivax-dominated, with negligible cases of P. falciparum which further used to conflagrate during either severe droughts when desert populations resorted to migration particularly in search of fodder for their cattle and other pet animals or rare heavy downpours and excessive ground breeding sites were formed. Till the 1920s there was no canal-based irrigation in the Thar Desert and only An. stephensi predominated the desert. Three major canal systems came in succession in the Thar Desert north-southwardly; Gang Canal (Year 1928, with its 1251 km of distribution system within Sri Ganganagar only, covering 300,000 ha of cultivable land), Bhakra-Sirhind Feeder canal (Year 1955, having a 1219 km distribution system irrigating another 300,000 ha of cultivable land), and the Indira Gandhi canal (previously known as Rajasthan Canal Project, Year 1958; total length 649 km), with first waters flowing only in 1957 and the Canal being fully operative in 1961), to be expanded in three stages to cover a major part of the arid environments. It covers 445 km in length and 45 km in width the area of the Thar Desert in the northwest of Rajasthan. Of all the three canal systems, the Indira Gandhi Nahar Pariyojana (IGNP) is the most important, embodying nearly 10,000 km network of distributaries, when fully operative (by now its network is only 547 km). The First Stage was completed as per the time schedule, but the Second Stage, though largely operative, could be also mostly completed on time; but it has created major mosquito breeding sites in the form of seepage resulting in vast swampy areas all along its journey through different desert districts. With the vast areas of ground breeding sites formed, several new species of mosquitoes some of them being vectors (An. culicifacies, An. subpictus etc.), also made their entry in the Thar Desert (Fig. 1.3). It is to be noted here that in spite of massive IGNP in operation, a major part (80%) of the Thar Desert is still unchanged and is existing in its original serenity. Together with An. culicifacies, An. stephensi levied a double impact of disease transmission on the desert populations, now suffering with a P. falciparumdominated malaria (Tyagi and Chaudhary 1996, 1997). After many years of repeated epidemics, the Thar Desert has partially evolved into a hotbed for malarial inferno, and a persistent threat to the adjoining non-desert region in the Rajasthan state or the other hyperendemic states under intensified elimination campaign. While the unchanged and noncanalized Thar Desert predominantly remains a home for An. stephensi and P. vivax, the irrigated part of the Thar Desert has been transformed into a multi-vectorial hotspot for P. falciparum-dominated malaria with strong potential for disease outbreaks and affecting the lands in the neighbourhood. This transformation of the Thar Desert from a meagre region of malaria hypoendemicity to a highly fulminating P. falciparum-dominated ecosystem is an irreversible one-way journey. This implies that the Thar Desert will continue to transform and experience more intensified epidemics in future! Conclusively, the new ecotype, ‘Desert Malaria’, is therefore defined as “a unique paradigm in the penetralium of desert and/or leveed xeric ecosystem which, in

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Fig. 1.3 A graphic representation of unidirectional transformation of the Thar Desert, with “Desert Malaria” in the offing: (A) The Original Thar Desert with only An. stephensi and P. vivax in dominance, (B) The triad of canal systems, topped by Indira Gandhi Nahar Pariyojana (IGNP) in operation, with multi-vector, intensified disease transmission dominated by P. falciparum and intensified outbreaks, and (C) A vector (An. stephensi + An. culicifacies) chorogeography-based classification proposed for malaria in the Thar Desert (Source: Dr. B.K. Tyagi, this work original)

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contrast to ‘Desert Oasis Malaria’ and ‘Desert Fringe Malaria’ ecotypes that are solely dependent on monsoon rains, is humanly created, for example, in the Thar Desert (India) in the first place, as underground water reservoir system either in the belly of a large dry pond (e.g., ‘Beri’) or dug up burrow pit in the ground as a gargantuan dome-shaped water-harvesting system (e.g., ‘Tanka’)—breeding invariably the deadly malaria vector, Anopheles stephensi, responsible for low, indigenous and unstable malaria in the arid environments of the desert with potential for occasional epidemics—for meeting out man’s daily domestic needs for his own survival in the hostile environment without a natural water source, for instance, an oasis, within a radius of tens of kilometres.” This specific type of paradigm, i.e., Desert Malaria, will be extensively dealt with in the following chapters of the book.

2

Global vis-à-vis Desert-Driven Malaria

2.1

Global Malaria Scenario

Malaria is amongst the oldest infectious diseases known to man. Currently malaria is still the most dangerous parasitic disease with the highest morbimortality globally. The history of malaria in humans is as old as man’s own history. For decades now malaria has been considered the most dreadful vector-borne disease that puts globally a massive economic burden (56,200,201 DALYS) (Hay et al. 2017; Breman et al. 2004; Carter and Mendis 2002). Currently, it is one of the major tropical diseases adversely affecting the health of the peoples and the economic development of many developing countries, particularly in sub-Saharan Africa (SSA) and SouthEast Asia. Malaria accounts for 300–500 million cases and up to three million deaths each year throughout the world; of this Africa alone shares more than 90% of the burden since over 80% of malaria deaths occur in Africa, while less than 15% of the deaths occur in Asia and Eastern Europe together; in the latter, 8000 cases of imported malaria are reported every year, the majority of which is due to P. falciparum. Around 90% of them come from sub-Saharan Africa and are mainly diagnosed in newly arrived migrants. Before the dawn of the nineteenth century malaria largely affected rural environments, but with the turn of the twentieth century increased degree of urbanization and immigration into urban settings have resulted in the formation of new cities and metropolises with extensive urban areas buffering with those of agriculture, inveigling mosquito vectors like both An. arabiensis and An. gambiae to maintain malaria transmission with prevalence rates as high as up to 30–40%. Soon after the discovery of the insecticidal/mosquitocidal properties of the dichlorodiphenyltrichloroethane (DDT) during the World War II, it became available as the major plank in the worldwide malaria eradication programmes launched in the 1950s and resulted in the dramatic decrease in the percentage of the world population at risk of the disease from 68% in 1946 to 52% in 1975, albeit an increase in the absolute number of people at risk from 2.1 billion in 1975 to about 3 billion in 2002. Despite several long-term research and control programmes with innovative # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_2

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strategies (such as deployment of Long Lasting Impregnated Bed nets, LLINs) the malaria eradication programme had little success initially in many parts of Africa south of the Sahara where the number of people at risk of malaria escalated to over 74% (about 600 million) at the end of the twentieth century, although the disease dramatically declined in prevalence in Asia, particularly in India (Ranjha and Sharma 2021). Demographic proportions between urban and rural are clearly favouring a steep increase toward the former and these upward demographic changes in the urban centres have important implications for malaria control in future, especially after the invasion of the Asian mosquito vector, An. stephensi—a specialist to breed in urban settings, in many Saharan countries in recent past.

2.2

Desert-Driven Malaria

2.2.1

Malaria in African Sahara Desert

Malaria is a major public health threat to the African continent and its control is critical to achieving the Millennium Development Goals in this region. Although considerable progress has been made to reduce the malaria burden in sub-Saharan Africa by introducing control measures such as the provision of insecticide-treated mosquito nets, indoor residual spraying, and easier access to effective antimalarial drugs, malaria epidemics continue to occur in many areas including some in the Sahara region. Populations in epidemic-prone areas have a poorly developed immunity to malaria and the disease remains life-threatening to all age groups in the desert. The expansive Sahara Desert covers 10 countries fully or partially: Algeria, Chad, Egypt, Libya, Mali, Mauritania, Morocco, Niger, Sudan, and Tunisia. The Western Sahara, a Spanish territory earlier and currently annexed to Morocco, is sometimes considered the eleventh nation. Many of these are already free from malaria and the World Health Organization has certified these countries as free from malaria at present (Algeria in 2019, Libya in 2012, Morocco in 2010, Tunisia in 2012). Malaria has been rampant in Africa south of the Sahara Desert; out of the global estimate of 229 million malaria cases in 2019, about 95% of the burden was shared by 29 sub-Saharan African region countries; majority (51%) being accounted for by only 5 countries, namely, Nigeria (27%), the Democratic Republic of the Congo (12%), Uganda (5%), Mozambique (4%), and Niger (3%). This propensity for hyperendemicity by the Sub-Saharan countries is due largely to preponderance of the major malaria vectors such as An. gambiae, An. arabiensis, and An. funestus. As far as the Saharan region is concerned, An. arabiensis has invaded some of these nations in the past and recently An. stephensi has also crossed over from Middle East, or from the Thar Desert directly via trade, and established in a few countries in the African Sahara, in both rural and urban centres. Some countries such as Ethiopia are not covered fully by any desert, but they still have some part of their land engulfed by the xeric environment of a desert. In case of landlocked Ethiopia, the Danakil Desert (situated in the Afar Triangle, stretching across 136,956 sq. km) swamps a major part of land in north-east Ethiopia, bordering

2.2 Desert-Driven Malaria

21

southern Eritrea and north-western Djibouti. Anopheles arabiensis, a member of the An. gambiae species complex, is the major malaria vector widely distributed in Ethiopia, besides the secondary vectors of malaria with limited distribution, viz., An. funestus, An. pharoensis, and An. nili.

2.2.2

Malaria in Arabian Peninsula Desert

The largest expanse (80%) of desert is spanning Saudi Arabia, and the desert also extends into neighbouring portions of southern Iraq, southern Jordan, central Qatar, most of the Abu Dhabi emirate in the United Arab Emirates (UAE), western Oman, and north-eastern Yemen. Some of these countries like Qatar (central region) (in 2012) and United Arab Emirates (UAE in 2007) were already certified malariafree by the World Health Organization. The Arabian Peninsula is largely free from malaria, although in past the transmission of malaria was governed by the diversity of dominant vectors and extreme aridity. However, in view of the possible presence of a few dominant vectors it is likely that malaria transmission, though limited, occurred across populated areas of most of the present day territories of Saudi Arabia, Kuwait, Qatar, United Arab Emirates (UAE), Bahrain, Oman, and Yemen at the turn of the last century (Snow et al. 2013). Campaigns to eliminate malaria were undertaken in the peninsular region countries since the 1940s but were met with varying degrees of success for next three decades, shrinking malaria transmission across the peninsula. After the 1990s epidemics all the desert national governments began pondering over a unified action throughout the peninsula, which took shape in course of the present global resolve for malaria eradication, and launched a collaborative malaria-free initiative in 2005. Even though this initiative did not succeed completely in eradicating malaria from the peninsula, it helped in further shrinking the malaria risk map. Currently, only Saudi Arabia and Yemen, with the latter contributing to over 98% of the clinical burden, manifest locally acquired clinical cases of malaria.

2.2.3

Malaria in the Middle East/Central and West Asian Deserts

Most of the Middle East region countries (by conventional political definition, the countries in the Middle East are Cyprus, Iran, Iraq, Israel, Jordan, Lebanon, the State of Palestine (West Bank and Gaza Strip), Syria, and the Asian part of Turkey) are malaria-free, as no indigenous cases of infection have been described in recent years. However, imported cases of malaria continue to occur in some of these countries (Al-Awadhi et al. 2021). Large expatriate population originating from malaria endemic countries and/or migrant workforce being employed in Middle East region countries and beyond are considered as a source of influx of imported cases.

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2.2.4

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Malaria in the Great Indian Thar Desert

Since the trend of malaria prevalence in the Thar Desert cannot be fully comprehended in totality without having an understanding of malaria scenario in the country and the state of Rajasthan, it is considered opportune to shed some light first on malaria in India and Rajasthan State. Covell (1927b) critically reviewed the data on transmission of malaria by different species of Anopheles in India, with notes on distribution, habits, and breeding places. Covell (1928) also deeply investigated malaria in Bombay, which set an example for controlling malaria in other fast evolving metropolises under the threat of malaria.

2.2.4.1 Brief History of Malaria in India Malaria has been known to the natives in the country as one of the most devastating diseases for centuries and many Ayurvedic remedies have been prescribed to get rid of these intermittent fevers. In the modern world of science, however, it was only towards the end of the nineteenth century, following the epoch-making discovery of malaria being transmitted by the anopheline mosquitoes (Ross 1897), that great scientific interest was generated in both studying the epidemiology and control as well as transmission dynamics of the disease (Hehir 1927). Many important pieces of taxonomic literature on malaria vector species, both larvae and adults, were produced in the late first and early second half of the twentieth century, notably by Christophers (1933), Puri (1949, 1955, 1960), Wattal (1963), Wattal and Kalra (1961), Rao (1984), and Tyagi et al. (2012, 2014). Indian history of malaria control has been exemplary to the whole world nations with malaria endemicity. Most of the major milestones in the journey of malaria control in India are presented in Table 2.1. Before malaria control programme was launched in India in 1953, nearly 100 million people suffered from the disease annually and close to one million people died every year (Sharma 1986a, b; Sharma and Mehrotra 1986; Tyagi 1994a). The latter figure clearly appears to be a gross underestimate since during frequent epidemics so common in the country during those days the overall number would have been much higher and the number of deaths indirectly or directly resulted from malaria had exceeded two million in 1931 (Sinton 1935). Besides, malaria affected the national as well as individual development as economic losses of the order of Rs. 2936 million per year were forced on India (Ramaiah 1980). Physiographically India is a highly heterogenous country encompassing within its limits a large range of ecosystems, from thousands of kilometers of coastline in the peninsula, spanning plateau in the humongous midland, highlands in north-east as well as central and southern India, dense forests of Eastern and Western Ghats to the sprawling Great Indian Thar Desert in the north-west. Owing to vast ecosystem and environment differences in these topographically varying habitats, generally the mosquito fauna and the malaria vectors, together with malaria endemicity, too differed a great deal. Therefore, epidemiological scenario of malaria differs from state to state, region to region, and ecosystem to ecosystem, and therefore the data of a given area cannot represent the situation in different regions or ecosystems. Although malaria in India is at present drastically controlled (Lal et al. 2000),

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Table 2.1 The milestones in malaria control programme in India (Adapted from free Wikipedia) Year/period Prior to 1940 Prior to 1953 1953 1958 1966 Early 1970s 1971 1976 1977 1984–1998 1995 1997 2005 2006 2008 2009 2009 2010 2016

Event No organized national malaria control programme Malaria cases estimated to be >75 million with 1 million deaths annually National Malaria Control Programme launched National Malaria Eradication Programme launched Cases reduced to less than 0.1 million with nil death Resurgence of malaria Urban Malaria Scheme launched Malaria cases escalated to 6.46, highest in post-DDT era Modified Plan of Operation (MPO) policy formulated and circulated Annual incidence reported within 2–3 million cases Malaria Action Programme World Bank assisted Enhanced Malaria Control Project (EMCP) Global Fund assisted Intensified Malaria Control Project (IMCP) ACT introduced in areas showing chloroquine resistant Falciparum-malaria Revised NVBDCP Drug Policy, extending ACT policy to high risk Pf districts World Bank assisted Project on Malaria Control and Kala-azar Elimination, LLIN introduced Artemisinin monotherapy banned in the country Revised NVBDCO Drug Policy 2010, extending ACT to all Pf cases; Global Fund (Rd. 9) assisted Intensified Malaria Control Project (IMCP- II) National Framework for Malaria Elimination (NFME) 2016–2030

Fig. 2.1 Annual malariometric information (P. falciparum, P. vivax and deaths) in India between 1964 and 2014. (Source: National Vector Borne Disease Control Programme, in public domain)

there is a trend towards increasing proportion of Plasmodium falciparum cases than that in the past (Fig. 2.1). There is also a report from central India showing increase in the proportion of P. falciparum malaria cases (Singh et al. 2000). Correspondingly, Tyagi and Chaudhary (1997) have demonstrated a rising trend of P. falciparum in the Thar Desert.

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Table 2.2 Magnitude of malaria problem in India during pre-eradication period and thereafter (Source: Tyagi 2002) No. of malaria cases per year (in million) 75.0

% of population with malaria per year 21.8

No. of deaths per year 800,000

Period of disease eradication Pre-eradication (estimates based on surveys) During eradication: lowest incidence (after 7 years of eradication operations) During eradication: highest incidence (after 18 years of eradication operation, immediately after the MPO was enacted) During Modified Plan of Operation (after 5 years of MPO-NMEP initiative) After creation of P. falciparum

Year 1947

Population 344.11

1965

487.0

0.1001 (-99.806)

0.02

Nil

1976

613.0

6.4 (-91.46)

1.04

59

1981

657.74

2.70 (-96.97)

0.41

170

1986

737.71

0.24

323

Containment Programme

1991

808.10

0.22

421

One year before Enhanced Malaria Control Project

1994

861.73

1.79 (-97.61) 1.81 (-97.58) 2.51 (-96.65)

0.29

1122

In Table 2.2 is presented the magnitude of malaria problem during pre- and posteradication periods with a view to assess, on the one hand, the grim situation caused by malaria before an organized malaria control campaign, the National Malaria Control Programme (NMCP), was initiated in 1953 and to acquaint with the discernible successes and failures in the ensuing decades with a vengeful comeback of malaria, on the other. Encouraged by the stupendous success of the NMCP, the Government of India stepped up goals and functions of National Malaria Control Programme and it was transformed into National Malaria Eradication Programme (NMEP) in 1958. Soon thereafter malaria cases were reduced to less than 0.1 million in 1965, without single death, and it appeared that malaria would be wiped off from India before very long. It is noteworthy here that decline in cases was in case of P. vivax and not in P. falciparum. Due to utter failure to sustain the success achieved, within the next 10 years malaria epidemics were widespread and the disease, recording the highest ever number of malaria cases (6.47 million) by 1976, invaded even those areas which were earlier unknown for malaria transmission or were once freed from its scourges. Subsequently, during the 1980s and the early 1990s, following a series of critical reviews of the malaria eradication programmes, the malaria incidence was brought down to less than two million in 1995, as reported by the National Malaria Eradication Programme (NMEP). More stringent policies and strategies to reduce

2.2 Desert-Driven Malaria

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Table 2.3 Countrywide epidemiological situation in India (1995–2020) (Source: National Vector Borne Disease Control Programme in public domain) Year 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 2018 2019 2020

Population (in ‘000) 888,143 872,906 884,719 910,884 948,656 970,275 984,579 1,013,942 1,027,157 1,040,939 1,082,882 1,072,713 1,087,582 1,119,624 1,150,113 1,167,360 1,194,901 1,211,580 1,221,640 1,234,995 1,265,173 1,283,303 1,315,092 1,337,617 1,349,006 1,372,316

Total malaria cases (million) 2.93 3.04 2.66 2.22 2.28 2.03 2.09 1.84 1.87 1.92 1.82 1.79 1.51 1.53 1.56 1.60 1.31 1.06 0.88 1.10 1.17 1.09 0.84 0.43 0.34 0.19

P. falciparum cases (million) 1.14 1.18 1.01 1.03 1.14 1.05 1.01 0.90 0.86 0.89 0.81 0.84 0.74 0.77 0.84 0.83 0.67 0.53 0.46 0.72 0.78 0.71 0.53 0.21 0.16 0.12

Pf % 38.84 38.86 37.87 46.35 49.96 51.54 48.20 48.74 45.85 46.47 44.32 47.08 49.11 50.81 53.72 52.12 50.74 49.98 52.61 65.55 66.61 65.53 62.70 48.19 46.36 63.84

API 3.29 3.48 3.01 2.44 2.41 2.09 2.12 1.82 1.82 1.84 1.68 1.66 1.39 1.36 1.36 1.37 1.10 0.88 0.72 0.89 0.92 0.85 0.64 0.32 0.25 0.14

Deaths due to malaria 1151 1010 879 664 1048 932 1005 973 1006 949 963 1707 1311 1055 1144 1018 754 519 440 562 384 331 194 96 77 93

malaria burden were subsequently followed up and by 2020 the incidence is brought to an appreciable low of 0.19 million (Table 2.3, Fig. 2.2). Ironically, the malaria incidence and deaths reported by NMEP were based on the parasitologically proved cases, thus excluded a large number of asymptomatic carriers and/or those who approached other medicinal systems for cure of disease or even resorted to self-medication. As earlier emphasized by the in-depth evaluation of the Modified Plan of Operation (MPO) (NMEP 1985), both morbidity and mortality were apparently underestimated. While the NMEP reported 2.5–3 million malaria cases and about 1000 malarial deaths annually, the WHO South East Asia Regional Office put the estimates to 15 million malaria cases (nearly 6 times) and 19,500 deaths due to malaria (Sharma 1999). Therefore, it appears safer to assume that the malaria incidence reported offers at most the disease trend and not its true incidence, knowledge of which, for logical reasons, is inevitably indispensable for effective implementation of malaria control in the country.

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Global vis-à-vis Desert-Driven Malaria

Fig. 2.2 depicts that the cases have consistently declined from 2.09 million to 0.19 million during 2001 to 2020. Similarly Pf cases have declined from 1.0 to 0.12 million cases during the same period. Less than 2000 deaths were reported during all the years within this period with a peak in 2006 when an epidemic was reported in NE States. The country SPR has declined from 2.31 to 0.19 and SFR has declined from 1.11 in 2001 to 0.12 in 2020. This indicates declining overall endemicity of malaria in the country. (Source: National Vector Borne Disease Control Programme, in public domain)

It can be seen from the above table that although the present epidemiological situation is nowhere near that of 1931, 1947, or 1976, there is nevertheless no room for complacence in view of the rising trend of P. falciparum proportion and heavy mortality in many parts of the country as well as a range of several strategic and operational constraints (Fig. 2.2). Malaria control in India is presently hampered mainly by two reasons: (1) development of drug resistance in malarial parasites, and (2) development of resistance in malaria vectors. Plasmodium vivax and P. falciparum are the dominant species in India, with the former responsible for 60–65% cases and the latter for 35–40% cases (Sharma 1999). Among the six major vector species prevalent in India, An. culicifacies, the main transmitter of rural and peri-urban malaria in the peninsular India, is alone responsible for 65% malaria and 55% P. falciparum annually. This mosquito is resistant to DDT and HCH all over the country, and to malathion in Maharashtra, Gujarat, and certain other States. Anopheles stephensi transmits nearly 12% malaria cases in the country, mostly in the urban and industrial areas. This species, too, has developed multiple resistance against various insecticides, many of which are however used as larvicides. Yet, another vector species, An. fluviatilis, which like the above two species is common in Rajasthan, transmits 15% of total malaria cases and 30% P. falciparum in the country.

2.2 Desert-Driven Malaria

27

The strategy of malaria control in India has been to cause interruption in the disease transmission by spraying residual insecticides in the rural areas (351.8 million population) and by source reduction and larviciding urban areas (62.1 million population) (Dev 2020). Because most of the primary malaria vectors in India are endophilic and/or endophagic in behaviour, indoor residual spraying of insecticides in the rural areas and anti-larval operations in the urban set-ups have been the major means to control malaria in the country. Led by widespread use of DDT in controlling vector population, now largely jeopardized owing to development of resistance in vector mosquitoes, other insecticides like HCH (later banned in 1997), malathion, and certain synthetic pyrethroids such as cyfluthrin, deltamethrin, and lambda-Cyhalothrin have also been selectively employed in the control of malaria, although spray targets were rarely achieved due to logistic and operational constraints. Major anti-malaria activities launched in India since independence can be summed up briefly as follows: (i) National Malaria Control Programme (NMCP): It was launched in 1953 with comprehensive indoor residual spray of DDT. By 1957, 165.7 million people were effectively protected. (ii) National Malaria Eradication Programme (NMEP): The success achieved under the NMCP was so spectacular and encouraging that the Government of India launched National Malaria Eradication Programme, in 1958, with the objective of eradicating the disease from the country (Mehta 1962; Sharma 1967; NMEP - A brief review for professional colleagues. Rajasthan Med J 7: 43-47.NMEP 1985)). This brought down malaria cases to 0.1 million and no deaths due to malaria were reported in the country in 1965. The euphoria of victory, however, proved to be ephemeral as malaria incidence began to escalate in the late sixties owing to multiple factors comprising financial, logistic, administrative and technical constraints, on the one hand, and a feeling of complacency due to a near victory over the disease in the country, on the other. Consequently, malaria resurged with a vengeance and reached its peak in 1976, when about 6.47 million cases of malaria were recorded in the country. The NMEP originally began as a completely centrally sponsored health programme and, till 1979, the entire expenditure on malaria control throughout the country was borne by the Centre. Thereafter, the programme was implemented on a 50:50 cost sharing basis with the States, with the exception of the seven north-eastern States which, from December 1994 onwards, were brought under 100% Central assistance as a special case. All other States in the country, while meeting out the entire operational costs for malaria control as their part of the cost sharing, continued to receive 50% of the costs from the Centre in the form of required equipment and material. The Indian Government spends nearly Rs. 350 crores on malaria control annually. Additionally, the World Bank also recently provided a sum of Rs. 1075 crores for 5 years for the Enhanced Malaria Control Programme.

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(iii) Modified Plan of Operation (MPO): The successes and failures under the NMEP were reviewed in depth and a Modified Plan of Operation was introduced in the year 1977 with three main objectives: (1) prevention of deaths due to malaria, (2) reduction of morbidity due to malaria, and (3) maintenance of industrial and green revolution due to freedom from malaria as well as retention of achievement gained so far. Under the MPO a new strategy was adopted from eradication of malaria to the containment of the disease in the country, i.e., prevention of death and reduction in morbidity due to malaria. As a strategy under this Plan areas with 2 Annual Parasite Incidence (API) or more were earmarked for regular rounds of spray. Surveillance activities in the whole country were decentralized to Primary Health Centres (PHC) along with laboratory services. People’s participation was solicited by involving volunteers in the distribution of antimalarials through Drug Distribution Centres (DDC) and Fever Treatment Depots (FTD). Malaria control in urban areas (>40,000 population) is carried out under the Urban Malaria Scheme (UMS) of the NMEP, launched in 1971–1972. This led to significant reduction in malaria incidence in the country to a level of around two million cases by 1987 for nearly one decade. Since 1994, however, focal outbreaks of malaria have been continuously reported from different parts of country, particularly the north-eastern States and the Thar Desert region in Rajasthan State in the north-west India. This unwarranted situation resulted in resurgence of malaria, generally pronounced by P. falciparum dominance, as well as deaths due to malaria in the country. (iv) Plasmodium falciparum Containment Programme (PfCP): The P. falciparum problem attained new dimensions when a focus of chloroquine resistant strain was discovered in Assam in 1973. Subsequently, new foci of chloroquine resistance were traced in different north-eastern States, Orissa, Madhya Pradesh, Maharashtra, Rajasthan, etc. This situation led to the creation of PfCP in 1977 to tackle the rising threat of P. falciparum. (v) Malaria Action Programme Based on Expert Committee Report - 1995: An expert committee that took cognizance of the fact of availability of appropriate technologies for control of malaria in different epidemiological situations or paradigms in the country attributed the various setbacks in malaria eradication programme, particularly recurrence of periodic epidemics and high mortality, to various different imminent factors like the administrative indifference, the organizational weakness, the low prioritization to malaria under the health services and apathy of middle-level and peripheral workers in the states. Accordingly, the Expert Committee recommended intensification of malaria control activities throughout the country with focus on high risk areas through an integrated malaria control strategy, with the following mentioned components: (1) Early case detection and prompt treatment, (2) Selective vector control, (3) Promotion of personal protection methods, (4) Early detection and containment of epidemics, (5) Information, education and communication towards personal prevention and community participation, and

2.2 Desert-Driven Malaria

(vi)

(vii)

(viii)

(ix)

(x)

(xi)

29

(6) Institutional and management capacity building, trained manpower development, and efficient management information system. Enhanced Malaria Control Project (EMCP): It was launched in September 1997 with the help of World Bank assistance and covered, in addition to 19 towns in 10 States, 62.2 million high risk tribal population living in 100 districts and 1045 PHCs of the seven major States, viz., Andhra Pradesh, Bihar, Gujarat, Madhya Pradesh, Maharashtra, Orissa, and Rajasthan. These PHCs, with a tribal population of more than 25%, had contributed 65.5% malaria cases and 78.6% P. falciparum cases in 1997. The benefits of the programme are conceived to reach other malaria endemic areas as well since the strengthening of the components of the Information, Education and Communication (IEC), trained manpower development and Management Information System (MIS) covers the whole country. Roll Back Malaria (RBM): In January 1998 the World Health Organization proposed Roll Back Malaria initiative taking into consideration large-scale morbidity and mortality due to malaria in developing countries and also observing the changing epidemiological scenario, and the experience of the past control efforts. The basic concepts of the RBM initiative are not different from the existing control strategy in India, but it lays more emphasis on social mobilization, intersectoral collaboration, effective partnerships, strengthening of Primary Health Care, investment in development of effective methods of control, shaping of existing tools by operational research and it is expected that this will result in sustained reduction in disease burden by the year 2010 (Alnwick 2000). National Anti-Malaria Programme (NAMP): Eradication concept was changed to Anti-Malaria Programme and, thus, the programme was once again renamed as National Anti-Malaria Programme (NAMP). National Vector Borne Disease Control Programme (NVBDCP): The vertical anti-malaria control programme transformed into a horizontal one with the establishment of a wide spectrum National Vector Borne Disease Control programme (NVBDCP) in 2003 for synchronizing efforts to control/eliminate six vector-borne diseases. It was erected as an umbrella programme for prevention and control of malaria and other vector-borne diseases viz., Lymphatic Filariasis, Kala-azar, Japanese Encephalitis, Chikungunya, and Dengue with special focus on the vulnerable groups of the society namely, children, women, scheduled castes (SC), and scheduled tribes (ST). The Global Fund to Fight AIDS, Tuberculosis, and Malaria (GFATM): It is an international financing and partnership organization that aims to “attract, leverage and invest additional resources to end the epidemics of HIV/AIDS, tuberculosis and malaria” to support attainment of the Sustainable Development Goals established by the United Nations. Founded in 2005 it aims to extend support and additional inputs in 106 districts of 10 states. World Bank Assisted Project on Malaria Control & Kala Azar Elimination (2008)

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(xii) National Framework for Malaria Elimination (2016–2030) & Integrated Vector Management (IVM) 2016 were launched to provide a roadmap to eliminate malaria from India (Nema et al. 2020). (xiii) Operational Manual for Malaria Elimination: It was launched in 2016. (xiv) National Strategic Plan (2017–2022) for Malaria Elimination by 2030: It was launched in 2017. (xv) Mosquito & Other Vector Control Response (MVCR): It was launched in 2020. (xvi) National Centre for Vector Borne Diseases Control (NCVBDC): The longstanding Directorate of NVBDCP was recently rechristened as National Centre for Vector Borne Diseases Control (NCVBDC) in 2021.

2.2.4.2 Malaria Situation in Rajasthan State Contrary to the common belief that Rajasthan State being largely a desert area embodies but a little chance of persistent malaria in the State, there exists certain areas with considerable patches of hyper-endemicity which for known reasons had been experiencing incessant episodes of focal and/or widespread epidemics involving huge morbidity and deaths (Tyagi 1994a, 1995a; Shukla et al. 1995; Anon. 2001; Bose 2004). However, the overall impression of the state has been that of a non-problematic area with few focal outbreaks here and there (Sharma 1986a, b; Anon. 1987a). In Rajasthan, the morbidity and mortality trends due to communicable diseases including malaria were highlighted by Chandra (1981). Based on malaria endemicity, Sharma et al. (1996a, b) have classified Rajasthan being covered under following two zones; (i) Zone or Stratum II, signifying moderately refractory areas with high epidemic potential (i.e., eastern plains and southern forested and mountainous districts of Rajasthan State), and (ii) Zone III, signifying nonrefractory areas with moderate to high epidemic potential (i.e., western and northern districts of Rajasthan State, including whole of the Thar Desert). It is interesting to note that in last nearly two decades the physiography of the Thar Desert, in particular, has undergone such a major change that the zoning of the region needs a re-characterization for its epidemiological potential (Tyagi 1995a, 1996a, b, c, d, e, f). Under prevailing grim circumstances, the malaria transmission dynamics in Rajasthan State particularly the Thar Desert region requires a serious thinking to be able to device appropriate control methodologies (Tyagi and Chaudhary 1996, 1997; Sharma et al. 1996a, b; Sharma 1996a, b, 1998, 1999). A careful review of the malariometric data reveals it all (Table 2.4). To understand the dynamics of malaria prevalence over the years in Rajasthan and the impact of ‘Desert Malaria’ on its malaria prevalence, it is considered worthwhile to briefly organize the entire richness of malaria research in three periods of time, as follows:

Year 1961 1962 1963 1964 1965 1966 1967 1968 1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1979 1980 1981 1982 1983 1984 1985

Population (×000) 17,562 18,785 19,048 20,917 22,001 22,454 23,040 23,850 24,670 25,320 25,850 26,510 26,715 27,560 27,560 28,031 29,104 29,670 31,092 31,594 32,491 33,113 33,583 34,124 34,655

Blood slides collected 669,202 943,159 1,779,180 2,200,707 2,212,563 1,863,401 1,772,313 1,661,789 1,485,220 1,741,741 2,184,134 5,037,069 2,233,100 2,694,698 3,186,044 3,578,216 3,318,120 3,260,421 3,515,605 4,208,295 3,992,445 3,284,810 3,161,396 2,901,731 3,037,182

Blood slides examined 595,176 1,082,815 1,743,916 2,184,182 2,183,592 1,857,961 1,763,870 1,659,286 1,471,587 1,736,028 2,174,281 2,215,322 2,162,576 2,688,624 3,062,207 3,572,281 3,318,120 3,226,710 3,515,605 4,208,295 3,991,672 3,284,810 3,161,396 2,901,731 3,037,182

Positive cases 8494 3210 3813 3164 2872 9680 23,898 14,999 15,487 79,788 109,773 82,517 118,012 177,596 354,567 412,776 231,862 154.549 83,394 96,118 100,694 75,320 115,177 101,955 67,040

Table 2.4 Malariometric data for Rajasthan state (1961–2000) (Source: Tyagi 2002) Pf cases 3266 508 1210 826 348 532 1221 923 1158 4985 8064 8470 16,451 13,663 31,304 24,163 12,445 8612 4670 15,871 14,752 12,296 35,462 20,443 12,643 % Pf 38.45 15.85 31.73 26.10 12.11 5.29 5.10 6.15 7.47 6.24 7.34 10.26 13.94 7.69 8.82 5.85 5.36 5.57 5.59 16.51 14.65 16.32 30.78 20.05 18.86

ABER 3.39 5.76 9.16 10.44 9.92 8.27 7.66 6.96 5.97 6.86 8.41 8.36 8.09 9.76 11.11 12.74 11.40 10.88 11.31 13.32 12.29 9.92 9.41 8.50 8.76

API 0.48 0.17 0.20 0.15 0.13 0.43 1.04 0.63 0.63 3.15 4.25 3.11 4.42 6.44 12.87 14.73 7.97 5.21 2.68 3.04 3.10 2.27 3.43 2.99 1.93

SPR 1.43 0.30 0.22 0.14 0.13 0.52 1.35 0.90 1.05 4.60 5.05 3.72 5.46 6.61 11.58 11.55 6.99 4.79 2.37 2.28 2.52 2.29 3.64 3.51 2.21

Deaths 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 (continued)

SFR 0.55 0.05 0.77 0.04 0.02 0.03 0.07 0.06 0.08 0.29 0.37 0.38 0.76 0.51 1.02 0.68 0.38 0.27 0.13 0.38 0.37 0.37 1.12 0.70 0.42

2.2 Desert-Driven Malaria 31

Year 1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000

Population (×000) 34,897 35,378 35,457 35,683 35,854 43,881 43,880 44,005 44,005 44,005 44,005 44,005 44,005 45,159 44,006

Table 2.4 (continued)

Blood slides collected 2,941,659 3,219,363 3,493,559 3,074,207 3,567,539 3,179,925 3,833,880 3,644,944 4,855,841 5,181,432 6,591,873 6,000,745 4,977,977 5,223,301 4,969,259

Blood slides examined 2,941,659 3,219,363 3,493,559 3,074,207 3,567,539 3,179,925 3,833,880 3,644,944 4,855,841 5,181,432 6,591,873 6,000,745 4,977,977 5,223,301 4,969,259

Positive cases 54,618 65,523 104,109 112,316 114,689 77,573 121,499 107,797 241,255 350,780 300,547 272,670 76,438 53,154 35,973

Pf cases 13,890 13,942 29,189 24,072 32,500 16,097 41,513 26,387 94,020 45,212 72,780 19,742 10,030 5857 3425 % Pf 25.43 21.28 28.04 21.43 28.34 20.75 34.17 24.48 38.97 12.58 24.21 7.24 13.12 11.02 9.52

ABER 8.43 9.10 9.85 8.62 9.95 7.25 8.74 8.73 11.04 11.77 14.97 13.63 11.31 11.57 11.29

API 1.57 1.85 2.94 3.15 3.20 1.77 2.77 2.44 5.48 7.97 6.82 6.19 1.73 1.18 0.82

SPR 1.86 2.04 2.98 3.65 3.21 2.44 3.17 2.96 4.97 6.76 4.55 4.54 1.53 1.02 0.72

SFR 0.47 0.43 0.84 0.78 0.91 0.51 1.08 0.72 1.94 0.87 1.0 0.32 0.20 0.11 0.07

Deaths 2 0 2 1 65 10 55 19 452 45 0 0 0 0 10

32 2 Global vis-à-vis Desert-Driven Malaria

2.2 Desert-Driven Malaria

33

Malaria Situation During Pre-1966 Period One of the earliest scientifically documented reports on malaria from Rajasthan had been by Green (1911), following which many an important but isolated malariological reporting was brought on record which mostly related to the southeastern Rajasthan being the stronghold for nearly all the epidemiological and entomological investigations in the pre-independence period, although a few reports from the Thar Desert also existed (cf. Christophers 1933; Macdonald 1931; Jaswant Singh 1933). It is interesting to note that because of its strategic location in the midst of desert and non-desert or plain regions in the State, Jodhpur, a desert township in the Thar Desert, also aptly referred to as the Rajasthan’s Gateway to the Great Indian Thar Desert, was selected as one of the earliest trials with DDT in controlling malaria vectors in the country in the late 1940s. There is ample evidence to show that malaria endemicity was of a very low order by the early 1950s, which however gradually accentuated in the ensuing years. The infant parasite rate (IPR), child parasite rate (CPR), and child spleen rate (CSR) are considered good indicators to comprehend the level of endemicity in a community, and when the same are analyzed for the period 1953–1954 to 1956–1957 in both the insecticide sprayed and unsprayed areas in Rajasthan, a steady increase in these rates could be noticed (Table 2.5). The funding situation in the state had been quite satisfactory, considering that most malaria cases appeared from the forested and mountainous Udaipur zone and the non-desert north-eastern areas under Jaipur and Kota zones. At a time when the incidence of malaria from various districts had begun to show an escalating trend around the mid-1980s, the budget allocation was also regularly increased (e.g., from Rs. 106.63 million in 1986–1987 to Rs. 127.41 million in 1988–1989). According to a recent report the State Government has spent about Rs. 31.5 million in 2001, which included the World Bank assistance of more than Rs. 15 million for Jodhpur zone (Anon. 2001). Much before the Thar Desert began to generate more hyper-endemic patches, the plains have always been liable to periodic epidemics that occurred almost every year, culminating into a severe epidemic every 6 or 7 years, e.g., Bharatpur district where child spleen and parasite rates were reported to be about 45% and 50%, respectively, with high adult spleen rates. In the flood-prone lower reaches of the Thar Desert malaria remained confined mainly to Barmer and Jalore districts, e.g., Sanchore tehsil in Jalore district was one such area where in 1954 and

Table 2.5 Infant parasite rate (IPR), child parasite rate (CPR), and child spleen rate (CSR) in insecticide sprayed (A) and unsprayed (B) areas of Rajasthan for period 1953–1954 to 1956–1957. (Source: Tyagi 2002)

Rates (%) IPR CPR CSR

Year 1953–1954 A B 0 0 1.3 – 4.8 –

1954–1955 A B 0.5 – 1.0 0 4.3 19.8

1955–1956 A B 0.8 0.4 1.2 3.6 16.9 42.0

1956–1957 B A 0 – 2.9 35.7 12.1 41.4

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Global vis-à-vis Desert-Driven Malaria

1956 the child spleen, adult spleen, and the child parasite rates were up to 50–100%, 25–70%, and 25%, respectively. Both Plasmodium vivax and P. falciparum were detected adequately, though P. malariae occurred rarely. However, in the last few decades, the Thar Desert has emerged malariologically as a singularly most important ecosystem and the vastly acknowledged factor attributable to the change in the desert malaria situation has been associated with the water management from the threesome of the Gang canal, the Bhakra-Sirhind feeder canal, and the Indira Gandhi canal systems—a subject that will be discussed in great detail in the following pages in this book. In the hilly and forested Udaipur area malaria was always endemic with hyperendemic patches, often with average spleen rate being close to 50%. (a) Season of Malaria: Generally high malaria transmission season starts after the monsoon in July and lasts up to November/December, although in certain areas (like Bharatpur district) two peaks of transmission of malignant malaria were noted each in July–November and February–March. In the hilly areas of Udaipur zone the transmission is always much longer due to persistent presence of the vector, An. fluviatilis. (b) Anopheline Fauna: A total of 15 species were reported to be present in Rajasthan (Anon. 1976), although Puri (1955, 1960) had enlisted a total of 16 species from Rajasthan. Of these species, An. culicifacies and An. fluviatilis were incriminated as the main vectors of malaria in plain and hilly regions, respectively, with sporozoite rates about 0.39% and 2.08% in the corresponding regions. Anopheles stephensi was suspected a vector of malaria in urban areas only. (c) Susceptibility Status of Vector Species against Insecticides: Both An. culicifacies and An. stephensi were confirmed to have developed resistance against DDT. Moderate to high resistance to DDT by An. culicifacies was found in 11 units, high level of insecticide resistance (i.e., mortality between 7–21% in 1–2 h exposure to DDT) was determined in Pratapgarh, Banswara, Udaipur, Dungarpur, Sirohi, Bharatpur, etc. Anopheles stephensi moderately resistant to DDT was confirmed in nine subunits comprising Ajmer, Barmer, Sojat, Bikaner, Nagaur, Jodhpur, Pali, Sanchore, and Jaipur, while high resistance level of An. stephensi was determined in Nagaur, Khetri, and Neem ka Thana. Malaria Situation During 1967–1976 (a) Malaria Prevalence. Since 1966 the epidemiological situation in the Rajasthan State had changed with malaria cases gradually increasing year by year, particularly the P. falciparum infection, thus threatening the life of people. During this period, a definite shift in Rajasthan’s malaria scenario was visible, and when compared to certain other problematic states, the malaria incidence (1973–1975) had apparently increased constantly with much bigger margin over each of the receding year (Table 2.6). Thus, while there occurred an increase of 50.5% in

2.2 Desert-Driven Malaria

35

Table 2.6 Comparison of malaria cases in Rajasthan state with those of other malariologically major problematic states (Source: Tyagi 2002)

State/UT Andhra Pradesh Assam Bihar Gujarat Haryana Karnataka Madhya Pradesh Nagaland Orissa Punjab Rajasthan Tamil Nadu Uttar Pradesh West Bengal

% of increase/ decrease for 1975 over 1974 -21.5

1973 94,400

1974 142,430

1975 111,807

% of increase/ decrease for 1974 over 1973 +50.9

37,918 39,989 437,292 103,777 78,443 262,780

49,684 82,299 570,799 243,543 163,343 437,774

49,182 98,776 758,344 506,465 332,257 676,593

+31.1 +105.8 +30.5 +121.9 +108.2 +65.1

+89.6 +20.0 +32.9 +107.9 +103.4 +55.9

2823 189,767 166,846 133,097 5869 52,052

3108 292,225 230,274 177,596 14,236 120,110

2710 267,359 279,150 355,635 87,708 359,824

+10.1 +53.9 +38.4 +50.5 +142.6 +265.2

-12.8 -8.5 +21.2 +94.7 +516.1 +89.3

12,433

18,938

37,090

+52.3

+95.8

Positive cases

1974 over 1973, the increase was 94.7% for 1975 over 1974 in Rajasthan being one of the four states in the country exhibiting an increase of over 90%. (b) Anopheline fauna. Anopheles culicifacies was the main vector in all plain regions of Rajasthan, the sporozoite rate being about 0.3%. The relative density of An. culicifacies tended to increase following the monsoon during August, September, and October. Anopheles culicifacies and An. fluviatilis were both confirmed to transmit malaria in the hilly and forested areas under Udaipur region, with sporozoite rates of An. fluviatilis being around 2.08%. Anopheles stephensi was strongly “suspected” to be a vector in the desert area of Barmer, Jodhpur, and Bikaner where its density increased during March and April, and again in August. Anopheles culicifacies is generally oriented for feeding between 9 and 11 p.m. but was sometimes found to continue feeding up to 1 a.m., as observed in Jodhpur. On the contrary, An. stephensi preferred to feed between 4 and 6 am. The anthropophilic indices recorded for both these vector species are tabulated below for comprehension of their blood meal preferences (Table 2.7). It is evident from the above tabled information that while An. culicifacies was the most significant vector in vast areas of the State, An. stephensi appeared equally important as a vector especially in the desert district of Jodhpur and even some other plain areas.

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Table 2.7 Anthropophilic indices (Al) for An. culicifacies and An. stephensi recorded in different places in Rajasthan (nd = not done) (Source: Tyagi 2002) Name of places Jodhpur Jaipur Bundi Kota Pratapgarh Ambamata ka khera Udaipur

AI for An. culicifacies 25.4% nd 12.0% 16.8% 14.8% 20.0% 34.0%

Al for An. stephensi 25.2% 24.4% 23.1% 12.9% nd nd nd

One of the important developments in the malaria control operations through vector control was of ULV (Ultra Low Volume) space spray with 10 or 15 days interval which the Government of India, with the aid of World Health Organization, undertook for the first time in India with effect from April 1973 to December 1974 in Jodhpur. The pilot project was initiated in the Soorsagar site in Jodhpur covering about 2–3 km2 area having persistent malaria transmission and vector resistance to DDT. The space spray with ULV was found very effective in reducing the vector density immediately after the spray. Particularly when applied with a 10-day interval, the ULV space spray reduced the density of both An. culicifacies and An. stephensi to very low levels and also brought down the malaria cases from 1222 cases in 1973 to 569 cases in 1974. However, as the experiment could not be sustained the vector density rebuilt itself soon after the spray. Malaria Situation During 1977–1995 This is perhaps the most critical period for Rajasthan, full of events that culminated in recurrence of a series of epidemics, particularly in the Thar Desert region, causing immense morbidity and heavy mortality year after year (Tyagi and Chaudhary 1997). After 1975–1976, it occurred for the first time in the known history of malaria of Rajasthan that the malaria cases exceeded 0.3 million mark, although no death was reported in the 1970s. When compared with the base morbidity results for 1961 (8494 positive cases), it was amazing to know that overall number of positive cases in the State had increased to 350,780 in 1995 (41-fold increase), while the targeted population increased only 2.5 times during the same period. While the slide positivity rate (SPR) had significantly increased from 1.43 in 1961 to 5.07 in 1994 (3.5-fold increase), the slide P. falciparum rate (SFR) had also increased as many folds only, from 0.55 to 1.95. However, the increase in either the SPR or the SFR was not steady and, therefore, no definite trend could be noticed. The maximum SPR was recorded in 1976, with several epidemics in non-desert parts of the State (Sharma 1986a, b; Tyagi 1994a). From the mid-1980s onwards, however, the trend had become clearer and both the SPR and SFR had steadily increased. In fact, the highest ever SFR had been recorded in 1994—the year when the State as well as the Thar Desert region experienced the maximum deaths due to malaria in their entire history. The annual parasite incidence

2.2 Desert-Driven Malaria

37

Fig. 2.3 Histograms showing total P. falciparum cases (×1000) total malaria cases (×1000) and deaths from malaria in Rajasthan between 1990 and 1995. (Source: Tyagi 2002)

(API) also showed a steady increase from 0.48 to 1.76. The state of disease prevalence, including death toll, in the State between 1990 and 1994 is depicted in Fig. 2.3. Malaria Situation During 1996–2020 Extensive control measures undertaken all over the State reduced the incidence steadily from 1995 onwards, and in 2000 the malaria cases were just 10% of what was reported for 1995. However, after a fall initially, P. falciparum proportion is stabilized around 10% which is a serious concern to disease managers and disease control implementers. Furthermore, once again heavy mortality was reported in 2000, although in 1999, too, some deaths could have possibly occurred during an epidemic in Jaisalmer. It is noteworthy that malaria outbreaks struck in western Rajasthan during the 3 consecutive years of 1999, 2000, and 2001, of which at least first 2 years were confirmed as drought years, while 2001 had a good rainfall. A sudden roll back of malaria cases in 2001 (total positives 1,29,233; P. falciparum 17,405) from a rather less vexing figure of 2000 (total positives 35,973; P. falciparum 3425) has once again alerted for possible epidemics in future (Anon 2002a, b, c, d). The period thereafter up till 2020 has been full of upheavals witnessing several major and minor outbreaks. Malaria Situation in the Great Indian Thar Desert (a) Background: Even though the Thar Desert has been reporting outbreaks of malaria infrequently and in a patchy manner, mostly in Sri Ganganagar, Bikaner, and Jodhpur districts, the xeric region was never considered a major player in engendering malaria in the country; in fact, the Thar Desert was regarded as a region with hypoendemic and unstable malaria with potential for occasional outbreaks! The changing scenario of disease endemicity in the Thar Desert, however, caught the attention of Indian Council of Medical Research, and at the behest of Prof. V. Ramalingaswamy, Director General, ICMR, New

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Global vis-à-vis Desert-Driven Malaria

Delhi, a “National Seminar on Deserts, Man and Health” (Anon. 1981) was organized by the S.M.S. Medical College, Jaipur, as a major attempt to understand in-depth the desert-based maladies among humans. Deliberations in this seminar, especially on vector-borne diseases including malaria, not only led to the inevitable necessity of establishment of the ICMR-Desert Medicine Research Centre in Jodhpur, but also analyzed for posterity the impending impacts of climate change and anthropization particularly the development of Indira Gandhi Nahar Pariyojana (IGNP) on both the infectious/communicable and non-infection/non-communicable diseases in desert communities. The real significance of the changing physiography of the Thar Desert on emergence of malaria, particularly Plasmodium falciparum-dominated malaria, was brought to light after long-term investigations by Tyagi (1995a, b, 1996a, b, c, d, e, f, g, 2002, 2003a, b, 2020), Tyagi and Chaudhary (1996, 1997), and Tyagi et al. (1995). (b) Advent of Canalized Irrigation and Transformation of Desert Physiography: The Thar Desert region in north-western Rajasthan does not remain any longer a mere hypoendemic area with precarious potential for infrequent and sporadic focal malaria outbreaks (Tyagi 1992a, b, 1995a; Akhtar and McMichael 1996). On the contrary, the Thar Desert has recently emerged as one of the more potential hot-beds in the country for recurrent Plasmodium falciparumdominated epidemics, particularly in the areas under the Indira Gandhi Nahar Pariyojana (IGNP). Recent experience in the Thar desert of western Rajasthan, India, does not support the view that canal-irrigated desert zones are at low risk of malaria outbreaks. Following an epidemic in this region in 1994, increased vector species—their density and vectorism, and a drastic change in meteorological factors and irrigation practices were postulated as the causes (Tyagi 1995a, b; Tyagi and Chaudhary 1997). One of the particular debates has focused on whether populations living in irrigated arid zones remain prone to malaria epidemics, or whether endemicity ensues (as in the more irrigated, heavier rainfall—but more socioeconomically favoured—Punjab State) (Akhtar and McMichael 1996)? (c) Emergence of Plasmodium falciparum-Dominated Malaria and the ‘Thar Desert Model’: Under the continuing dynamic xeric environmental circumstances, together with increased quantum of vectors, vectorism, and vectorization, high human mobility and migration during droughts, expanding urbanization, and climate change, the Thar Desert’s malariology is also shifting from low endemic, unstable, and occasional malaria epidemics to potentially more epidemic-prone and Plasmodium falciparum-dominated malaria in the canalirrigated Thar Desert (Tyagi 2003a, b). It is to be noted here that more than two-third of the Thar Desert is still devoid of canalized irrigation system despite the three major canal-based irrigation systems in the desert. Conclusively, The Thar Desert can be safely acknowledged as an effective model to understand a correlation between changes in a xeric environment, brought about mainly by extensive canalization, and escalation in P. falciparum-dominated malaria incidence as well as more or less ‘yearly cyclic’ epidemics. The ‘Thar Malaria

2.2 Desert-Driven Malaria

39

Model’ is good also in further understanding how an effective, or otherwise, water management can have a bearing on the vector composition, vectorial capacity, and prospective mosquito nuisance in a region that was virtually a terra incognito for several of these mosquito species till a few decades ago. Milestones on Malaria Research in the Thar Desert The whole subject of malaria in the Great Indian Thar Desert will be discussed in extenso in the following chapters. However, major achievements in malaria research and anti-malaria activities in the Thar Desert are chronologically presented below with a view to acknowledge, on the one hand, the real malaria potential of the Thar Desert region and, on the other, the future challenges awaiting indefatigable malariologists/medical entomologists to decipher the enigmatic ‘Desert Malaria’. The Thar Desert in north-western India has a long history of malaria (Tyagi 2002). The sun-baked arid environments of the Thar Desert are a far cry from the aquatic habitats in which mosquitoes generally breed and complete half of their life cycle. Yet, even in the driest and dustiest part of India mosquitoes can still manage to survive under quaint conditions and emerge to feed on human blood and transmit the deadly malaria disease. Although malaria research in the Thar Desert is nearly a century old, nevertheless, more active malariological investigations have been initiated rather recently since the late 1980s. Many of these research activities have gone a long way in making better our understanding about ‘Desert Malaria’ and showing a need to make use of more useful modern tools such as those based on molecular biology and genetic engineering to further enrich our knowledge on the subject and the means to control the disease. In Table 2.8 are presented some of the major milestone research activities.

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Table 2.8 Milestones in the malaria research in the Thar Desert Year/ period 1933

1948– 1949 1955– 1960 1962

1980s– 1990s 1989– 1990

1990– 1991

1990

1995

1995– 1996 1997

1999

Event For the first time, the Thar Desert region’s anopheline fauna were described in detail by Christophers (1933), in his magnum opus on ‘Family Culicidae: Tribe Anophelini’ in the classic ‘Fauna of British India’ series One of the earliest trials with the DDT as an indoor residual adulticide for controlling malaria vectors was made in Jodhpur Puri (1955, 1960) described in great detail the larval identification keys of Indian anophelines, some of which referred to the Thar Desert fauna, too Wattal and Kalra (1961) described comprehensively the identification keys based on adult characteristics for the Indian anophelines, some of which occurred in the Thar Desert as well Dr D. Kochar and his group made important investigations on malaria and discovered that Plasmodium vivax could be also associated with neurological complications For the first time in the Thar Desert, Anopheles culicifacies was incriminated with the malarial parasite in Sri Ganganagar, and its distribution with canalized irrigation was demonstrated during the course of a long-term entomological investigation (Tyagi and Verma 1991) For the first time, Anopheles stephensi was incriminated with the malarial parasite from the interior of the rural Thar Desert. Its predominance in the xeric environments was demonstrated and its exclusive breeding in the household underground water reservoir, ‘tanka’ and ‘beri’, both carrying tremendous malariological significance in the desert ecosystem, was brought on record with the coining of a new malariological paradigm, “the Desert Malaria” (Tyagi 1995a, 1998a, b; Tyagi and Yadav 1996a) March 22, an indigenous mosquito sampler was developed by Dr. B.K. Tyagi, which was registered with the National Research Development Corporation, New Delhi for seeking PATENT by the Indian Council of Medical Research, New Delhi, in 1996 In acknowledgement of repeated malaria epidemics in the Thar Desert, influencing the overall malaria scenario in the Rajasthan State, as well as strong malaria research potential at the Desert Medicine Research Centre, Jodhpur (established in 1984), malaria was identified as a major thrust research area at the DMRC. This mandate was once again reinforced with greater emphasis in 1999 Various kinds of factors underlying emergence of malaria epidemics in the Thar Desert region were clearly outlined and defined (Tyagi 1995a, b, 1996a) A clear-cut correlation between P. falciparum-dominated malaria conflagration in the Thar Desert and the management of canal irrigation water was established (Tyagi and Chaudhary 1997) A ‘tanka lid’ was developed by Dr. B.K. Tyagi for effective control of vector (An. stephensi) breeding in this malariologically very important household and community-based water reservoir, and the technology handed over to the District Collector in Jaisalmer

3

World Deserts: Environments and Malaria Potential

3.1

Introduction

The word ‘desert’ is derived from the ecclesiastical Latin dēsertum, meaning an abandoned place (Ezcurra et al. 2006). A desert naturally paints kind of a picture in the human mind that exhibits a grossly inimical environment for humans and animal populations to live in under generally soaring temperatures, very low humidity, and scanty precipitation, to say the least. All deserts are, however, not characterized with such critically extreme attributions and, particularly when there are cold deserts as well. It is interesting to know that about 33% of the Earth’s land surface is arid or semi-arid, both ‘hot’ and ‘cold’ types. The latter includes much of the polar regions, where little precipitation occurs, and which are sometimes called polar deserts or ‘cold deserts’ due to extreme weather conditions. Characteristically, as a rule, ‘cold deserts’ are free from malaria. Therefore, it is rather difficult and complex to attempt to judge some correlation between aridity and sparse population dynamics including the living conditions, socio-culture, agriculture practices, and technologies. Therefore, in the outset itself, it considered opportune and of paramount importance to foremost clear beforehand the term ‘desert’ particularly in its relation to malaria. Before the dawn of the twentieth century, desert was often used in the sense of ‘unpopulated area’, without specific reference to aridity; but today the word is most often used in its climate-science sense as an area of low precipitation. Accordingly, a desert is a barren area of landscape where little precipitation occurs and, consequently, living conditions are hostile for plant and animal life with abysmal diversity whatsoever (Sher et al. 2004). Deserts generally receive less than 250 mm (10 in) of precipitation each year, though it may vary a great deal in reference to a given desert. As a rule, all hot deserts in the world exhibit very low evapotranspiration which may be close to zero. Semi-deserts (when clad in grass, these are known as steppes), buffer zones, or the desert fringe areas are regions which receive relatively much higher precipitation generally ranging between 250 and 500 mm. The lack of vegetation exposes the unprotected surface of the ground to the processes of denudation (Bhandari 1978). # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_3

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3 World Deserts: Environments and Malaria Potential

Even though there are close to 100 deserts, small and big, and hot and cold, across the globe, nevertheless less than only a dozen of them are large enough with characteristic arid environment that generally attract human attention for their malariogenic potential (Table 3.1, Fig. 3.1). While the Sahara desert is the largest hot desert in the world (9.2 million km2 covering a total of 8% of the earth’s land area; and the third largest overall after the Antarctica and the Arctic), the Namib Desert is believed to be the oldest desert (55 million years) (Barnard 1998), and the Aralkum Desert, lying to the south and east of what remains of the Eastern Basin Aral Sea in Uzbekistan and Kazakhstan, is currently the youngest desert in the world since it has appeared in 1960 on the seabed once occupied by the Aral Sea. The Atacama Desert, forming part of the arid Pacific fringe of South America, is one of the driest regions in the world. The Thar Desert in the north-west India is peculiar owing to its massive canalized irrigation system called Indira Gandhi Nahar Pariyojana (IGNP), complemented by two others, namely, the Gang Canal and the Bhakra-Sirhind Canal, and regarded as one of the world’s most gigantic projects of its kind in a desert ecosystem (app. 10,000 km) that has not only partially transformed the desert’s physio-demography in favour of annual cyclic malaria epidemics in recent decades, on one hand, but also proved it to be the first model of malaria in arid environments. ‘One usually does not associate malaria with a desert environment. Common sense dictates that mosquitoes, that breed only in stagnant water, would give arid, water-scarce spaces such as a desert a wide go-by. But that is not the case in the Thar desert. Rajasthan, India, is also the land of persistent desert malaria. The Thar Desert has a unique ecosystem. But over the last two decades, its physiography has undergone a major change. What precisely changed? And what is the relation between this change and the transformation of malaria from an occasional to a persistent, endemic disease? The startling answer is: extensive canalisation! Though these projects were set up with good intentions—they would provide a fillip to irrigation, allow more crops to be grown, and solve the water problem of the region—they also brought with them swarms of mosquitoes. Drastic changes began to occur in the ecosystem: increase in the water table, water logging, and a change in the rainfall pattern along with relative humidity were observed’ (DownToEarth 2003).

3.2

Desert Environments, Man, and Malaria

There are many theories about the origination of the hot deserts and one of these ascribe weathering processes being the reason behind the desert formation. The weathering process is characterized by the large variations in temperature between day and night which put strains on the rocks and consequently break them in pieces (Mann 1978). Scanty precipitation is another feature of the desert, although occasional downpours happen in certain areas that can result in flash floods such as those in the Thar Desert during 1988, 1990, and 1994 (Tyagi 2002). When rain falls on hot rocks, they shatter them into smaller strands, and rubble strewn over the desert floor are further eroded by the wind. This fast billowing wind in the desert gathers up fine

3.2 Desert Environments, Man, and Malaria

43

Table 3.1 A complete list of hot deserts of the world S. No. 1

Country Afghanistan

2 3 4

Algeria Argentina Australia

5 6 7 8 9 10

Bahrain Botswana Bulgaria Colombia Chile China

11 12

Kyrgzstan Egypt

13 14 15 16 17

Eritrea Ethiopia Greece India Iran

18 19 20 21 22

Iraq Israel Italy Jordan Kazakhstan

23 24

Kenya Libya

25 26

Mexico Mongolia

27 28 29 30

Namibia New Zealand Niger Oman

Deserts Dasht-e Khash, Dasht-e Leili, Dasht-e Margo, Dasht-e Naomid, Ragistan Desert Erg Chebbi, Erg Chech, Grand Erg Occidental, Tademait Salar de Arizaro, Monte Desert, Patagonian Desert, Salinas Grandes Great Victoria Desert, Great Sandy Desert, Tanami Desert, Simpson Desert, Gibson Desert, Little Sandy Desert, Strzelecki Desert, Sturt Stony Desert, Tirari Desert, Pedirka Desert Sakhir Kalahari Desert Pobiti Kamani Guajira-barranquilla Xeric Scrub, La Guejira Desert, Tatacoa Desert Atacamara Desert, Lomas, Patagonian Desert, Sechura Desert Gobi Desert, Badain Jaran Desert, Dzungaria, Gurbantunggut Desert, Hami Desert, Kumtag Desert, Lop Desert, Mu Us Sandyland, Ordos Desert, Shapotou District, Taklamakan Desert, Tengger Desert Betpak-Dala, Muyunkum Desert Blue Desert, Eastern Desert, Great Sand Desert, Libyan Desert, Qattara Depression, Sinai Desert, Wadi El Hitan, Wadi El Natrun, Western Desert Danakil Depression, Eastern Desert Danakil Depression, Eastern Desert Pachies Ammoudies of Lemnos Thar Desert, Cold Desert Dashte-e Kavir, Dasht-e Lut, Dasht-e Naomid, Kavir National Park, Maranjab Desert, Petregan Playa, Polond Desert Arabian Desert, Syrian Desert Negev, Judaean Desert, Negev, Zin Desert Acona Desert Arabian Desert, Syrian Desert Aral Karakum Desert, Aralkum Desert, Betpak-Dala, Central Asian Nrothern Desert, Karagiye, Karakum Desert, Kasakh Semi-Desert, Kyzylkum Desert, Muyunkum Desert, Ryn Desert, Saryesik-Atyrau Desert Chalbi Desert, Nyiri Desert Calanshio Sand Sea, Calansho Desert, Great Sand Sea, Idehan Ubari, Libyan Desert, Murzuq Desert, Rebiana Sand Sea, Tadart Acacus Chihuahuan Desert, Gran Desierto de Altar, Sonoran Desert Gobi Desert, Dzungaria, Khongoryn Els, Flaming Cliffs, Khongoryn Els Kalahari Desert, Namib Desert Maniototo, Rangipo Desert Erg of Bilma, Talak, Ténéré Arabian Desert, Empty Quarter, Gulf of Oman Desert and SemiDesert, Jiddat al-Harasis, Umm al Samim, Wahiba Sands (continued)

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3 World Deserts: Environments and Malaria Potential

Table 3.1 (continued) S. No. 31

Country Pakistan

32 33 34

Peru Poland Saudi Arabia

35 36 37 38

Senegal Serbia South Africa Spain

39 40 41 42 43

Sudan Syria Turkmenistan United Arab Emirates United States

44

Uzbekistan

45

Venezuela

46

Yemen

Deserts Thar Desert, Bhakkar Tehsil, Cholistan Desert, Cold Desert, Hazarganji-Chiltan National Park, Hingol National Park, Indus Valley Desert, Kachho, Kharan Desert, Thal Desert, Thar Desert Garua, Lomas, Sechura Desert Bledow Desert Ad-Dahna Desert, An Nafud, Arabian Desert, Arabian Peninsula Costal Fog Desert, Empty Quarter, Red Sand Ferlo Desert, Lompoul Desert Deliblato Sands Kalahari Desert, Karoo, Namib Desert, Richtersveld Bardenas Reales, Cabo de Gata-Nijar Natural park, Monegros Desert, Tabernas Desert Bayuda Desert, Eastern Desert, Libyan Desert, Nubian Desert Syrian Desert Karakum Desert, Kyzylkum Desert Al Khatim Desert, Arabian Desert, Empty Quarter Chihuahuan Desert, Mojave Desert, Yuma Desert, Lechuguilla Desert, Sonoran Desert, Painted Desert, Tonopah Desert, Tule Desert, Amargosa Desert, Eastern California, Great Basin Desert, High Desert, Low Desert, Old Plank Road, Yuha Desert, Owyhee Desert, Yp Desert, Black Rock Desert, Smoke Creek Desert, Alvord Desert, Tamaulipan Mezquital, Bonneville Salt Flats, Escalante Desert, Great basin Desert, Great Salt Lake Desert, Sevier Desert Aralkum Desert, Central Asian Northern Desert, Karakum Desert, Kyzylkum Desert, Mirzacho Guajira-Barranquilla Xeric Scrub, la Guarjira Desert, Medanos de Coro National Park Arabian Desert, Arabian Peninsula Coastal Fog Desert, Empty Quarter, Ramlat al-Sab’atayn

particles of sand and dust, which can remain airborne for extended periods and if densely matrixed can cause the formation of sand storms or dust storms. Further any solid object in their path such as the embedded rocks in the desert are smoothed down by the striking of wind-blown sand grains and are abraded on the surface, and the wind sorts sand into uniform deposits, but sometimes the finely grained sand particles end up as overlaying sheets of sand or are piled high in billowing sand dunes or levees. But all deserts, though maintaining xeric environments throughout, are not sandy but are flat, stony plains commonly known as desert pavements. Still, beyond the sandy and rock-hard flat deserts, at times a desert may imbibe other desert features such as rock outcrops, exposed bedrock, and clays once deposited by flowing water. When occasional rainfall occurs, the gushing floodwater may run down along the hard surfaced rocky payments and get collected as temporary lakes in the deeper cavities emerged in the whole process of desert formation. After

3.2 Desert Environments, Man, and Malaria

45

Fig. 3.1 A global distribution of the desert areas according to their Aridity index. Deserts distribution throughout the land surface, making up 33% of the total land area. The map indicates the most famous deserts in each continent, the Mojave, Sonoran, and Chihuahua Desert in North America and the Atacama Desert in South America. The largest deserts in the world are the Sahara desert in North Africa, along with the Kalahari and Namibia deserts in the southern parts of Africa. In the Middle East, the Negev and the Arabian Peninsula Deserts. In East Asia, the Thar Desert (90%) in North India and (10%) in parts of Pakistan, and in west Asia the Lut Desert, while the Gobi and Taklamakan Deserts cover North China and a large part of Mongolia. In Australia, Great Sandy and Gibson Deserts are shown. The map classifies the deserts based on the global Aridity index (AI), which is defined as the numerical indicator of the degree of climatic dryness in a specific location. The map shows the hyper-arid zones in bright yellow, semi-arid zones in orange, and arid zones in brown. (Source: Available free online at: http://wad.jrc.ec.europa.eu)

evaporation of water from lakes salt pans, such as the Sambhar Lake in the outskirts of the Thar Desert, are formed. Generally deserts may harbour a variety of water sources aplenty in the form of springs and seepages from aquifers. Where these are found, oases can occur, attracting ‘Desert Oasis Malaria’ such as in the Phalodi Tehsil area in the Thar Desert. Desert plants and animals possess special adaptations to sustain in the hard-tosurvive environment. From outside plants appear to be sturdy, sparsely branched, cuticle-clad, and spiny with small or no leaves to deter herbivory. During occasional rains some annual plants germinate, bloom, and die in the course of a few weeks after rainfall such as swan grass, Lasiurus scindicus (Poaceae), found in the dry parts of Jaisalmer, Barmer, and Bikaner in the Thar Desert, while other perennial plants such as Prosopis cineraria (Fabaceae) survive for years in dry soil conditions of the Thar Desert in India, besides arid portions of Afghanistan, Behrain, Iran, Oman, and Pakistan. Animals likewise are few in species diversity; while invertebrates like arthropods e.g., dung beetle (Scarabaeidae) and vertebrates like reptiles, e.g., desert lizard or Sara hardwickii (Agamidae) are poikilothermic (i.e., animals whose body temperature varies considerably and more or less in regard with the temperature of their environment) and suitably adapted to desertic conditions. As far as mosquitoes

46

3 World Deserts: Environments and Malaria Potential

are concerned, Anopheles stephensi, is an extraordinary example of desert adaptability; it is the only anopheline mosquito in the Thar desert which can live throughout the year beating the extreme temperature ranges (0 °C in winter to 50 °C in summer) (Tyagi 2002). Desert animals efficiently conserve water extracting most of it from their food and concentrating their urine. Desertification is a continuous process and is on the increase in many continents of the world. For millennia the growing human and cattle populations, with their vital needs in decline, have been constantly forcing nomadic people to quest for more space to settle in the vast, yet inhospitable, expanses of the desert environments and the less inimical surrounding semi-arid lands. Oases, being the major source of water and abysmal agriculture, have not only provided opportunities for a comfortable settlement of life but also grazing and fodder for their flocks and herds of milching, transport, and nutritive significance. Some nations, realizing early that oases may not suffice for a prosperous development of people in the desert, worked out to bring in canalized water from other places with surplus sources in the Himalaya to the desert and upscaled farming with the fresh aid of irrigation. The birth of Indira Gandhi Nahar Pariyojana (IGNP) in the Thar Desert, western India, being the one such project of its kind aiming to convert the barren land into verdure and upgrade people’s GDP (Gross Domestic Product), is a glittering example in the world. Presently three major canal systems exist in the Thar desert (Gang Canal, Bhakra-Sirhind Canal, and Indira Gandhi Nahar Pariyojana). This Herculean task of bringing Himalayan waters to the Thar desert, with an investment of INR 1161 crores (at 1990 level) has resulted in growing irrigation-intensive crops such as sugarcane, mustard, groundnut, wheat, and of course paddy. Paddy is mostly grown in Sri Ganganagar, Bikaner, and Sikar districts. The production of paddy in Sri Ganganagar district alone, the most irrigated among all desert districts, has topped the list in the whole State of Rajasthan. Nomadism and, during severe droughts, regular migration of the local folks in search of food and fodder for their pets across the desert limits and beyond to other areas or countries have ushered in many trade routes across deserts. Some mineral extraction also takes place in deserts, and the uninterrupted sunlight gives potential for the capture of large quantities of solar energy. Depending upon nature, deserts are categorized under (i) hot, (ii) cold, (iii) semiarid, or (iv) coastal head. Some of the hot deserts, being heartlands for malaria conflagration, are invariably characterized by high temperatures in summer; greater evaporation than precipitation by high temperatures, strong winds, and lack of cloud cover; considerable variation in the occurrence of precipitation, its intensity, and distribution; and low humidity. Winter temperatures vary considerably between different deserts and are often related to the location of the desert on the continental landmass and the latitude. Daily variations in temperature can be as great as 22 °C (40 °F) or more, with heat loss by radiation at night being increased by the clear skies. However, such factors as the temperature, humidity, rate of evaporation and evapotranspiration, and the moisture storage capacity of the ground have a marked effect on the degree of aridity and the plant and animal life that can be sustained. Rain falling in the cold season may be more effective at promoting plant growth, and

3.3 Deserts with Potential to Exacerbate Malaria

47

defining the boundaries of deserts and the semiarid regions that surround them on the grounds of precipitation alone is problematic. Excluding cold (or temperate) deserts in view of any malaria history ever, the hot deserts based on precipitation alone fall under the following four different categories: (i) Hyperarid Deserts: characterized by 80 persons/sq. km). This implies that An. stephensi breeding man-made ‘Beris’ and ‘Tankas’ abound in thousands in the overall span of nearly 96,000 sq. km. Thus Anopheles stephensi became the original and foremost anopheline mosquito which must have evolved and established in the Thar desert. Since the human dwellings and cattle-sheds, if at all existing, are approximated the mosquito invariably feed with freedom on both man and animals. Since the ‘Beris’ and ‘Tankas’ are generally loosely covered at the lid, the mosquito has all the freedom to enter, breed and populate in these desertic reservoirs. Its preponderance in the Thar Desert has become a phenomenon of ‘Anophelenization.’ As we will see elsewhere in the book, with the advent of a massive canalization— a combination of three canals, viz., the Gang Canal, Bhakra-Sirhind Feeder Canal, and Indira Gandhi Canal—in the Thar Desert, anophelines such as An. culisifacies and An. subpictus which entered the penetralium of the desert’s arid environment also anophelenized, albeit breeding in altogether different surface water sources (Table 8.2). Though in the mainland peninsular India An. stephensi has been existing in all the five States of Karnataka, Telangana, Andhra Pradesh, Tamil Nadu, and Kerala, nonetheless its entry in Kerala State has been confirmed rather recently (Sharma and Hamzakoya 2001). Soon afterwards the vector seems to have entered the Lakshadweep Archipelago during early 1990 and since then gained a permanent foothold on these islands due to the availability of a large number of community and rain-harvesting cement storage tanks. It is noteworthy that malaria was already reported in Lakshadweep islands two decades ago (Roy et al. 1978). These developments also threaten the northern islands of Maldives which are about 90 km south of Lakshadweep, where water storage practices are identical (Sharma and Hamzakoya 2001).

8.3 Chorogeography of Anopheline Mosquitoes

155

Table 8.2 Possible evolutionary correlation between the anopheline fauna, malaria incidence, and the extent of canal irrigation in the Thar desert

Period Pre-1930 to 10,000 yrs 1930– 1934 1935– 1939 1940– 1944 1945– 1949 1950– 1954 1955– 1959 1960– 1964 1965– 1969 1970– 1974 1975– 1979 1980– 1984 1985– 1989 1990– 1994 1995– 2021

Number and names of anopheline mosquitoes Vector species Non-vector species No. Name No. Name 1 An. stephensi – –

1

An. stephensi

–

–

2

An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies An. stephensi, An. culicifacies, An. fluviatilis An. stephensi, An. culicifacies, An. fluviatilis

4

An. subpictus, An. annularis, An. vagus, An. splendidus An. subpictus, An. annularis, An. vagus, An. splendidus An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus,An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. subpictus, An. annularis, An. vagus, An. splendidus, An. barbirostris An. annularis, An. subpictusc, An. vagus, An. splendidus, An. nigerrimus, An. barbirostris An. annularis, An. subpictus, An. vagus, An. splendidus, An. nigerrimus, An. pulcherrimus, An. d’thali, An. barbirostris

2 2 2 2 2 2 2 2 2 2 3

3

4 5 5 5 5 5 5 5 5 5 6

9

(a) Until the late 1980s An. culicifacies was recorded only from desert fringe urban areas, e.g., Bikaner; (b) An. fluviatilis is yet to be incriminated with malaria parasites in the Thar Desert, though it is a very efficient vector in southern Rajasthan; (c) An. subpictus is rarely incriminated in the Thar Desert Source: Tyagi (2002)

9

Sibling Species Complexes of Malaria Vectors in Major Deserts

9.1

Introduction

A species complex is primarily a taxonomic phenomenon of immense evolutionary importance, which is fairly common among arthropods, and carries additionally a great epidemiological significance in context with vector-borne diseases such as malaria. In Culicidae, when a mosquito species consists of a group of closely related species which are morphologically nearly indistinguishable and may share the same ecological niche (sympatry), but not interbreeding among themselves at all, it is referred to as a species complex. Correct identification of such complexes among dominant vector species (DVS; Sinka et al. 2010, 2011, 2012, 2020; Sinka 2013), with their zoogeography mapped and behavioural differences against insecticides deployed in the indoor residual spraying (IRS) recorded, help the vector control campaigners to design malaria control efforts effectively without losing sight on the vectors’ bionomics and epidemiological importance. A species complex differs strikingly from a mere species which is a group of individuals that are morphologically, geographically, and ecologically alike but are reproductively isolated from such another group (e.g. subspecies, populations). The complexity of species complexes can be understood from the fact that within a specific group such as Anopheles gambiae in Africa and An. culicifacies in India, there are both the deadly vectors (primary vectors) and less efficient vectors (secondary vectors) or species without any transmission potential. This implies that it is of paramount importance to know beforehand undertaking a control measure in an endemic or outbreak-hit area as to which species in the complex is primary, secondary, or carry no importance epidemiologically. Malaria endemic deserts of the world house some of the species of a complex that derives a great deal of epidemiological significance due to their differential transmission potential, e.g. Anopheles arabiensis in the Sahara Desert (Africa) and An. culicifacies in the Thar Desert (India). Mosquito systematics and phylogeny are often complicated by the excessive nature of species complexes, more specifically under the genus Anopheles. By an estimate there could be more than 50 species complexes under Anopheles which is # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_9

157

158

9

Sibling Species Complexes of Malaria Vectors in Major Deserts

represented by 465 formally recognized species throughout the world (Sinka 2013). Of these, about six dozen species (70#) are vectors of some measure while 41 are confirmed primary vectors of malaria transmission.

9.2

Species Complexes in Deserts

Some of these species complexes have extended into the deserts, although no complete species complex is specifically limited to the arid environments of the deserts.

9.2.1

The Sahara Desert

Anopheles arabiensis is a member of the An. gambiae complex, which is most common in Africa south of Sahara (Sinka 2013). It is also a major vector, perhaps along with An. quadriannulatus, in the Sahara Desert. There is a suspicion that a new species sympatric with An. quadriannulatus exists in Ethiopia, but until more evidences are brought on record it has been designated as An. quadriannulatus ‘B’ (Hunt et al. 1998). As far as deserts are concerned, following vector mosquito species complexes needs careful attention. Anopheles sergentii is a species complex in Africa and Middle East, hence described under the latter below.

9.2.2

The Middle East/West Asia/Central Asia Deserts

Anopheles sergentii, a dominant vector, is associated with oases, hence deriving the sobriquet, ‘oasis vector’. Due to its ability to cope with the extreme climates across this region and specific propensity to breed in the oases, Anopheles sergentii has become the most important ‘desert malaria vector’ whose distribution is synchronous to the distribution of oases across the Saharan belt in northern Africa and into the Middle East (Fig. 9.1). Besides oases, the vector can breed in a large selection of habitats including streams, seepages, canals, irrigation channels, springs, rice fields, and most other non-polluted, shallow sites that contain fresh water, but also sometimes brackish habitats, with a slow current, slight shade (exceptionally in full sunlight), and emergent vegetation or algae—the latter being the only characteristic common to all larval habitats of this species. An. sergentii, principally a zoophilic species, is still an important malaria vector. The mosquito has been found uncharacteristically feeding on humans and/or animals both indoors and outdoors, and, therefore, its exo-/endophilic and exo-/endophagic status is unclear. Like An. stephensi in the Thar Desert (Tyagi 2002), An. sergentii can also tide over extremely low temperature (overwinter) as both adult females and larvae, in the desert environment of the African Sahara, the Arabian Peninsula, and the Middle East/West Asia.

9.2 Species Complexes in Deserts

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Fig. 9.1 Distribution of Anopheles sergentii in Africa, Arabian Peninsula, and Middle East/West Asia (Source: Free Wikipedia)

As a “desert malaria vector” Anopheles sergentii prominently represents the northern Africa, the Mediterranean basin, and the Middle East (viz., Albania, Algeria, Bulgaria, Burkina Faso, Cameroon, Chad, Côte d’Ivoire, Djibouti, Egypt, Eritrea, Ethiopia, Greece, Guinea, Iran, Iraq, Israel (and Gaza Strip & West Bank), Italy (includes Sicily), Jordan, Libya, Kenya, Mali, Morocco, Pakistan, Portugal, Saudi Arabia, Senegal, Spain (including Canary Islands), Somalia, South Sudan, Sudan, Tunisia, United Arab Emirates (UAE), and Yemen). Anopheles sergentii is found from Algeria and as far south in Africa as Kenya and Cameroon, northeast to Italy, Greece and Albania, and southeast to Pakistan. Anopheles sergentii comprises two valid subspecies: (1) An. sergentii sergentii described from Algeria and (2) An. sergentii macmahoni Evans described from Kenya. Anopheles sergentii macmahoni appears limited to the sub-Saharan belt of Africa. The subspecies macmahoni has one synonym—An. barkhuusi GiaquintoMira, described from Ethiopia. These two taxa are placed in the Demeilloni Group (Myzomyia Series) along with six others—An. carteri Evans & de Meillon, An. demeilloni Evans, An. freetownensis Evans, An. garnhami Edwards, An. keniensis Evans, and An. lloreti Gil Collado.

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Sibling Species Complexes of Malaria Vectors in Major Deserts

The Thar Desert in India

There are as many as six Anopheles species in India which are complexes of sibling species, of which four occur in the Thar Desert (Table 9.1). These complexes carry immense epidemiological significance since some of these are vectors, which only need to be targeted for controlling. Some of these are annotated below: 1. Anopheles culicifacies Giles Anopheles culicifacies, which also has its cradle in the central India, is the most important vector responsible for more than 65% of malaria cases in the country particularly in the rural environments. The species, despite its wide distribution in the Indian subcontinent (Nepal, India, Pakistan and Sri Lanka), in addition to several Southeast Asian countries (e.g., Vietnam, Cambodia, Lao PDR and southern China), and extending on the other hand as far as Yemen in the Middle East as well as Eritrea in the Horn of Africa (Sinka et al. 2011), has been extensively investigated in India Table 9.1 Sibling species complexes of Anopheles mosquitoes in India

Species An. culicifacies An. fluviatilis An. subpictus An. annularis An. dirus

An. sundaicus

Sibling species in complexes duly named taxonomically –

S,T,U and V

Species of complex in India A,B,C,D and E S,T and U

4

A,B,C and D

A and B

–

2

A and B

A and B

–

7

A,B,C,D,E and F, as well as a duly named species, plus another species though an incertae sedis.

D and E

4

An. sundaicus s.s.

An. sundaicus s.s.

Species A = An. dirus s. s., Species B = An. cracens, Species C = An. scanloni Species D = An. baimai Species E = An. elegans Species F = An. nemophilous and An. takasagoensis (additionally, a cryptic Species tentatively designated as An. aff. Takasagoensis) An. sundaicus s.s., An. spiroticus (formerly species A), An. sundaicus species D and An. sundaicus species E.

No. of sibling species 5

Designated species A,B,C,D and E

4

–

9.2 Species Complexes in Deserts

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and Sri Lanka (Surendran et al. 2000; Jude et al. 2010; Subbarao 1988; Subbarao and Sharma 1997; Amerasinghe et al. 1999; Barik et al. 2009). Save for the Species B (which is a highly zoophilic species, hence a non-vector; Subbarao 1988; Vatandoost et al. 2004; Dev 2020), all others are vectors with some degree of potential to transmit malaria, but Species E, owing to its highly anthropophilic and endophilic behaviour, is singularly the most virulent of all vector species to transmit with equal prowess the parasites, P. vivax and P. falciparum (Subbarao et al. 1988; Sharma 1998; Kar et al. 1999; Surendran et al. 2003). These cytospecies are best identifiable and distinguishable from each other through cytotaxonomic methods (Figs. 9.2 and 9.3). These five sibling species overlap each other in distribution in different proportions and a clear understanding of whether a vector or two among them is predominantly prevalent is to be inevitably determined to understand the intensity of malaria transmission, on the one hand, and to bring about effective vector control, on the other (Fig. 9.4). As far as the Thar Desert is concerned, species A and B have been diagnosed there. Both these species overlap each other in large areas and there is hardly any area which is species-specific. As a result, controlling the vector species in the complex through indoor residual spraying is often very challenging (Fig. 9.5). 2. Anopheles fluviatilis Species Complex A dangerous vector for malaria contributing approximately 12–15% of all the annually reported cases, An. fluviatilis is next only to An. culicifacies in intensity of malaria transmission in India, with Species ‘S’ being the vector due to its strong anthropophilic and endophilic behaviour (Fig. 9.6). Anopheles fluviatilis s.l. is distributed widely in the sylvatic-cum-mountainous regions and foothill areas of India, Nepal, Bangladesh, and Myanmar and certain southwestern Asia nations like Iran, Pakistan, and Afghanistan. India and Iran are the only two countries where the biology, distribution, dynamics of orientation for feeding, and ecology of the An. fluviatilis complex have been extensively studied. Adapted to breed in fast flowing mountain rivulets, An. fluviatilis still can abundantly breed in wide-ranging man-made habitats such as irrigation canals, borrow pits, domestic wells, tanks, and gutters as well as natural sites such as stream margins and rock pools in terai area in the foothills of northern States of India as well as the Eastern and Western Ghat regions, where the larvae of this complex are associated with fast-flowing water in streams or river margins. Apparently, the species prefers fresh water sites in comparison to brackish water habitats. 3. An. subpictus Anopheles subpictus Grassi s.l. is a primary (Malaysia, Indonesia) or a secondary malaria vector (India, Sri Lanka) in different Southeast Asian countries; in Sri Lanka it is secondary to Anopheles culicifacies Giles s.l.

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+a

ab

+b

b a

a

b

a

b

b

a Chromosome arm 2

1

+g +h

1

i1 +h

1

g1 +h

1

1

+g h1

1

+i i1

h1

h1

h1

h1 h1

h1

h1

h1

i1 g1 i1

g1

g1

g1

g1 g1

i1 i1

Species A

Species D

Species B

Species C

Fig. 9.2 Anopheles culicifacies sibling species complex (Four only; A, B, C, and D) in a schematic representation of polytene chromosomes (Source: WHOSEARO 2007; allowed with acknowledgement)

9.2 Species Complexes in Deserts

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Fig. 9.3 Anopheles culicifacies: Mitotic karyotypes; (a–c) chromosomes prepared from larval brain tissue; (a) Species B female, (b) Species E male with submetacentric Y-chromosome, and (c) Species B male with acrocentric Y-chromosome (Source: WHOSEARO 2007; allowed with acknowledgement)

Fig. 9.4 Distribution of Anopheles culicifacies sibling species complex in Asia, and parts of Middle East and Africa (Source: Dev 2020, 2022)

Polytene chromosome banding patterns are the most dependable attributes, which, suitably supported by stage-specific morphometric traits, characterize all the four sibling species (A–D) within the An. subpictus complex (Fig. 9.7). Like India where the species and the complex have both been extensively studied (Reuben et al. 1984), all four sibling species of the Subpictus Species Complex have been described in the neighbouring island nation of Sri Lanka (Pavillupillai et al. 2014). Bio-ecologically and behaviourally all the sibling species differ strikingly among themselves, especially in context with breeding habit, fresh or saline/

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9

Fig. 9.5 Western part of Rajasthan State (India) with the Thar Desert (indicated with an arrow) is marked by the presence of species A and B in the Anopheles culicifacies Complex

Sibling Species Complexes of Malaria Vectors in Major Deserts

Thar Desert

Fig. 9.6 Distribution of An. fluviatilis sibling species complex (Source: Dev 2020, 2022)

estuarine habitat, and resting habits indoors or outdoors, but also inclination for blood-feeding (hematophagy) on man (anthropophily) or animals (zoophily). Species A is present in the interior of the mainland India, while Species B, a comparatively stronger vector, exists in coastal areas (Suguna et al. 1994). In Sri Lanka it is Species C which occurs inland. In the Indian Ocean’s pearl-island country,

9.3 The Enigmatic Status of Anopheles stephensi

165

Fig. 9.7 Polytene chromosome complement of An. subpictus species A. Break-points of inversions, a and b, reported by Suguna et al. (1994) are shown on the X-chromosome (Source: WHOSEARO 2007; allowed with acknowledgement)

Species B, C, and D are both anthropophilic and zoophilic, albeit Species C and D are endophilic and endophagic, respectively, while species B is outdoor-resting with no significant preference for indoor- or outdoor-resting (Pavillupillai et al. 2014).

9.3

The Enigmatic Status of Anopheles stephensi

Anopheles stephensi is currently the most intensely investigated species in the world, due singularly to its following traits: 1. engendering ‘Desert Malaria’ in the Thar Desert, 2. adapting de novo to open ground surface water,

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3. most importantly, transcending ecological borders from the Indian subcontinent, the cradle of An. stephensi, to the Arabian Peninsula, through Iran and Iraq, in the west of the Thar Desert (India), as well as Bangladesh, southern China, Myanmar, and Thailand in the east, as the most important urban vector (Krishnan 1954), and 4. recent invasion over new geographic areas so far terra incognito for the species, such as Djibouti (in the Horn of Africa) and Sri Lanka. Anopheles stephensi is a notorious vector of urban environments (Rao 1984), but after its discovery with epidemiological significance for malaria transmission in the Thar Desert (Tyagi 1995a, b, 2020) the species has assumed an unparalleled universal significance in the realms of malaria research. Under the changed dynamics of phenotypic and genotypic plasticity, the dubious status of its species complex, the enigmatic broad behavioural spectrum, e.g., endophily/exophily and endophagy/ exophagy, and rare activity to overwinter in both larval and adult stages during cold months when temperature crosses approx. 50 °C, render An. stephensi an altogether different identity and definition (Tyagi 2002). The urban ‘Type’ species (An. stephensi s.s.) is highly anthropophlic/anthrophagic particularly when people, such as those practicing water storage in a variety of containers in high-rise multistorey buildings, a rising urban trait, are more active outdoors during warm months (Rao 1984), and therefore an increased risk of malaria transmission (Subbarao et al. 2019; Rajagopalan et al. 1987; Tyagi pers. comm.). In general, malaria is considered to be a disease confined to rural environments, as a simple consequence of the tendency of anophelines to search for clean and unpolluted larval habitats, and thus the existence of An. stephensi in such areas is a defining new characteristic of the species. In India, Sharma et al. (1969) were among the first to have given a clear picture of the polytene chromosomes of An. stephensi stephensi. Anopheles stephensi Liston s.l. is regarded to have three subspecies or strains, viz., the type subspecies, variety mysorensis, and an intermediate. These are classically distinguishable through cytogenetic techniques (WHOSEARO 2007) (Fig. 9.8), although recently even more powerful molecular tools have reconfirmed their presence. The type form is a strong vector and occurs in urban agglomerations; mysorensis is a poor rural vector in certain pockets, while intermediate is not showing any trait to assert it is a vector of concern. In the Thar Desert region, Anopheles stephensi is the major vector of malaria. In certain parts of Iran An. stephensi var. mysorensis was found as the only vector transmitting malaria. In these areas, animal hosts were very low in number or were totally absent. It is most interesting to note here that very recently this species is speculated to be a complex based on examination of odorant binding protein 1 intron I sequence in An. stephensi specimens collected from Iran and Afghanistan (Firooziyan et al. 2018). The three biological species recognized as species A, B, and C correspond to type form, intermediate form, and var. mysorensis, respectively. Singh et al. (2021a, b) have refuted existence of the biological species. According to them, AsteObp1 cannot serve as a marker for the identification of biological forms of An. stephensi. The probable existence of sibling species in An. stephensi based on the AsteObp1 intron-1 is thus refuted.

9.3 The Enigmatic Status of Anopheles stephensi X

2

167

3

4

5

c a i1

f1

p1 c

p1 g1.d a

c d

i1

f1

o1

q

c1 f1 a.b d

e1.g1 d e1.f1

r1 n1

c.c1 b d1

c a

c.b1 d1.h1 b b1

q

q1 m1.n1.r1 o1

q1 m1

g1 h1

h1

b

g1 h1

Fig. 9.8 Photomap of An. stephensi polytene chromosomes showing the break-points of the inversions (Source: WHOSEARO 2007; allowed with acknowledgement)

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Sibling Species Complexes of Malaria Vectors in Major Deserts

Since An. stephensi is principally an urban vector, its control is naturally beset with certain comprehensible operational constraints such as refusal of inhabitants to allow spraying on the walls due to fear of stains left behind, repulsive smell of the insecticides deployed in spraying, and, above all, contamination of living environment. Therefore, the main strategy to interrupt malaria transmitted by An. stephensi in urban areas is generally based on larval control under the urban malaria scheme, also followed by National Centre for Vector Borne Diseases Control (the erstwhile Vector Borne Disease Control Programme, NVBDCP). However, in rural areas of Rajasthan where this species is reported resting and biting indoors, the indoor residual spraying is additionally practiced. Reacting to the excitorepellent properties of insecticides like the DDT in Rajasthan, An. stephensi shifted much of its resting behaviour from resting on walls during the pre-DDT era to that of the household objects (e.g., hanging clothes, furniture, stacked clothes), to prevent contact with the insecticide-sprayed surface on the wall.

Anopheles stephensi Liston 1901: Origin and Chorogeography—A New Hypothesis

10.1

10

Introduction

Anopheles stephensi is an important malaria vector in several Middle East and South Asian countries, most eminently in the urban India as well as its vast expansion in the Thar Desert region (Zahar 1985, 1990a, b; Tyagi 2002; Ishtiaq et al. 2021). About 12% of malaria cases in India are due to An. stephensi (Sharma 1999). Apart from malaria, in which case it is a serious vector for Plasmodium falciparum, the mosquito An. stephensi is a vector of bovine leukaemia virus (Anon. 2019) and Plasmodium berghei (Mack et al. 1979). Anopheles stephensi is included under the same Subgenus—Anopheles—as is Africa’s deadliest malaria vector, An. gambiae (Valenzuela et al. 2003). However, though An. gambiae consists of a complex of morphologically identical species of mosquitoes, along with all other major malaria vectors (An. arabiensis, An. funestus, and An. sergentii), An. stephensi has not yet been identified to comprise any sibling species complex (cf. Firooziyan et al. 2018), albeit two races in existence based on differences in egg dimensions and the number of ridges on the eggs (Malhotra et al. 2000), exhibiting differential potential for malaria transmission: 1. Anopheles s. stephensi s.s., or the ‘type form’ (14–22 ridges on the egg-floats; Subbarao et al. 1987), is the most dangerous malaria vector among all three forms in the urban areas of India (Sharma 1986a, b) (Fig. 10.1). The ‘type form’ is never encountered in rural areas (Subbarao et al. 1987). It is noteworthy here that the species status of the desert specialist and the originally most dominant vector, An. stephensi, which has been prominently incriminated in the Thar Desert, is still evading a proper resolution (Tyagi et al. 1991). Indeed the Thar Desert’s An. stephensi is neither ‘mysorensis’ nor ‘intermediate’ form which only occur in rural environments, and certainly absolutely inevitably different from the ‘type’ form, which has no distribution outside the urban habitations. Recently Chakraborty (2021) decoded the genome of An. stephensi and shed a new light on genome evolution and phenotypic variations in the species via novel species-specific transposable element (TE) families and insertions in functional # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_10

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Anopheles stephensi Liston 1901: Origin and Chorogeography—A New Hypothesis

Fig. 10.1 Anopheles stephensi Liston 1901 (Source: Free Wikipedia)

genetic elements. They revealed new candidate genetic elements and such 29 hidden members of insecticide resistance genes which were previously unknown. They also identified seven new male-linked gene candidates, by far the highest for any mosquito, and 2.4 Mb of the Y chromosome. The Y-linked heterochromatin landscape revealed extensive accumulation of long-terminal repeat retrotransposons throughout the evolution and degeneration of this chromosome. More recently, Thakare (2022), working genomics on a 2016-collected Chennai (IndCh) strain of An. stephensi, reported the genome assembly of the type-form. The genome reported with an L50 of 4, completes the trilogy of highresolution genomes of strains with respect to a 16.5 Mbp 2Rb genotype in An. stephensi known to be associated with adaptation to environmental heterogeneity. 2. Anopheles s. mysorensis, the ‘variety form’ (9–15 ridges on the egg-floats; Subbarao et al. 1987), exists in rural and semiurban areas and exhibits considerable zoophilic behaviour, making it a poor malaria vector in western and peninsular India (Rao 1984; Malhotra et al. 2000), but a highly detrimental vector species in certain areas of Iran (Sinka et al. 2011), and, 3. Anopheles stephensi ‘intermediate form’ (12–17 ridges on the egg-floats; Subbarao et al. 1987) also exists in rural communities and peri-urban areas, though its vector status is unknown (Basseri et al. 2008; Sinka et al. 2011). Chavshin et al. (2014) have recently molecularly characterized all the three biological forms and highlighted the malaria transmission potential of Anopheles stephensi in southern Iran by counting sporozoite rate. In the backdrop of information of three forms of An. stephensi, Tyagi et al. (1991) had demonstrated that the Thar Desert populations of An. stephensi are of relatively larger size (likely ‘type’ species) than those found in other parts of India and

10.2

Classification

171

elsewhere and propounded his hypothesis of the possibility of a sibling species complex for An. stephensi. Recently, Firooziyan et al. (2018), based on odorant binding protein Ansteobp1 (OBP1) intron I sequences, introduced a new robust molecular marker for identification of its biological forms, viz., mysorensis, intermediate, and type, using insectary colony specimens in Afghanistan. They suggested as new Anopheles complex species including An. stephensi sibling A (type form), An. stephensi sibling B (intermediate form), and An. stephensi sibling C (mysorensis form). This is the first molecular markers’ evidence-based scientific report on the existence of An. stephensi sibling species complex. Khan et al. (2020) have further provided information on morphological and molecular characterization of mysorensis biological form, and, based on gene sequence analysis for COI, COII, ITS2 and OBP1 intron I, confirmed the presence of An. stephensi sibling C (mysorensis biological form), while working in China.

10.2

Classification

Anopheles stephensi is an extraordinarily elegant mosquito adorned with heavily spotted upper legs, mouthparts, and wings (Fig. 10.1). My experience for sampling the adults in resting condition, particularly when they are resting on hanging objects by roof, will guide me to spot the females in the torch-lit flash-lights as ‘the glittering stars’ that this species will appear to make in the pitched-dark night. Three egg phenotypes, based on varied dimensions of size and number of ridges on the floats, have for the past several decades been regarded to exist in the species, viz., type (Liston 1901), mysorensis (Sweet and Rao 1937), and intermediate (Subbarao et al. 1987). In contrast, WRBU (2022) informed on the genetic analysis of An. stephensi (wherein four synonyms are on record: metaboles Theobald, intermedia Rothwell, folquei de Mello, and mysorensis Sweet & Rao) using mtDNA COI barcoding that clearly indicates two separate taxa: (1) one in India, Pakistan, Djibouti, Ethiopia, and derived colony strains, and (2) another distinct species-level group originating in Saudi Arabia. In view of the continuous zoogeographic expansion, often transboundary (i.e., from across India to others), in parallel to anthropically induced climate change, today An. stephensi emerges the only other mosquito, and the only anopheline, after Wyeomyia smithii, which is known as the first animal model to demonstrate global warming impact of climate change on life (Bradshaw and Holzapfel 2001), that is again proving the phenomenon albeit a different factor in consideration this time, i.e., rise in urbanization, prompting movement of An. stephensi over to new and unexplored areas (countries or regions), hitherto terra incognito for the intruding or invasive species! The species appears to be on the move with climate change, demographic vicissitudes between rural and urban settings, and social behaviour with respect to increased water storing habit (Surendran et al. 2019). Discovery of An. stephensi (type form) in 2014 from Djibouti, followed by its reporting from several localities in Ethiopia and the Republic of Sudan, marked its first incursion onto the African continent, and introduction as the first urban malaria vector on the

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African continent. Around the same time, An. stephensi (type-form) intruded Mannar Island, Sri Lanka, a largely sylvatic environment. Anopheles stephensi is perhaps the world’s most enigmatic species, which has raised a very interesting debate on whether it is a species complex or not. There is no species with which An. stephensi can well be confused; it is the only Indian as well as global species, with broad thoracic scaling and a double broad pale band on the palpi, in which the hind legs are not conspicuously with white. The species has such marked features which make it distinguishable most comfortably from any other anopheline species without an iota of scepticism. The species is classified as follows: Phylum Class Order Family Subfamily Genus Subgenus Series species

10.3

Arthropoda Insecta Diptera Culicidae Anophelinae Anopheles Cellia Neocelli stephensi

Etymology of Anopheles stephensi

The species Anopheles stephensi, discovered by Lt. Col. William Glen Liston in 1901, is derives its name after the famous malariologist and medical entomologist Professor J.W.W. Stephens. The type locality of Anopheles stephensi is Ellichpur in Vidharbha area of Maharashtra State, India. The type specimen of a female Anopheles stephensi is deposited in the Natural History Museum, London.

10.4

Distribution

Originally an Indian species (originated likely in the Thar Desert) it has now a wide distribution in Asia, Middle East, Arabian Peninsula and north-eastern Africa including Afghanistan, Bahrain, Bangladesh, Djibouti, Egypt, Ethiopia, India, Iran, Iraq, Kuwait, Myanmar, Nepal, Oman, Pakistan, People’s Republic of China, Philippines, Qatar, Saudi Arabia, Somalia, Sri Lanka, Sudan, Thailand, United Arab Emirates and Vietnam (Fig. 10.2) (Christophers 1933; Rao 1984; Surendran et al. 2019).

The New ‘Out of Range’ Occurrence of An. stephensi Since. . .

10.5

173

Decade

1980 – 1989 1990 – 1999 2000 – 2009 2010 – 2019 year unknown An. stephensi EO

Fig. 10.2 The latest ‘out of range’ occurrence of An. stephensi in the Arabian Peninsula and Horn of Africa. Note: The 358 site locations for species distribution models (SDMs) were used as: Yellow-shaded area shows the 2011 expert opinion range based on data published up to 31 October 2009; Data showing the presence of An. stephensi more westerly across the Arabian peninsula (sampled in 2005–2006) were published after 2010. Thus, An. stephensi may have been present but unreported or been expanding its range into the western areas of the Arabian peninsula over the last 30 years (Source: Sinka et al. 2020)

10.5

The New ‘Out of Range’ Occurrence of An. stephensi Since Early Twenty-First Century

The acknowledged zoogeography of An. stephensi encompasses southern Asia and the Arab Peninsula, including India, Pakistan, Afghanistan, Iraq, Iran, Baharin, Oman, Saudi Arabia, Bangladesh, South China, Myanmar, and Thailand. Although Rao (1984), citing Gad (1967), informed that An. stephensi, being the first record on the African continent, showed its existence in Sinai, Egypt, about 1.5 km from the Suez Canal, but later this claim was confounded (cf. Manouchehri et al. 1976). According to Zahar the identification of this new find from Egypt was checked by Dr P. F. Mattingly (British Museum, Natural History) who found it resembling A. dancalicus Corradetti, thereby stripped off its identification as An. stephensi for future reference. Five decades later, however, An. stephensi firmly established itself in the African continent, without an iota of scepticism this time, alarming nations for its impact on their disease elimination campaigns. Anopheles stephensi seems to be spreading in geographic expansion within South Asia (Sri Lanka 2016; Dharmasiri et al. 2017; Surendran et al. 2018, 2019; Abubakr et al. 2022), the Middle East, and Africa (Djibouti in 2012, Ethiopia in 2016, Sudan

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in 2018/2019, and Somalia; Balkew et al. 2020; Seyfarth et al. 2019; Carter et al. 2018; Faulde et al. 2014; WHO 2021a, b; Mnzava et al. 2022; Ahmed et al. 2022), and there is growing evidence that this species might soon be expanding, if remains unchecked, its geographical range would affect approximately 126 million people in cities across Africa alone (Sinka et al. 2020). Due to its high degree of anthropophilic behaviour, invasion of new geographic ranges, hitherto regarded terra incognito for An. stephensi, has certainly raised many new challenges and threats to the policy designers to thwart any attempt of either re-emergence of malaria (from a country such as Sri Lanka which was declared malaria-free in 2016 by World Health Organization) or establishment in, Egypt, Ethiopia, and Sudan in north-eastern Africa about which World Health Organization has called upon to remain vigilant (Sinka et al. 2020).

10.5.1 Gulf Countries The oriental malaria vector An. stephensi is present over a fairly large area in the northern and eastern parts of the Gulf region. Anopheles stephensi mysorensis has been identified in the Eastern Province of Saudi Arabia and in southern Iran.

10.5.2 Africa In contrast to the endemic African mosquitoes (e.g., An. gambiae, An. arabiensis, An. funestus), the Asian malaria vector Anopheles stephensi is possibly the only malaria mosquito yet known on the soil of Africa which is urban savvy, alluding to its ability to quest for potable water in any kind of container to lay its eggs. Lack of its propensity to breed in transient water bodies such as puddles or ditches, often found to be turbid or polluted (e.g., with oil or sewage) in urban settings which repel pollution-sensitive anophelines such as An. stephensi, the latter is so far confined to freshwater containers only. However, there is increasing evidence that some African species are increasing their tolerance against polluted and/or turbid water, and the void is amply compensated by An. arabiensis—a member of the An. gambiae complex and a desert specialist, which breeds in polluted, turbid water, just as in clear, clean habitats, although unlike An. stephensi, it remains solely a rural environment breeder.

10.5.3 Middle East and West Asia Anopheles stephensi, in all of its three forms, i.e., ‘type’, ‘intermediate’, and ‘mysorensis’ forms, is quite common in Pakistan, Afghanistan, and southern Iran (e.g., Abadan, Bandar Abbas, Kazeroun and Dezfu, Jiroftl) (Mehravaran et al. 2012). There it is highly anthropophilic, too (15.7%) (Manouchehri et al. 1976). While An. stephensi stephensi (type form) and ‘intermediate’ occur in urban and urbanized

10.5

The New ‘Out of Range’ Occurrence of An. stephensi Since. . .

175

coastal areas with the type form predominant, An. stephensi mysorensis is found only in rural mountainous areas (Vatandoost et al. 2006). Both the type form in urban areas and mysorensis in rural areas are competent malaria transmitters, albeit the latter being a weaker vector carrying a lower vectorial capacity. Against various types of adulticides, such as bendiocarb, propoxur, malathion, fenitrothion, deltamethrin, permethrin, cyfluthrin, and lambdacyhalothrin, all these forms of the species exhibit susceptibility, save for one case of resistance against DDT, together with low level of tolerance to dieldrin. In contrast to imagicides all the stephensi forms are susceptible to malathion, fenitrothion, temephos, and chlorpyrifos at diagnostic doses, except the larvicide fenitrothion. Pyrethroid insecticides like permethrin and lambdacyhalothrin highly irritate the vector species, but have low irritability to cyfluthrin and deltamethrin. Abai et al. (2008) compared the performance of imagicides on Anopheles stephensi in southern Iran.

10.5.4 The Thar Desert In terms of medical importance Anopheles stephensi is but next only to An. culicifacies and A. fluviatilis in India (Christophers 1933; Zahar 1988, 1990a, b; Rao 1984), although Tyagi (1991a–c, 1995a, b) has demonstrated for the first time its predominance and epidemiological significance in the arid environments of the Thar Desert—a unique ecosystem with which one usually does not associate malaria. Common sense dictates that mosquitoes that breed only in stagnant water would give arid, water-scarce spaces such as a desert a wide go-by. But that is not the case in the Thar Desert in north-western Rajasthan, India, which is also the land of persistent desert malaria (Anon. 2003). Amerasinghe (2004) has dedicated this pathbreaking research finding to ‘long years of research into mosquitoes, malaria and irrigated agriculture in the Thar Desert’ by Tyagi between 1988 and 2001, and again 2015 onward (cf. Veer et al. 2021). In cognizance of the fact that An. stephensi is the original species from the Thar Desert’s arid environments, adapted to breed in fresh water, and there too mostly in potable water, a highly carefully planned vector control without facing protest by the village communities needs to be enacted to interrupt the malaria transmission cycle (Tyagi 2020; Singh et al. 2021a, b). The matter of controlling malaria in the mobile and difficult-to-approach people of the Thar Desert appear simple but it is in fact highly complicated considering the transient human behaviour involved in the mobile and hard-to-approach populations (Tyagi 2022). The Thar Desert in the north-western Indian province of Rajasthan (23°–30° N and 69°–78° E), lying between the irrigated lands of the rivers Indus and Sutlej in the east and the western edge of the Aravalli Hills, is the only desertic ecosystem in the country which supports a unique malariologic paradigm, ‘The Desert Malaria’. Organized into 12 desert districts spread over 75,000 km2, it harbours a population of 12
8 million. Until the 1980s it was regarded as a hypoendemic region of unstable malaria with potential for occasional outbreaks. However, due to a mélange of factors such as anthropization including extensive irrigation canal-network and

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climate change, the Thar Desert has at present transformed into a towering inferno of cyclic malaria epidemics dominated by Plasmodium falciparum. The Thar Desert’s inhospitable conditions make human living extremely challenging. Populations living deep inside desert are hardly accessible by health care provisions which render them vulnerable to malaria-related morbidity and mortality, particularly infants and pregnant mothers. Humans live in sparsely and distantly located habitations called ‘Dhani’—which can be one-to-few dwellings, in addition to villages in the far flung remote areas, hardly interconnected with motorable passages ever. Such ‘Dhanis’ as well as villages essentially associate with the ’Tanka’ or ‘Beri’—their indigenous innovations to conserve water as underground reservoirs to meet their and animals’ vital needs round the year, perhaps more (Fig. 10.3)! The desert malaria vector, An. stephensi, profusely breeds in these marvellous engineering feats, spreading malaria through transmission of P. falciparum and P. vivax. Human populations in ’Dhanis’ and villages are generally at the Nature’s mercy when sickened due to malaria, despite a well-placed health care delivery system. Its noteworthy that Primary Health Centres (PHCs)/Drug Distribution Centres (DDCs) with their multi-tasked staff called Multipurpose Health Worker (MPWs), Lady Health Worker (LHW), and/or Auxiliary Nurse Midwife (ANM), located at places far from ‘Dhanis’, find it extremely cumbersome to make regular active surveillance. Tyagi (2002, 2020, 2022) carried out long-term investigations into the eco-biosocial aspects of malaria on these mobile and hard-to-reach populations during 1988–2001 and 2015–2022, and it was revealed that the ‘Dhani’-inhabitants were at high risk of malaria infection. They were not only heavily malariated en masse but almost inevitably lost precious time to either set out to access or to be accessed for antimalarial treatment on time. Due to this ‘disconnect’, their knowledge about malaria was also found to be clouded with uncertainties. They hardly knew the role of mosquitoes in malaria transmission, particularly An. stephensi, breeding in their only water reservoirs, ‘Tanka’ and ‘Beri’, a stone’s throw from the dwellings. During malaria outbreaks the ‘Dhani’ inhabitants are hard to approach and timely delivered treatment as an active surveillance measure. Since draughts in the Thar Desert have been a recurring phenomenon every few years, the life of the desert population, along with their cattle (camel, goat etc.), is doubly challenged for survival. Thus, they are forced to set out in quest for green pastures more than 1000 km away across the interstate borders over to other neighbouring (malaria) hyperendemic States, e.g., Gujarat and Haryana. On return, however, they bring malaria infection to their habitats in the Thar Desert where again they are hard to reach. After the massive desert malaria epidemic in 1994 (deaths >300), the scenario has changed (0 death in 2020), thanks to communication technologies, advanced training, and regular exercise with Knowledge, Education and Practice (KAP), the health department is optimally providing medical aid to such mobile and hard-to-reach populations to prevent morbidity and mortality, but still much is possibly desired to achieve the goal of malaria elimination.

10.5

The New ‘Out of Range’ Occurrence of An. stephensi Since. . .

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Fig. 10.3 (a, b) ‘Beri’—the man-made underground well-like structure in the cavity of a pond naturally recharged by occasional rains with a gap of several years; (c) Each mound of stones in the middle of the near-dry belly of the pond marks the entry to a ‘Beri’ from where the local folks draw a pail of water (Source: Tyagi and Yadav 1996a)

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Anopheles stephensi Liston 1901: Origin and Chorogeography—A New Hypothesis

The Original Desert Mosquito: Anopheles stephensi

Anopheles stephensi is malariologically both important and enigmatic. Discovered at Ellichpur, Vidharbha area of Maharashtra State, India, Dr William Glen Liston scientifically described it from a single female specimen in 1901. It is interesting to note here that Ross (1897) had claimed the mosquito, on which he had founded his epochal theory about the discovery of malaria–mosquito relationship, to be possibly An. stephensi—his ‘dappled winged mosquito’ or ‘Mosquito C’! Ever since the species was described it has been subjected to continuous scrutiny for its gargantuan potential to transmit human malaria, in general, and P. falciparum, in particular. Also its status as a species or complex of species has always been intriguing the scientists. At least three synonyms were put forward in the course: (1) metaboles Theobald, 1902, (2) intermedia Rothwell, 1907, and (3) folquei de Mello, 1918. In addition to the nominal subspecies stephensi Liston 1901, two more subspecies (or varieties) have also been brought on record, namely, mysorensis Sweet and Rao (1937) and intermediate Subba Rao et al. (1987). Anopheles stephensi is amongst the most investigated mosquito species, yet there are many traits which are either incompletely understood or not known at all. The following attributions make An. stephensi the most sought-after malaria vector and still so enigmatic and quaint to science: 1. An. stephensi (type species) is pronouncedly urban in nature as a vector; however, it is 100% vectorial in the Thar Desert’s arid environments. 2. An. stephensi is preferably zoophilic (Rao 1984), but human blood index (HBI) is reported as high as 37.5% (Nair and Samnotra 1967) in India. 3. An. stephensi, with a spectrum of three subspecies, stephensi, mysorensis, and intermediate, is a vector in both urban and rural agglomerations. 4. An. stephensi is a pollution-sensitive species, inherently inclined to breed in clean potted water of most kinds which are generally man made. 5. An. stephensi can breed prodigiously in both wells as deep as 30–40 ft and overhead tanks in high rise buildings (>50 ft). 6. An. stephensi is able to overwinter in the Thar Desert, but not reported elsewhere. 7. An. stephensi is able to manifest the phenomenon of reflex immobilization or thanatosis (death-feigning) as a defence mechanism. 8. An. stephensi can transmit both P. falciparum and P. vivax parasites, but its potential to transmit the former is threatening especially in newly invaded nations of Africa and Sri Lanka. 9. An. stephensi has evolved as a strong synanthropic mosquito; it tends to move with humans in their trade, travel, and settlements, since in all these events the mosquito can find in plenty its breeding ground, the fresh potted water. 10. An. stephensi is recently attempted to be proven a species complex with a greater degree of scientific experimentations (Firooziyan et al. 2018), even though Tyagi et al. (1991) had pointed out about the same on the basis of morphometric studies. Still there are studies which try to prove otherwise; Alam et al. (2008) and Islam

A New Hypothesis on the Origin and Evolution of Anopheles stephensi

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et al. (2017) have demonstrated that the type and mysorensis forms of An. stephensi in India exhibit identical ribosomal DNA ITS2 and domain-3 sequences.

10.7

A New Hypothesis on the Origin and Evolution of Anopheles stephensi

10.7.1 The Hypothesis Based on the Rule of Reinig (1938, 1939) Since the Darwin (1859) theory of origin of species by means of natural selection, many zoologists have propounded several chorogeographic hypotheses most tenable among which has in recent times been that by Reinig (1938, 1939), although Kiauta (1968), who studied morphological and kinetical features of the so-called mchromosomes in dragonflies worldwide, refuted its validity entirely on the basis of m-chromosome variability among various populations. Nonetheless he emphasized that the relative size of the m-chromosomes varies in some species, but not in all, and that the size is peculiar, in some dragonflies, for populations originating from different portions of the species range, and therefore it could be used to advantage in the taxonomy of infraspecific forms. Reinig’s (1938, 1939) chorogeographic hypothesis explains that populations of a given species evolved near the point of origin have larger size in comparison to those borne far away from it! This implies that, as far as An. stephensi is concerned, the size of specimens of the populations from the leveed Thar Desert environment, which here is believed to be the cradle of this species, must be larger than all those occurring elsewhere, in south India, Sri Lanka, Middle East, Arabian Peninsula, or ‘the Horn of Africa.’ A fair test of this hypothesis will explain it all.

10.7.2 The Basis To test the Rule of Reinig (1938, 1939), it is desired foremost to put morphometric attributes of the species existing in the Thar Desert as well as those (species or subspecies) found in other parts of the world (Table 10.1). From the tabulated data it is comprehensible that the type An. stephensi extant in the arid environments of the Thar Desert seems to have an edge in morphometric measurements over others of the same clan, which in a way justifies the application of the chorogeographic hypothesis of Reinig (1938, 1939) in the case of An. stephensi (Fig. 10.4), and supports the hypothesis alluding to its origin in the Great Indian Thar Desert region. An appreciable degree of intra-specific variation in An. stephensi is a testimony to the species’ plasticity and adaptability potential to survive in ecologically different biotopes (Krishnan 1954; Tyagi 1995b). In the Thar Desert, there is only one published scientific study on the intra-specific variation in An. stephensi (Tyagi et al. 1991). Females of An. stephensi examined in this study originated from a group of ten highly irrigated villages of Sangaria Tehsil and another group of six

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Table 10.1 Frequency (f) of selected characters of feral females of two geographically isolated populations of An. stephensi

Part of the body Head Palpi

Thorax Wing

Legs

a

Standard characters (1) Vertex with nine flattened chaetae forming frontal tuft (1) Base swollen (2) Segment half or more than the preceding segment (index 0.58) (3) Patches (2–3) of white scales on dorsum of palpi (1) Mesonotum covered by scales (1) Prehumeral accessory dark spot undivided (2) Anal vein with three dark spots (1) Front femur swollen at base (2) Speckles distinctly (3) First tarsus with 2–3 patches

Villages of SuratgarhAnupgarh tehsil (25)a f (No. of specimens examined) 0.08 (2)

Villages of Sangaria tehsil (10)a f (No. of specimens examined) 0.90 (9)

Range between populations (%) 8.0–90

1.0 (25) 0.8 (20)

1.0 (10) 0.9 (9)

Nil 80–90

0.8 (20)

1.0 (10)

80–90

0.92 (23)

0.5 (5)

50–92

0.90 (24)

0.9 (8)

90–96

0.56 (14)

1.0 (10)

56–100

1.0 (25)

1.0 (10)

Nil

0.04 (1) 0.8 (20)

1.0 (10) 0.9 (9)

4.10 80–90

Figures in parentheses show the number of females examined

unirrigated villages in totally desertic environment of Suratgarh-Anupgarh Tehsils in Sri Ganganagar district (Fig. 10.5). Frequency of selected characters in the feral females examined from physiographically isolated areas is given in Table 10.1, whereas degree of variance in the measurement of different body parts in the females examined from both the areas is given in Table 10.2. Differences in various different kinds of body parts can be summarized as follows: (1) Palpi and Head: The palpi differed remarkably in size, speckling and extent of white bands. In the desert specimens, the smallest palpi (1.4 mm) are equal to the largest in the Sangaria specimens (1.5 mm). The apical and subapical white bands are contiguous laterally, with the former often longer in size. Nearly all Sangaria specimens (90%) had nine flattened chaetae in the frontal tuft, but very few specimens in the desert villages (85%) had such a situation, (2) Mesonotum: Desert specimens usually had more conspicuous mat of pale scales on the mesonotum extending somewhat posteriorly to scutellum and to the lateral aspects of dorsum,

10.7

A New Hypothesis on the Origin and Evolution of Anopheles stephensi

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Fig. 10.4 Average difference in palpi size between (a) desert and (b) non-desert populations of Anopheles stephensi Liston 1901 (Source: Tyagi et al. 1991)

(3) Wings: In several specimens from both the Sangaria villages and the desert villages in Suratgarh/Anupgarh tehsils the prehumeral dark accessory spot was found split into an inner and outer dark accessory spot. The largest specimen (5.3 mm) collected from the above desert villages measured 7.8 mm across the wings. The largest specimen (4.0 mm) collected from Masani village in the Sangaria Tehsil measured 5.0 mm across the wings, and, (4) Legs: Femur of the foreleg was swollen in all specimens but there was variation in the pattern of speckling of femur, tibia, and the first tarsal segment in the females of both ecotypes. While speckles in Sangaria specimens were far more distinctly pronounced, in the desert specimens these are irregular in shape and often contiguous. The first tarsus has a few white scales at 2–3 places, although these white scales were sometimes obscured in the desert specimens.

10.7.3 The Evolution and Migration Pathways of New Species or Subspecies to Other Regions Anopheles stephensi originated, in every likelihood, in the Thar Desert region of north-western Rajasthan state of India, from where several decades or even centuries ago it must have migrated to Southeast Asia and the Arabian Peninsula. It has recently emerged as an efficient and invasive urban malaria vector in Africa, intruding four countries (Djibouti, Ethiopia, Somalia, and Sudan) within a short

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Fig. 10.5 Variations in proboscis (A,B), legs (1,2,3), and wing parts of An. stephensi collected from desert and non-desert areas in the Thar (Ph/h prehumeral/humeral dark spot) (Source: Tyagi et al. 1991)

span of only 7 years (2012–2019); Djibouti being the foremost ‘invaded’ destination in Africa in 2012 and Sudan the latest in its intrusions in Africa (2019). Compared to all major malaria-endemic deserts of the world, the Thar Desert in the north-western India seems to have undergone a more severe catastrophic

Suratgarh/Anupgarh tehsil (10a) Range (mm) Mean Standard deviation 1.4–1.9 1.05** 0.19 1.4–1.9 1.6** 0.19 5.1–5.3 5.23** 0.08 3.0–3.8 3.7** 0.29 5.1–5.5 5.35** 0.15 5.8–6.3 6.08** 0.154 6.2–7.2 6.8** 0.355

Figures in parentheses show the number of females examined **P < 0.001

a

Part of the body measured Palpi Proboscis Full body length (including palpi) Wing length Foreleg Midleg Hindleg Variance 0.036 0.036 0.006 0.084 0.022 0.024 0.126

Sangaria tehsil (10a) Range (mm) Mean 0.9–1.5 1.11 0.9–1.5 1.13 4.0–4.4 4.15 2.4–2.6 2.47 4.4–4.7 4.57 5.2–5.3 5.24 5.9–6.0 5.92

Standard deviation 0.172 0.182 0.135 0.082 0.125 0.051 0.042

Variance 0.029 0.0334 0.0183 0.0062 0.0158 0.0026 0.0014

Table 10.2 Degree of variance in the measurement of various body parts in females of An. stephensi collected from physiographically different areas of highly irrigated villages of Sangaria tehsil and unirrigated villages of Suratgarh/Anupgarh tehsil in Sri Ganganagar

10.7 A New Hypothesis on the Origin and Evolution of Anopheles stephensi 183

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Fig. 10.6 Schematic representation of a possible ‘uniparous helicoids cyme’ type (blue arrows) of chorogeographic evolutionary pathway of Anopheles stephensi, or its races/subspecies/sibling complex species first to West Asia/Middle East/Arabian Peninsula and finally to the ‘Horn of Africa’ (Source: B.K. Tyagi, original this work)

physiographic change. It is on record that the Thar Deserts various parameters have so changed as to favour mosquito (An. stephensi) density, proliferation, and expansion. While the ambient temperature in the IGNP region has decreased, (on the one hand), the rainfall has significantly increased, on the other. The other factor, human density, too, has increased several times, and so has diversified the mode of transportation. All these factors seem to have in modern times favoured a significant change in behaviour and ecology of An. stephensi which began moving out of its cradle (the Thar Desert) in quest of more space for its successful survival (Fig. 10.6). A careful scrutiny of environmental vicissitudes, physiographic metamorphosis and phylodynamics of the desert specialist vector, An. stephensi—an Indian mosquito by origin, will reveal that there has been a direct correlation between extraterritorial movement of the species and the climate change, and the most characteristic factor involved in the process has been the urbanization—the newly mushrooming urban centres!

10.7.4 Test of Bergmann’s Rule on the Origin of Anopheles stephensi Notwithstanding the fact that the Bergmann cline, most often applied to mammals and birds, is difficult to predict in poikilothermic insects, such as mosquitoes, nevertheless, it seems adventurous enough to see that by putting credentials of morphology of An. stephensi to the Bergmann’s Rule, whether it can be further elucidated to pinpoint on the cradle point of the mosquito, i.e., the Thar Desert? The Bergmann Rule (1847) explains that those species, populations, or individuals born at high altitudes, with slow development process due to lower temperature, seem to

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A New Hypothesis on the Origin and Evolution of Anopheles stephensi

185

develop larger body size than those in relatively lowlands, with high temperature and quick developmental process. Bergmann’s Rule is applicable to whole body size and not the body parts. Now, let us consider different locations of An. stephensi, in The Thar Desert, in other parts of India, in Middle East and in the Horn of Africa. It is notable that most of central and southern Indian plateaux (e.g. Delhi), coastal metropolises (e.g., Mumbai, Chennai, Kolkata) are at a lower altitude, with the latter group of cities with warmer climate more or less throughout the year. While An. stephensi ‘type form’ is common in all the metropolitan towns, it is mostly An. stephensi mysorensis that is widely distributed in the peninsular rural plains (Rao 1984). Close to the peninsular tip of India, in Sri Lanka it is An. stephensi ‘type-form’ detected for the first time in Mannar Island—sylvatic environment with nearly uniformly warm temperature. In Middle East, in northern Iran, mostly it is the ‘mysorensis’ form. In contrast, the Thar Desert ecosystem, with both large-sized populations in the penetralium of the desert and the relatively small-sized populations in the IGNP Command Areas under irrigation, enjoys a relatively higher altitude, with far lower precipitation and extreme temperature ranges in summer and winter months, more or less in accordance with similar factors in both the Peninsular and Saharan deserts. The Thar Desert is the only ecotype rife with the An. stephensi populations throughout its expanse, while both the Arab Peninsula and the African Sahara deserts are but recently inhabited or invaded by the vector, pointing out towards a possible pathway commencing out of the Thar Desert into the African Continent via Arab Peninsular deserts (Fig. 10.6). Thus, it appears that though Bergmann’s Rule is not fully applicable in the case of An. stephensi, it nevertheless tries to explain the evolutionary significance of two populations of the vector in the Thar Desert, hook, line, and sinker (Tyagi et al. 1991)!

Invasive Vector Species of Malaria in Desert Environments

11.1

11

Introduction

Species that reproduce quickly and grow stupendously in population structure, and disperse aggressively, with potential to cause harm, are labelled as ‘invasive’. Mosquitos and the infections they carry are travelling along trade routes and settling in ever-expanding cities. In as far as Culicidae is concerned, an invasive mosquito is a species that, by its introduction, causes ecological, economic or health-related harm in a new environment where it is not native. Human health and economies are at recurring risk from invasive mosquito species’ potential to affect a large number of vector-borne diseases. Such invasive species have an indelible, irreversible and multidimensional influence on our natural ecosystems, particularly in context with human health and economy, which may invite billions of dollars’ expenditure each year to counter its ill effects by way of recurring investments in vector and vector-borne disease interventions of different nature. Since healthy native ecosystems are essential to sustain many of our commercial, agricultural and recreational activities, therefore, it is desirable to keep a check on the invasion of such species of inimical attribute. Many countries across the world have faced a quaint yet tragic phenomenon of invasion by exotic mosquitoes, both in tropical and temperate regions. In as far as malaria is concerned, the Asian An. stephensi and the African An. arabiensis are the only two species which have very recently invaded either different lands within the same country (e.g. An. stephensi in Lakshadweep in 2001 and Rameswaram ils. in India), isolated island countries (e.g. An. stephensi in Sri Lanka in 2017) or intercontinental regions (e.g. An. arabiensis in Natal, Brazil, in 1930) hundreds and even thousands of kilometres away from their respective original habitat. However, in the past several invasive malaria vector species had been brought on record: (1) An. dirus seems to have intruded India from across Myanmar borders during the 1970–1980s, and (2) An. stephensi was sampled for the first time in Kerala State from Kochi in 1992. Apart from Anopheles, other mosquitoes too have their own quota of invasive species, e.g. Aedes koreicus, an invasive species to India (Collector: Dr S.K. Ghosh; specimen identified at the ICMR-Centre for Research in Medical # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_11

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Invasive Vector Species of Malaria in Desert Environments

Entomology), near the Bengaluru Airport in 2013, and Aedes aegypti got introduced to the Lakshadweep il. in 2001. In Europe, five Aedes mosquito species are regarded invasive, namely, Aedes albopictus, Ae. aegypti, Ae. japonicus, Ae. koreicus and Ae. atropalpus (Cebrián-Camisón et al. 2020). Two of these invaders, viz. Aedes albopictus and Aedes aegypti, were also incriminated as vectors during the recent outbreaks of chikungunya and dengue fever in Europe. In the USA, other than Ae. aegypti and Ae. albopictus in the past, very recently even the presence of Ae. scapularis, a vector for many kinds of encephalitides, has been documented (Reeves et al. 2021). After Aedes albopictus, the only other invasive mosquito that has captured the mind of vector-borne disease specialists globally is Anopheles stephensi. However, unlike Ae. albopictus which has unleashed a worldwide threat for chikungunya epidemics in a very short time, An. stephensi, though slow, has already entered in Africa and, considering its ecology and behaviour, might as well cross over to the Americas in few decades from now! Currently, An. stephensi is rated as the most intrusive, invasive and ‘silent’ vector species in the world!

11.2

What Makes a Vector Species ‘Invasive’

Every species, including a vector, needs its specific food (blood for haemophagic vectors), shelter, interbreeding populations and, of course, breeding habitats. When it has reached a point of optimum in terms of utilization of space and time, population explosion, sex ratio imbalance and inter- and/or intraspecific competition, it tends to move out, sometimes in long-distance migrations, in the quest of easy and abundant resources or alternatives. In case of an invasive blood-feeding disease vector, the species intrudes a land (ecosystem, country or region) on grounds of heavy risks and uncertainties, the biggest of all being the pathogen’s response to the vector in a changed ecology and physiography. If the intruding vector (e.g. An. stephensi or An. arabiensis) receives well the biology of the pathogen (in this case a human malaria causing Plasmodium species) and is potent enough to effect successful transmission, then the vector turns out to be crowned ‘invasive’, and the taxon involved is labelled as an invasive species. It is a logical move forward (Perkins and Nowak 2013), implying that the phenomenon of conversion from ‘vector’ status to that of the ‘invasive vector’ is irreversible, in the outset at least (Tyagi, this work). The Species Survival Commission (SSC) of the International Union for Conservation of Nature (IUCN), looks into matters pertaining to the unharmed sustenance of all the biological entities and their habitats, including the invasive alien species (IAS) because these are regarded the main agent of biodiversity loss in protected natural areas. In Fig. 11.1, a hypothesis on the possible mode of reincarnation of a vector like An. stephensi into an ‘invasive alien vector species’ (IAVS) is graphically presented. The role of invasive vector species, such as Anopheles stephensi and An. arabiensis (the malaria vectors) and, for that matter, Aedes albopictus (the vector for dengue and chikungunya) as well as scores of other arboviruses, is not yet

11.3

Interplay Between Vector-Pathogen Interaction Dynamics and the Climate Change 189

Fig. 11.1 A graphical presentation of a hypothesis on the possible mode of reincarnation of an invasive vector species (IAS), e.g. Anopheles stephensi, into an ‘invasive alien vector species’ (IAVS)

established in context with the biodiversity dynamics, owing to the absence of any integrated multinational bioinvasive risk assessments (Ruiz and Carlton 2003; Brancatelli and Zalba 2018).

11.3

Interplay Between Vector-Pathogen Interaction Dynamics and the Climate Change

Long-distance crossovers of both disease pathogens and vectors between continents and/or regions have been greatly facilitated by the ever-increasing international trade by land, sea and air routes. Invasive vectors encounter a spree of challenges in the new lands where the environmental and climatic changes of foreign lands are likely to raise the risk of pathogen transmission by these invasive mosquitoes. Realizing the seriousness of the issues associated with invasive vector mosquitoes, the World Health Organization has taken a lead in developing a framework to enact actions if any invasive mosquito, particularly the vector, of public and/or veterinary health importance is documented in any country and all neighbouring nations’ health policy and intervention implementation managers of the receptive countries must be alerted forthwith (van den Berg et al. 2013). The invasive vector-resident pathogen relationship depends much on the dynamics of climate change that shapes the future of mosquito-borne disease epidemiology in the host country. For example, a striking escalation in temperature in Europe during 1980–1990 witnessed an unprecedented influx of the Asian tiger mosquito, Aedes albopictus, since the late 1990s whereafter it continuously expanded its distribution to new countries every year (Medlock et al. 2012). Along with the yellow fever mosquito Aedes aegypti, the Asian Tiger mosquito, Aedes albopictus, is a primary vector for chikungunya, and disease

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Fig. 11.2 Distributional range of Anopheles stephensi (Source: Ishtiaq et al. 2021)

outbreaks that Europe experienced during the mid-2005 were largely transmitted by it. It must be cautiously remembered, however, that an invasive species does not have to come from another country. While Tyagi and Yadav (1996a–c) and Tyagi and Hiriyan (2004) have elicited the invasion of the Thar Desert by the yellow fever mosquito, Ae. aegypti, more recently Tyagi et al. (2006) have demonstrated de novo invasion of the Western Ghats region in Kerala by the yellow fever mosquito, Ae. aegypti. In both these new ecosystems of invasion, the vector mosquito had either originated transmission of dengue and chikungunya such as that in the xeric environments of the Thar Desert or played a significant role in exacerbating both these infections. Deserts around the world, some of which are nefariously known for their hyperendemic nature for malaria, for example, Sahara Desert in Africa, are no exception and are rather deeply vulnerable to invasive mosquito species due significantly to human actions like the riverine and/or canalized irrigation, rare metal or ore mining where they colonize stupendously. Their occurrence is often associated with changes in ecosystems, human behaviour and climate (Randolph and Rogers 2010). The most glaring example of an invasive mosquito to the African continent where it is being widely feared to soon put more than 125 million city dwellers across Africa to face a higher malaria risk, is the Asian mosquito, An. stephensi, that is quickly moving across the continent and the eastern parts of Sahara Desert. Anopheles stephensi has rapidly extended its geographical range, with the type form being reported in the Lakshadweep islands (2001), in countries in the Horn of Africa (2012), Sri Lanka (2017) and most recently in the Republic of Sudan (2019). The introduced An. stephensi exhibits resistance to several classes of insecticides, posing challenges in controlling the spread to new areas (Fig. 11.2).

11.4

11.4

Invasion of Anopheles stephensi Within India

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Invasion of Anopheles stephensi Within India

As discussed in the previous chapter, it seems very likely that An. stephensi has its cradle point in the Great Indian Thar Desert from where, during the course of several decades’ long dispersal, the species spread far and deep in the mainland, particularly Peninsular India, on the one hand, and to the various neighbouring countries in the West Asia, on the other, all due largely and primarily to its strong affiliation for breeding in the fresh and potable water, an attribution of the water-deficient growing urban agglomerations and secondarily, and much to its advantage, a highly escalated population movement, massive new constructions and trade both within and across trans-international borders. Among all the known malaria vectors across the world, Anopheles stephensi Liston 1901 is possibly the most important invasive species at present, which has recently ventured to explore new habitats in Africa and South Asia, from its historically established abode in Asia and the Middle East. It is noteworthy to mention here that An. stephensi was discovered and reported for the first time in Ellichpur in Vidarbha area of Maharashtra State, India. In India it occurs in all the main zones, including the inhospitable arid environments of the Thar Desert (Tyagi 2002, 2003a, b, 2004a, b, 2020; Tyagi and Baqri 2005), becoming scarcer at high altitudes in the Himalaya and in the northeastern states. The species is wanting in the Andaman and Nicobar islands where malaria has been endemic in for nearly a century and An. sundaicus is the incriminated vector (Covell 1927a; Rao 1984), though the Lakshadweep archipelago has recently reported breeding of An. stephensi (Sharma and Hamzakoya 2001). Within the boundaries of the mainland of India, An. stephensi has first invaded the nonmalarious Kerala State through its northern most district, Kasaragod, and introduced malaria in the virgin ‘God’s own lands’, a sobriquet for Kerala, in 1969 onwards (Devi and Dass 1999). A similar scenario occurred in a rather more serious manner when An. stephensi was for the first time observed in the Rameswaram island in 2002 (Tyagi pers. comm.). Anopheles stephensi is a mysterious mosquito due to the following unfamiliar characteristics: (1) its genomic traits are widely differentiated from other closely allied taxa including An. arabiensis, (2) it is the only Anopheles vector which can overwinter both in larval and adult stages and (3) it is the only major vector of malaria Anopheles stephensi which manifests the phenomenon of ‘reflex immobilization’ or thanatosis (death-feigning) as a tool of selfdefence. In recent past, An. stephensi has caused several malaria outbreaks in Kerala State, India, where such epidemics were not reported until 1996, and it is now even reported breeding in water storage tanks in Lakshadweep islands almost a thousand kilometres off the coast of Kerala, indicating possibilities of invasion of other nearby islands (Sharma and Hamzakoya 2001). Establishment of this invasive species in the Rameswaram island in the vicinity of Sri Lanka is a continuous reminder of a tip of an iceberg of a major threat of resurgence of transmission of malaria in a recently declared ‘malaria-free’ nation (Dharmasiri et al. 2017). Sri Lanka’s malaria-free status is highly threatened by the ongoing socio-political turmoil in the country, and the following factors will only aggravate the situation of re-introduction of malaria into the country: hundreds of refugees ferrying out and in daily in Sri Lanka;

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Rameswaram island in India is a site of important pilgrimage and thousands of pilgrims gather there every day to visit the historic temples, and mixing of refugees with them is likely to escalate fresh malaria-parasite picking by the two major vectors, An. culicifacies and An. stephensi, and results in likely importation of malaria cases from an endemic country; and different trades by workforces through sea or air routes. The new entry of An. stephensi in the formerly already heavily malariated island nation has further rendered the Sri Lankan people more vulnerable and receptive to a possibility of re-introduction of malaria.

11.5

Invasion of Anopheles stephensi in Sri Lanka

The island nation of Sri Lanka situated in the Indian Ocean is situated only a few kilometres south of Rameswaram island (India) but has been struggling to cope up with a constantly dwindling economy due mostly to perennial malaria endemicity across 22 districts in its intermediate and dry zones (Konradsen et al. 2000). In Sri Lanka, An. culicifacies is the main vector of malaria, with support from An. subpictus, An. annularis and An. varuna as the secondary vectors (Amerasinghe et al. 1999). The World Health Organization certified Sri Lanka in November 2012 to harbour nil indigenous transmission of malaria and, in 2016, awarded it with the certification of elimination of malaria. Thus, Sri Lanka became the first nation in the Indian subcontinent who achieved this distinction of a malaria-free country. Surendran et al. (2019) postulated the progression of movement of An. stephensi, a major vector for malaria transmission in urban India (1970s, Goa; 1980s, Kanyakumari; and 2001, Lakshadweep islands in the Arabian sea) from north- to southwards into Sri Lanka in 2017 but also westwards into the Arabian Peninsula and the northeastern Africa between 2012 and 2019, from the Indian mainland, more or less in agreement to the brooding urbanization and associated water storage practices. These developments have threatened the northern islands of Maldives (90 km south of Lakshadweep), where water storage practices are identical, with an invasion by An. stephensi in the future. In Sri Lanka An. stephensi has been sampled both in larval and adult stages from multiple sites in Mannar and Jaffna, and a fear of further expansion of the vector looms large over the country (Surendran et al. 2019) (Fig. 11.3). Earlier Dharmasiri et al. (2017), who credited the discovery of An. stephensi in the island of Mannar, had made interesting observations on its breeding. Considering the fact that An. stephensi has a great penchant for colonizing urban environments and a strong affinity to P. falciparum and P. vivax in all of its resident countries, its recent discovery in the Mannar Island can certainly pose a serious warning to thwart the recurrence of malaria on the mainland in Sri Lanka, particularly when other highly potential vector species such as An. culicifacies, An. subpictus, An. annularis and An. varuna are already prevailing despite country-wide entomological surveillances and intensified vector control programmes. In the Mannar Island An. stephensi has been sampled breeding profusely in the wells. The occurrence of larvae of An. stephensi was mainly reported from the wells, while adults were

11.6

Invasion of An. stephensi in West Asia/Middle East

193

Fig. 11.3 (a) Sri Lankan map in the Indian Ocean, located south of India, and (b) collection sites of An. stephensi s.s. in Mannar and Jaffna (Source: Surendran et al. 2019)

sampled both from human dwellings and cattle-sheds. The presence of An. stephensi, in both larval and adult stages, was confirmed microscopically and molecularly, the latter by sequencing the barcode region of the cytochrome c oxidase I (COI) gene.

11.6

Invasion of An. stephensi in West Asia/Middle East

Mosquitos and the infections they carry are travelling along trade routes and settling in ever-expanding cities. Anopheles stephensi is a major vector in the Middle East, including areas of Iran, Afghanistan and Pakistan. Recently in eastern Iran, Chavshin et al. (2014) have characterized biological forms of An. stephensi and estimated its sporozoite rate in the transmission of malaria using molecular techniques. Abai et al. (2008) studied comparative performance of imagicides on An. stephensi in the southern Iran. On the other hand, Safi et al. (2017) put on record evidence of metabolic mechanisms playing a role in multiple insecticide resistance in Anopheles stephensi populations in Afghanistan. In Pakistan An. stephensi is a major vector of malaria in all urban settings. In summary in Iran and neighbouring West Asia countries An. stephensi, with its various subspecies/species, is a serious vector for decades.

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Invasion of An. stephensi in Arabian Peninsula

The Kingdom of Saudi Arabia (KSA) is the largest among all nations within the Arabian Peninsula. Malaria transmission in the Arabian Peninsula is largely factored by the dominant vector species and aridity with oases. At present malaria cases are reported only in Saudi Arabia and Yemen, with the latter contributing to over 98% of the clinical burden. The KSA is generally having a high quality of health machinery, and malaria is largely under control. Anopheles stephensi ‘type form’, the main malaria vector in the eastern region, is 1 of the 18 anopheline species found in the KSA (Mattingly and Knight 1956; Zahar 1985; Daggy 1959); the other ecotypes are not known to occur in the KSA. The Kingdom of Saudi Arabia is nearing elimination of malaria due to its practical approach in tackling the disease, especially imported cases.

11.8

Invasion of An. stephensi in Africa

The Asian vector An. stephensi was for the first time discovered by Djibouti in 2012 (soon followed by Ethiopia in Kebri Dehar, Somali Region, in 2017), and since then the event raised concerns about the impact of vector control campaigns in the country and the rest of the Horn of Africa. Developing effective malaria control strategies needs updated knowledge of biology, ecology and behaviour of the local mosquito vector species. With the uninvited addition of An. stephensi to local fauna, the sense of disease control through vector management has become very complicated and confusing since there is not much information yet mined on the intrusive species on either the genotypic or phenotypic characteristics. Continuous expansion of vectors into new areas has posed a serious threat to progress against malaria in Africa already pathetically represented (>90%) of the disease burden, mostly in the sub-Saharan Africa (SSA) region. Almost the entire malaria transmission in the sub-Saharan Africa is carried out by the deadly An. gambiae complex species. The capital port city in the Horn of Africa, Djibouti, is widely known as Pearl of the Gulf of Tadjoura due to its location in the Republic of Djibouti (23,200 km2)—a country strategically bordered in south by Somalia, in southwest by Ethiopia, in north by Eritrea and in the east by the Red Sea and the Gulf of Aden, where an unusual An. stephensi-driven urban outbreak of P. falciparum epidemic with 1228 cases struck in 2013 (February–May), soon followed by yet another severe epidemic the same year (November) and in 2014 (January–February). Since An. arabiensis is also present in Africa, a careful scrutiny of the identity of Anopheles stephensi, based on both the microscopic and molecular diagnoses (i.e. sequencing of the Barcode cytochrome c oxidase I (COI) gene and the rDNA second internal transcribed spacer (ITS2) gene). The indigenous nature of malaria infection was confirmed in March 2013 through positive tests for P. falciparum circumsporozoite antigen in two of six female An. stephensi sampled from the dwelling of malaria patients. This evidence of autochthonous urban malaria transmission by An. stephensi in Djibouti complimented by cognizance of the species’ genetical susceptibility to P. falciparum and tolerance to

11.8

Invasion of An. stephensi in Africa

195

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Fig. 11.4 Possible distances (in km) of An. stephensi covered/to be covered up to countries at risk from the first Africa-based discovery in Djibouti in 2012

urban environment led water pollution and adaptive potential to the new arid environments alarmed not only the African nations but also the World Health Organization (WHO 2019a; Mnzava et al. 2022). The WHO (2019a, b) has particularly urged all countries at risk to be vigilant and to improve and upscale their surveillance systems for the early detection and control of this invasive mosquito species. Next to the An. stephensi-mediated P. falciparum malaria in Djibouti in 2012, a similarly unusual but of higher-intensity P. falciparum-dominated malaria epidemic broke out in Ethiopian Somali region in the sub-Saharan Africa in 2016 and An. stephensi, of which a total of 2231 morphologically and molecularly identified samples were sampled, was incriminated there, too (Carter et al. 2018). Interestingly, additionally, Aedes aegypti were noticed coexisting in many of the An. stephensi larval habitats, an observation akin to that in the Thar Desert (Tyagi and Yadav 1996a–c; Tyagi and Hiriyan 2004). After Djibouti and Ethiopia, the presence of the invasive emergence of Anopheles stephensi was first documented from the coastal and sub-coastal regions of the Red Sea in Sudan (WHO 2019a), and subsequently its geographical expansion was confirmed up to the capital city Khartoum, in Sudan (Ahmed et al. 2021). Anopheles stephensi captured in Ethiopia and Sudan was confirmed to be the same (Folmer et al. 1994; Kumar et al. 2007). The expansion of the invasive An. stephensi continued far and wide, and the next country intruded by the vector was Eritrea in the Horn of Africa, in addition to Chad, Egypt, Libya and Republic of Central Africa (Abubakr et al. 2022). Sinka et al. (2020) have developed, with the help of global data on zoogeography of Anopheles stephensi in Africa during past one decade, a model reflecting a possible future expansion of the invasive species in Africa: Kenya, Uganda, Tanzania, Rwanda, DRC Egypt, CAR and Malawi. Figure 11.4 presents possible distances to be (or already) covered in reaching new sites or countries. With more data to generate on the expansion of An. stephensi in the next couple of decades, it seems to make us grow au fait to presume with some degree of certitude

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about a more far and wide distribution in Africa, and who knows much beyond, into a new continent altogether, taking cues from the life of An. arabiensis.

Epidemiology of Desert Malaria

12.1

12

Introduction

Epidemiological patterns of malaria are influenced by different kinds of climate. Epidemiology of malaria may change from one region to another or even within a country from one specific population to another within the same region depending on their ecological, biological and social conditions. Since the world’s deserts are irreversibly impacted by the climate change, the epidemiology of malaria is also shifted remarkably. Knowledge of the changing epidemiological trends of desert malaria in the eliminating countries will ensure improved targeting of interventions to continue to shrink the malaria map. Epidemiologists have recently paid greater attention than in the past to the epidemiology of desert malaria owing to the fact that it may help spread infection to the neighbouring plain areas where elimination has been successfully carried out. This change of emphasis has been stimulated in part by the need for better epidemiological definitions of malaria in the evaluation of control measures such as insecticide-treated materials and malaria vaccines. Methods of determining mortality from malaria and of defining severe and uncomplicated malaria have been devised through extensive epidemiological investigations including clinical. For instance, the limited data available indicate that malariaattributable mortality and the incidence of severe malaria do not increase with an increase in the entomological inoculation rate above a threshold value, an observation that has important implications for the likely long-term effects of attempts to contain malaria through vector control in a typical desert ecosystem which is full of challenges in establishing surveillance. Epidemiologic studies and clinical description of severe Plasmodium vivax malaria in adults living in malaria-endemic areas are rare, and more attention is needed to understand the dynamics and its interaction with the immune system. Historically, the prevalence of malaria was significantly higher than today, even in temperate regions of Europe and North America, before large control measures were undertaken following World War II. Malaria elimination was achieved post 1970s for European countries and during the 1950s in the USA. Over the African # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_12

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and Asian continents, the situation started improving during the past two decades with increased financial support and malaria control efforts (insecticide spraying, distribution of long-lasting impregnated bed nets, development of rapid diagnostic tests, door-to-door availability of drugs and better infrastructure).

12.2

Ecological, Biological and Social Aspects of Malaria Disease in Major Deserts

Studies of epidemiology of severe malaria in the African Sahara and the Great Indian Thar deserts have shown different epidemiological patterns for the two most frequent forms of this condition: cerebral malaria and relapsing malaria (Tyagi 2002; Kochar et al. 2005, 2007). Severe malarial anaemia is seen most frequently in areas of very high malaria transmission and most frequently in young children. In contrast, cerebral malaria predominates in areas of moderate transmission, especially where this is seasonal, and it is seen most frequently in older children. The study of patients with uncomplicated malaria has established the relationship between fever and parasite density and has demonstrated ways of defining fever thresholds. Malaria-eliminating countries achieved remarkable success in reducing their malaria burdens between 2000 and 2010. As a result, the epidemiology of malaria in these settings has become more complex. Malaria is increasingly imported, caused by Plasmodium vivax in settings outside sub-Saharan Africa, and clustered in small geographical areas or clustered demographically into subpopulations, which are often predominantly adult men, with shared social, behavioural and geographical risk characteristics. The shift in the populations most at risk of malaria raises important questions for malaria-eliminating countries, since traditional control interventions are likely to be less effective. Approaches to elimination need to be aligned with these changes through the development and adoption of novel strategies and methods. Knowledge of the changing epidemiological trends of malaria in the eliminating countries will ensure improved targeting of interventions to continue to shrink the malaria map.

12.3

Dynamics of Malaria Prevalence in Major Deserts

Human malaria is a parasitic disease caused by five species of Plasmodium and is transmitted by the bite of an infected Anopheles female mosquito to a human host. The tropical form of the parasite, Plasmodium falciparum, causes the most severe clinical form of malaria and is widespread in African Sahara Desert (Chemison et al. 2021). Malaria is responsible for many deaths worldwide: 405,000 reported in 2018 of which 67% occurred among children between 0 and 5 years of age (Griffin et al. 2014). Ninety-three percent of total cases and 94% of global deaths occurred in Africa, mostly south of Sahara Desert, in 2018 (WHO 2019a). Hence desert malaria has serious socio-economic impacts and can hamper development of overall malaria elimination campaign in the world.

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Dynamics of Malaria Prevalence in Major Deserts

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Malaria is a climate-sensitive disease, with transmission often seasonal, as specific temperature and rainfall conditions are necessary for the development of Anopheles mosquitoes and Plasmodium parasites. Various different deserts in the world have their own specific vectors of malaria; for example, in Africa these include An. gambiae, An. arabiensis and An. funestus are the primary malaria vectors in the worst-affected desert and semiarid regions of Africa, while in the Thar Desert, An. stephensi and An. culicifacies are the main transmitters (Tyagi 2002). They are present when humidity exceeds at least 40%, but adult mosquitoes die rapidly above 38 °C; the only exception is being An. stephensi in the Thar Desert which evidently has developed a mechanism to tide over extremities on both sides of temperature, i.e. 40 °C in summer and 4 °C during winter. Their presence is strongly regulated by the (rare seasonal) rains, which provide breeding sites after long gaps. After the sporogonic cycle, which is the incubation period for the mosquito to become infectious, the mosquito can infect additional humans. This incubation period shortens when temperature increases. A minimum temperature for sporogonic development was observed at 17 °C for An. gambiae and P. falciparum (Waite et al. 2019). Therefore, temperatures must be high enough for the parasite to complete its sporogonic cycle, but if the temperature is too high, then the mortality of the vector increases, leading to a decrease in malaria transmission risk.

12.3.1 The Sahara Desert Malaria in Africa is phenomenally rampant in the region south of Sahara where species of Anopheles gambiae Complex, viz., Anopheles arabiensis, An. bwambae, An. melas, An. merus, An. quadriannulatus, An. gambiae sensu stricto (s.s.), An. coluzzii and An. amharicus, especially An. gambiae and An. arabiensis, threateningly transmit P. falciparum parasite. The Sahara Desert stretches from the Red Sea in the West and the Mediterranean in the North to the Atlantic Ocean in the West, including ten countries: Algeria, Chad, Egypt, Libya, Mali, Mauritania, Morocco, Niger, Sudan and Tunisia. All these countries have been reporting malaria with varying degree of prevalence. Smith et al. (2005) have worked on entomological inoculation rate in malaria vectors and estimated Plasmodium falciparum infection in African children. 1. Algeria Malaria in Algeria was first identified in 1880, and by the 1960s around 80,000 cases a year were reported. Through an integrated approach including free provision of diagnosis and treatment, as well as indoor residual spraying and bed net use, this figure declined over the next 40 years to just 28,000 cases/year. Thanks to the malaria eradication campaign launched in Algeria in 1968, the number of malaria cases fell down significantly from 95,424 cases in 1960 to 30 cases in 1978. At that time the northern part of the country was declared free of Plasmodium falciparum. Only few cases belonging to P. vivax persisted in residual foci in the middle part of the country. In the beginning of the 1980s, the south of the country was marked by

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an increase of imported malaria cases. The resurgence of the disease, and introduction of the exotic vectors, in the oases coincided with the opening of the TransSaharan road and the booming trade with the neighbouring southern countries. Now, the totality of malaria autochthonous cases in Algeria is located in the south of the country where 300 cases were declared during the period (1980–2007). The recent outbreak recorded in 2007 at the borders with Mali and the introduction of Anopheles gambiae, An. arabiensis and An. sergentii s.l. into the Algerian territory show the vulnerability of this area to malaria which is probably emphasized by the local environmental changes (Ramsdale and de Zulueta 1983; Hammadi et al. 2009). Despite Algeria’s turbulent history of civil wars, the country joins the malaria-free list as the third country from Africa, after Mauritius in 1973 and Morocco in 2010. The present WHO Director-General, Dr Tedros Adhanom Ghebreyesus, credits this success of Algeria to the unwavering commitment and perseverance of the people and leaders of the country. 2. Chad Some 80% of Chad’s population live in high malaria transmission areas, with 2.5 million cases and 8700 deaths reported in 2018. With high levels of malaria transmission during a short rainy season, central areas of Chad can benefit from implementation of seasonal malaria chemoprevention (SMC)—a particularly effective treatment for preventing malaria in children between 3 and 59 months during peak transmission periods. Malaria Consortium established an office in N’Djamena, the capital of Chad, in May 2016 as part of its ACCESS-SMC project through which it continues to work with government and partners to protect 900,000 children in 20 health districts from malaria and cascade knowledge of SMC delivery through training of health workers. 3. Egypt Like Algeria, Egypt, had eliminated malaria, and until now, the last locally transmitted case was in 1998. It was argued that the P. vivax malaria came from Sudanese migrants. However, with the recent invasion of the Asian malaria vector, An. stephensi, possibilities of recurrence of malaria in the Egyptian town has become stronger. 4. Libya Libya, too, is now free from local malaria transmission and has no indigenously reported cases of the malaria. The last local case was in 1973. 5. Mali Mali is a landlocked country with a mostly flat terrain and some rocky hills in the north. The Niger River crosses the southern part of the country and forms an interior

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Dynamics of Malaria Prevalence in Major Deserts

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delta. Mali also has a subtropical to arid climate. Those parts of the country which receive significant rainfall experience a rainy season for part of the year and extremely dry weather for the remainder of the year. During the rainy season, Mali often faces problems with flooding when the Niger River overflows. When combined with environmental problems of deforestation, soil erosion and desertification, this creates conditions ideal for the transmission of malaria. Malaria is one of the principal causes of mortality and morbidity in Mali (Koné et al. 2015). With a population of approximately 11 million, Mali has over 800,000 reported cases of malaria annually, according to the World Health Organization (WHO). Malaria accounts for 13% of all mortality in Mali for children under the age of 5. Malaria is endemic throughout the more populated southern half of the country, with over 90% of the total population at risk of endemic malaria, with young children and pregnant women being the most vulnerable. Anopheles gambiae and An. arabiensis are the most dangerous vectors of malaria in Mali. The following anophelines, including the two above, have been reported from Mali so far. An. coustani coustani Laveran, 1900 An. coustani tenebrosus Donitz, 1900 An. coustani ziemanni Grünberg, 1902 An. funestus Giles, 1902 An. gambiae Giles, 1902 An. hancocki Edwards, 1929 An. leesoni Evans, 1931 An. longipalpis Theobald, 1903 An. maculipalpis Giles, 1902 An. nili Theobald, 1904 An. obscurus Grunberg, 1905 An. paludis Theobald, 1900 An. pharoensis Theobald, 1901 An. pretoriensis Theobald, 1903 An. rhodesiensis Theobald, 1901 An. rivulorum Leeson, 1935 An. rufipes Gough, 1910 An. squamosus Theobald, 1901 An. wellcomei Theobald, 1904 An. ziemanni Grunberg, 1902 Mali’s economy has been struggling. Therefore, keeping this fact in mind, a low-cost control technology is a priority. Thus, public-private partnership (PPP) funded by international health organizations and philanthropy and distribution of long-lasting insecticide-treated nets (LLIN) brought a radical change malaria prevalence.

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6. Mauritania The Islamic Republic of Mauritania (population 3,378,250) is situated in northwest Africa between 15 and 27° N latitude and 5 and 17° W longitude. It is spread over 1,030,700 sq. km. Population pyramid shows that nearly 43.7% are under 15 years old. Sedentarization and rural exodus, partly related to the periods of drought in the 1970s and 1980s, are the most significant demographic phenomena that have occurred in Mauritania since the country’s independence in 1960. Whereas the proportion of urban population was 9% in 1965, it increased to 22.7%, 46.7% and 60% in 1977, 2005 and 2010, respectively. Divided into three ecological zones, two-thirds of the surface area of Mauritania is covered by the Sahara Desert, and one-third is sub-Saharan semi-desert. It has a low annual rainfall that increases from north to south, one rainy season from June/July to September/October, depending on the year and/or region, and a dry season (‘cold dry season’ from November to March and ‘hot dry season’ from March to June). Malaria epidemiology in Mauritania has been characterized on the basis of epidemiological strata, defined by climatic and geographic features, which divide the country into three zones: (1) the Sahelian zone, (2) the Sahelo-Saharan transition zone and (3) the Saharan zone. In a study of malaria incidence in Nouakchott, Mauritania Lekweiry et al. (2009) had observed that malaria prevalence rate was 25.7% (61/237), the majority of positive blood slides as well as nested-PCR products were due to P. vivax 70.5% (43/61) and P. ovale 24.6% (15/61). Two malaria patients, both with P. vivax, have never travelled out of Nouakchott and seem likely to have been autochthonous (3.3%). Of the 237 individuals included in the survey, 231 (97.5%) were clinically diagnosed and treated as malaria cases. 26.4% of clinically diagnosed cases were positive for Plasmodium using microscopic examination and PCR. Thus, false-positive cases constituted 73.6% (170/231) of the clinically diagnosed malaria cases. The search for mosquito vectors in Dar Naïm district allowed morphological and molecular identification of An. arabiensis and An. pharoensis. In another study Moukah et al. (2016) had found that out of 3445 children examined, 143 (4.15%) were infected with malaria parasites including P. falciparum (n = 71, 2.06%), P. vivax (57, 1.65%), P. falciparum-P. vivax (2, 0.06%), P. ovale (12, 0.35%) and P. malariae (1, 0.03%). A large majority of P. falciparum infections were observed in the Sahelo-Saharan zone. Malaria prevalence (P < 0.01) and parasite density (P < 0.001) were higher during the rainy season (2013), compared to cool dry season (2011). Plasmodium vivax was mainly observed in the Saharan region [43 of 59 (73%) P. vivax infections], mostly in Nouakchott districts, with no significant seasonal variation. Of 3577 mosquitoes captured, 1014 (28.3%) belonged to genus Anopheles. The vector Anopheles gambiae was the predominant species in all three epidemiological strata during the ‘cool’ dry season in 2011 but was absent in all study sites, except for Teyarett district in Nouakchott, during the ‘hot’ dry season in 2012. During the rainy season in 2013, An. gambiae, An. arabiensis, An. pharoensis and An. rufipes were abundant in different zones.

12.3

Dynamics of Malaria Prevalence in Major Deserts

203

Fig. 12.1 The number of reported malaria cases from 1990 to 2012 in Mauritania (Source: Lekweiry et al. 2015)

Malaria has become a major public health problem in Mauritania since the 1990s, with an average of 181,000 cases per year and 2,233,066 persons at risk during 1995–2012 (Lekweiry et al. 2015) (Fig. 12.1). Totally the following 12 Anopheles species and subspecies occur in Mauritania: An. funestus, An. gambiae s.l., An. pharoensis, An. rufipes, An. melas, An. dhtali, An. rhodesiensis, An. coustani, An. ziemmani, An. pretoriensis, An. squamosus and An. demilloni. Among these anopheline species, only An. gambiae, An. arabiensis and An. funestus are known to be major malaria vectors in Africa. In Mauritania, An. gambiae s.l. appears to be the dominant malaria vector (Sautet et al. 1948; Dia et al. 2009). Anopheles arabiensis collected in Mauritania has been incriminated with P. falciparum and P. vivax sporozoites in the salivary glands (Dia et al. 2009; Lekweiry et al. 2011, 2015). Lemrabott et al. (2020) have brought on record the first time occurrence of An. (Cellia) multicolor in Mauritania. Mauritania faces several challenges in the management of malaria, including limited financial resources, crisis in human resources, shortage of health workers and health structures with reliable diagnostic facilities, insufficient epidemiological data on parasite distribution and malaria vectors, and regular epidemics. 7. Morocco Morocco is currently free from malaria. Malaria resurgence risk in Morocco depends, among other factors, on environmental changes as well as the introduction of parasite carriers since the local principal malaria vector, An. labranchiae, has low infectivity for Afrotropical P. falciparum strains. It is noteworthy here that An. stephensi has already made its entry in many African countries.

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Epidemiology of Desert Malaria

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Fig. 12.2 Malaria admissions and deaths (Source: Free Wikipedia)

8. Niger Malaria is endemic throughout Niger and is the primary cause of illness (Anon. 2020). It accounts for 28% of all illness in the country and 50% of all recorded deaths. However, the estimated number of cases decreased by 7.9%, between 2015 and 2019 (from 370 per 1000 population to 343 per 1000 of the population at risk), and the number of deaths decreased by 25.9% in the same period (from 0.919 per 1000 population to 0.730 per 1000 of the population at risk) (WHO 2020) (Fig. 12.2). According to the National Malaria Strategic Plan (NMSP), between 2014 and 2015, children under 5 years of age accounted for about three-fifths of the burden of disease (62%) and about three-quarters of malaria-related mortality in the country (74%) (Anon. 2020). 9. Sudan Sudan is one of the most dangerously malaria-affected countries in the Sahara Desert region. In 2019 malaria breached the epidemic threshold in Sudan so far. Over 1.8 million cases of malaria were reported from across Sudan so far in 2019. Several states in Darfur region, White Nile, Khartoum, and several other states are affected most. In November alone, about 250,000 cases of malaria were reported from Darfur. The rise in malaria cases is closely related to the floods in Sudan this year. The widespread presence of stagnant floodwaters offers breeding grounds for mosquitoes—which transmit the malaria parasite. The main vector of malaria in Sudan is An. arabiensis, a member of An. gambiae complex.

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Dynamics of Malaria Prevalence in Major Deserts

205

10. Tunisia Tunisia has eradicated malaria in 1979. However, the threat of malaria continues to hover in the country due to the persistence of mosquitoes and coexistence with a potential parasite reservoir in the form of imported cases.

12.3.2 The Arabian Peninsula The Arabian Peninsula’s constituent countries, all of which are mostly desert, are Kuwait, Bahrain, Qatar, the United Arab Emirates, Oman, Yemen and Saudi Arabia. While malaria has been eliminated from Kuwait, Bahrain, Qatar, the United Arab Emirates and Oman, the last two countries in the Arabian Peninsula remaining to achieve elimination yet are Saudi Arabia and Yemen (Snow et al. 2013). 1. Saudi Arabia The Kingdom of Saudi Arabia covers the greater part of the Peninsula. The majority of the population of the Peninsula lives in Saudi Arabia and Yemen. In distant past the peninsular countries suffered from malaria episodes perennially. Malaria control in Saudi Arabia was initiated in 1948 by the Arabian American Oil Company (ARAMCO) in the Eastern province, primarily to protect employees living around the oases, but soon, in 1954, the Saudi Arabian government adopted the template of this programme for a national malaria programme. The country faced a series of outbreaks in course, and the worst was in 1998. A rapid scaling up of vector control measures, adoption of artesunate plus sulfadoxine-pyrimethamine as first-line treatment, and the establishment of a regional partnership for a malaria-free Arabian Peninsula (the latter two occurred in 2007) have resulted in the number of autochthonous/indigenous (locally transmitted) malaria cases in Saudi Arabia decreased dramatically between 2000 and 2014, from 511 in 2000 to just 30 in 2014, and the country has been included in the E-2020 WHO initiative, which is focused on achieving a target of zero autochthonous cases by 2020 (Daggy 1959; Coleman et al. 2014). Today Saudi Arabia is almost there to eliminate malaria, and malaria persists in the provinces of Aseer and Jazan, both bordering the Republic of Yemen (Memish et al. 2014). Major vectors for malaria transmission in Saudi Arabia are An. arabiensis and An. sergenti. Oases malaria is common in Saudi Arabia. 2. Yemen Malaria remains a major public health problem causing heavy mortality and morbidity in Yemen with great variations in different ecosystems; deserts are considered free of malaria, whereas other areas are plagued with the disease (Anon. 2002a, 2006), with an annual incidence of about 900,000 cases and approximately 60% of the total population considered to be at risk of the disease (WHO 2009). Malaria parasites

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Plasmodium falciparum, P. vivax and P. malariae exist in Yemen. In a cross-sectional study, P. falciparum was detected with the predominance (83.33%) (Abdulsalam et al. 2010). Three vector mosquitoes are of concern in different ecosystems: Anopheles arabiensis is the predominant, An. culicifacies plays an important role in malarial transmission in the coastal areas of Yemen, and another known vector species, An. sergenti, has been reported in the mountainous hinterland and highland areas of the country (Alkadi et al. 2006; Bin Mohanna et al. 2007).

12.3.3 Middle East/West Asia/Central Asia Deserts Approximately all the countries in the MENA region are at risk of malaria, except for Egypt, the UAE and Jordan. The disease often affiliates travellers to most of the countries of the Middle East. Malaria has been known to be endemic in the lowlands of Saudi Arabia, and three species of Anopheles mosquitoes have been identified in this region. However, the risk of malaria is very low in parts of North Africa and the Middle East that are most visited by tourists. Malaria occurs in several endemic regions of Iran, including provinces of Kerman, Hormozgan and Sistan and Baluchestan (Ghasemian et al. 2016; Naddaf et al. 2003; Hanafi-Bojd et al. 2010; Vatandoost et al. 2006). In south of Iran, Anopheles culicifacies was the most frequent vector of malaria with a frequency of 37.5%, followed by An. d’thali (18.3%). There have been no reports of malaria in Iraq since 2009. There has been continued presence of imported malaria in Jordan, mainly from East Africa (Sudan and Eritrea) and Southeast Asia.

12.3.4 The Thar Desert The World Health Organization (WHO) estimated that between 2000 and 2010, global malaria incidence decreased by 17% and malaria-specific mortality rates by 26% (WHO 2011). Subsequently, a greater degree of progress was brought on record by many malaria-endemic countries such as India which, within the WHO Southeast Asia Region, has recorded a continuous decrease in malaria—the largest absolute reductions in the region—from about 20 million cases in 2000 to about 5.6 million in 2019 (Ranjha and Sharma 2021). An analytical understanding of the epidemiological scenario of malaria in the desert environment will help control the disease before it conflagrates to impact even in the hyperendemic neighbouring areas where disease elimination campaigns would be underway (Tyagi et al. 2001a, b). In India, after the northeastern states, the Thar Desert seems to be the most vulnerable area to the new dimensions of malaria disease at present. The correlation of environmental changes brought about in the Thar Desert by extensive canalization and irrigational activities with malaria prevalence of varying intensities in different physiographic situations is so clearly discernible and demonstrable that the Thar Desert practically offers an infallible model to understand the causes underlying resurgence of malaria in a desert ecosystem and control of vector mosquitoes with

12.3

Dynamics of Malaria Prevalence in Major Deserts

207

12 10

A

8

P

6

I

4 2 0 1979 1980 1981 1982 1983 1984 1985 1986 1987 1988 1989 1990 1991 1992 1993 1994 Desert districts

Non-desert districts

YEAR Fig. 12.3 Comparison of annual parasite incidence (API) in the desert (the Thar) and non-desert districts of Rajasthan between 1979 and 1994. Note the appreciable rise in API in desert districts from the mid-1980s onwards

proper water management. Since the Thar Desert has vigorously undergone a drastic change in its ecology during the last few years, in particular, it is worthwhile to review the malaria situation in the following two time periods: 1. Pre-1994 Period: Malaria in Exacerbation Before malaria epidemics began to appear regularly in the desert region from the mid-1980s onwards, most of the positive cases were reported from the hilly and forested terrain of Udaipur in the southern part of Rajasthan (Sharma 1986a, b). Thus, while in 1986 the Udaipur zone had contributed 44.1% positive cases and 67.7% P. falciparum cases as against 24.4% positives and 11.6% P. falciparum cases in the desert region (Anon. 1987a, b), in 1994 only 14.1% positives (P. falciparum 26.6%) hailed from Udaipur zone compared to 53.3% positives from the desert districts with a whopping 62.5% P. falciparum cases (Sharma et al. 1995). Among the then 11 desert districts, Barmer was the most malarious in 1994 contributing 31.3% positive cases and 35.8% P. falciparum cases (Tyagi et al. 1995). In Fig. 12.3 a comparison of annual parasite incidence in desert and non-desert districts in the state is presented for period 1979–1994 which indicates a definite increase in the desert districts. For the application of malaria control, all the districts in the Thar Desert have been organized in three zones: Jodhpur zone (Jodhpur, Pali, Jaisalmer, Barmer and Jalore districts), Bikaner zone (Sri Ganganagar, Hanumangarh, Bikaner, Churu and Nagor districts) and Jaipur zone (Sikar and Jhunjhunu districts). Mostly malaria epidemics affected Jodhpur and Bikaner zonal districts, particularly the former. In

208

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Epidemiology of Desert Malaria

this zone % P. falciparum showed a marked escalation in at least three of the five districts during 1981, 1986 and 1991 (Table 12.1). When the data of Jodhpur zonal districts at these three points of time are pooled and compared with those of Sri Ganganagar district and the state, it became clear that the SPR had steadily increased in the Jodhpur zonal districts, while in Sri Ganganagar and Rajasthan, it was down or unchanged in 1991 against the base year 1981. On the other hand, the % P. falciparum in the Jodhpur zonal districts, after being slightly down in 1986, showed a significant rise in 1991, but in both Sri Ganganagar and Rajasthan, it was down in 1991 after significantly increasing in 1986 against that in 1981 (Table 12.2). However, in all the three categories, the % P. falciparum was much higher in 1991 than in 1981. It was suggested that changes in % P. falciparum over the years had come about regardless of SPR. Therefore, in a region such as the Thar Desert, % P. falciparum is a rather significant factor in determining the severity of the magnitude of fatal infection or even future epidemics. 2. 1994–2000 Period: New Challenges This period had posed several challenges to both disease controllers and management implementers as well as the academicians and theoreticians. The slide positivity rates (SPR) and annual parasite incidence (API), along with the P. falciparum proportion, had been alarmingly high in some of the districts in the Thar Desert. After malaria-related deaths having been reported in 1994 and 1996, once again deaths due to malaria were reported in 2000, which is only indicative of the grim malaria situation in the Thar. Most of these alarmingly malariated districts are covered under the Indira Gandhi Nahar Pariyojana (IGNP), and a possible correlation between water management in the irrigated areas and the malaria resurgence has been established (Tyagi and Chaudhary 1997). One of the most significant features that has attracted attention in recent years is the recognition of Jaisalmer as the most malarious district, followed by Barmer and Jodhpur districts. However, as far as the prevalence of P. falciparum cases is concerned, the Jaisalmer district is unparalleled. The district also boasts of the maximum focal outbreaks of malaria in recent years. While during 1994 and 1995, Jaisalmer manifested P. falciparum proportion of 68.66% and 31.32%, respectively, after nearly 5 years of rigorous control measures, it still exhibited relatively high (17.48%) % P. falciparum in 2000. Most parts of Jaisalmer and Jodhpur districts, which have only recently been brought under the IGNP, harbour A. culicifacies in addition to An. stephensi which together transmit malaria in the area (Tyagi and Yadav 2001a; Tyagi et al. 1994). The physiography of this part of the Thar Desert is currently under transformation, and the population living there is largely non-immune to malaria infection. Under such circumstances, and with P. falciparum having already ushered into interior Thar Desert, the area is seemingly highly vulnerable to recurrent focal malaria epidemics (Tyagi et al. 2001a, b). It is noteworthy that the 1999 epidemic had engulfed only those villages which were in close vicinity (2–5 km) to the main Indira Gandhi Canal. It is likely, rather sure, that more malaria outbreaks will strike this area, with or without any rainfall. In addition to this, the urban malaria

District Jodhpur Barmer Jaisalmer Pali Jalore

1981 Census (×1000) 1655 909 167 1346 851

ABER 9.6 12.4 11.1 13.4 9.3

SPR 0.6 0.3 0.5 1.3 0.3

API 0.5 0.4 0.6 1.7 0.3

Pf (%) 9.7 9.9 16.3 7.2 5.0

1986 Census (×1000) 1965 1118 231 1390 9.05 ABER 6.0 6.9 6.1 8.8 4.2

SPR 1.7 0.7 1.0 1.6 0.8

API 1.0 0.5 0.6 1.4 0.3

Pf (%) 6.3 10.0 1.9 13.4 11.5

1991 Census (×1000) 2127 1433 343 1484 1141

Table 12.1 Malariometric data at 5-yearly intervals in the desert districts of the Jodhpur zone (Source: Tyagi 2002)

ABER 5.1 7.1 6.2 9.0 6.5

SPR 5.7 10.7 1.3 7.2 2.2

API 3.0 7.7 0.8 6.5 2.1

Pf (%) 16.1 11.0 29.5 12.5 13.1

12.3 Dynamics of Malaria Prevalence in Major Deserts 209

District Jodhpur zone districts Sri Ganganagar Rajasthan

ABER 11.1

13.5

11.0

1981 Census (×1000) 985.6

1828

32,491

2.5

0.8

SPR 0.6

3.1

1.1

API 0.7

14.6

2.6

Pf (%) 9.2

34,670

1984

1986 Census (×1000) 1067.8

8.5

9.6

ABER 6.4

1.8

2.2

SPR 1.1

1.5

2.1

API 0.7

25.6

6.8

Pf (%) 8.6

45,880

26.18

1991 Census (×1000) 1305.6

7.0

6.0

ABER 6.7

2.5

0.1

SPR 5.6

0.2

0.1

API 4.0

21.2

5.5

Pf (%) 16.4

Table 12.2 Comparison of averaged malariometric data of Jodhpur zonal desert districts with those of the most irrigated Sri Ganganagar district and Rajasthan State (Source: Tyagi 2002)

210 12 Epidemiology of Desert Malaria

12.3

Dynamics of Malaria Prevalence in Major Deserts

211

particularly in Jodhpur township may pose serious challenges in the near future, due mostly to the influx of malaria cases from the nearby quarry mines. The Soorsagar area which abounds with quarry mines, on the one hand, and braces the northwestern flank of the city, on the other, is the major focus of P. falciparum cases. 3. Post-2000 Period Although malaria incidence in the Thar Desert region is on the consistent decline, now and then cases escalate with outbreaks in major desert districts like Jodhpur which has been a pivotal point of various investigations. District Jodhpur (22,850 sq. km.; 26°0′–27°37′ N Latitude and 72°55′–73°52′ E Longitude) has a population of 6.86 Crores as per year 2011 census. The health setup in district comprises nine block primary health centres (BPHCs). The temperature varies from 49 °C in summer to 1 °C in winter. The district enjoys an average annual rainfall of 302 mm. Although here is no perennial river in the district, two major seasonal rivers, namely, Luni and Jojari, flow through it; the former enters Jodhpur district near Bilara and flows for a distance of over 75 km within the district. Tyagi et al. (2000) have emphasized on the breeding prowess of An. stephensi in Jodhpur, in construction sites’ open-ground as well as underground tanks and the multi-storey buildings’ overhead tanks. Batra et al. (1999) reported the problem of malaria in district Jodhpur where they recorded slide positivity rate and slide falciparum rates as 67.54% and 7.10%, respectively. Tyagi et al. (2001a, b) investigated a differential potential of malaria transmission in vectors in both desert and non-desert irrigated villages in the vicinity of Indira Gandhi Nahar Pariyojana (IGNP). Anand (2009) conducted a primary health centre-based prospective case control study wherein he recruited 42 cases of malaria along with 84 age- and gender-matched controls. Information on selected exposures was collected on pretested questionnaire by trained field staff after getting informed and written consent of participant. Matched odds ratio and multivariable analysis were performed in Epi Info software to estimate the independent association of exposures with malaria without confounding effects of other variables. Malaria cases occurred from the month of May till October, but only 2 months, i.e. August and September being the months of rainy season, entirely yielded 27 cases from Fidusar PHC, whereas Banar and Bisalpur PHCs recorded only 5 and 10 sets, respectively. No cases could be found in Keru, Narwa and Salwakala PHCs. Maximum cases occurred in the 15–44-year age group. Occupation-wise 50% of the cases were manual labourers. Anand et al. (2011) analytically summarized the secondary data obtained for the Jodhpur district, city and the nine CHCs (Table 12.3). He plotted a secular trend of malaria incidence, transmission dynamics, mapping of disease burden areas and surveillance of malaria and deduced that the range of annual parasite incidence (API) was from 0.52 to 2.85 in district Jodhpur, with API 3 mg/dl) Hyperpyrexia Psychosis Multiple factors

No. of cases (%) 137 (25.75) 31 (5.83) 11 (2.07) 16 (3.00) 11 (2.07) 28 (5.26) 51 (9.58) 13 (2.44)

No. of deaths (%) 46 (33.57) 22 (70.97) 5 (45.45) 13(81.25) 3 (27.27) 13(46.43) 4 (7.84) 1 (7.69)

42 (7.89) 34 (6.39) 68 (12.78) 61 (11.47) 132 (24.81) 11 (2.07) 51 (9.59)

4 (9.52) 1 (2.94) 2 (2.94) 22 (36.06) 20 (15.15) 2 (18.18) 42 (82.35)

The overall mortality recorded due to complications was 11.09% (# 59) which was quite high because of infection in the non-immune population in the Thar Desert (Sharma 1995). Mortality was reported more (82.35%) in those patients who presented with more than three syndromes together. It is interesting to note that, in variation to general belief, though the largest group of cases admitted was of cerebral malaria, deaths caused due to cerebral malaria stood only next to those having pulmonary oedema (81.25%), severe anaemia (70.97%), algid malaria (46.43%), renal failure (45.45%) and jaundice (36.06%). Most pregnant women with malaria were found to be more prone to develop severe anaemia, hypoglycaemia, cerebral malaria and pulmonary oedema compared to non-pregnant women, and these factors obviously contributed to high mortality and morbidity. The aetiology of foetal distress had been traced to the preferential parasite sequestration and development in the placenta, wherein it interferes with the transplacental delivery of nutrients to the foetus. Acute placental insufficiency is the net result, and, in areas like the Thar Desert with unstable malaria transmission where symptomatic disease in the mother is not uncommon, foetal distress is generally undiagnosed, resulting in high mortality. Of the 30 pregnant malaria patients, of which 10 (33%) had died, only 11 (37%) succeeded to continue with pregnancy, while 5 (17%) had aborted and 4 (13%) delivered still birth. Mortality reported in females was more than double (16.06%) than in males (7.64%) because of specific neglect in getting rapid treatment for them and the deleterious effect of pregnancy. Clinical pattern arisen due to complicated malaria in the Thar Desert population was stressed by some workers (Gupta et al. 1987). In an important investigation,

230

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Epidemiology of Desert Malaria

Kochar (2001) studied 441 adult patients suffering with cerebral malaria from Bikaner. Apart from fever and unconsciousness in all patients, other complications included convulsions (12.13%), neck rigidity (19%), psychosis (5.21%), conjugate deviation of eyes (2.26), extrapyramidal rigidity (2.25%), trismus (1.13%), decorticate rigidity (1.13%) and de-cerebral rigidity (0.90%). A total of 145 (32.87%) patients expired, and mortality was highest in pregnant ladies (39.28%). The most important neurological sequelae in survivors were psychosis (5.06%), cerebellar ataxia (4.72%), hemiplegia (1.68%), peripheral neuropathy (1.01%) and isolated sixth nerve palsy (0.33%). All the survivors, treated with quinine orally, recovered but continued to manifest certain complications in the follow-up examinations. The associated illness included microscopic haemoglobinuria (12.92%), ARF (9.07%), jaundice (6.8%), anaemia (6.8%), bleeding (6.8%), pulmonary oedema (4.53%) and hypoglycaemia (4.08%). Multiple organ dysfunction syndrome (MODS) was observed in 14.51% patients. In a pilot study to assess the impact of malaria epidemic on the health of affected population in some villages of Jaisalmer in 1999, the following most common illnesses were found to inflict the population (Tyagi et al. 2001a, b). Clinically fever (47.9%) was identified as the most common cause of illness, followed by headache (21.1%), abdominal pain (8.9%), body ache (6.5%), giddiness (5.6%), loss of appetite (3.2%), cough and expectoration (1.6%) and nausea/vomiting (1.6%). Most of the examined cases were febrile in all but one age group (0–11m), while most febriles were found in the 15+-year age group. No serious illness could be identified in the cases in 0.05 0.05

276 16 Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts

16.3

Health Impact of Malaria

277

Table 16.3 Indigenous preparations used for remedying different common health disorders in villages with Health Facilities (HF) and Without Health Facility (WHF) S. no. 1

2

3

4

Health problem Fracture

Measles

Pain in bone joints

Cough and cold

Type of villages HF

Respondents (%) >33% Traditional plaster (70.5)

WHF

Milk (47.3), common tallow Laurel (40.0)

Indigenous sugar (25.5)

HF

Millet (69.5), jaggery (72.1)

WHF

Millet floor (73.1), jaggery (72.1)

HF

–

Crocus (25.6), thyme-leaved gratiola (22.6), omum (21.3), black salt (21.3) Thyme-leaved gratiola (30.8), holy basil (30.8), omum (30.8), water (21.0) Ghee from cow’s milk (31.3), seed (23.3), aloe ((27.6)

WHF

–

Aloe (26.2), ghee (25.2), sheep’s milk (20.6)

HF

Dried ginger (41.1), black pepper (34.9), indigenous sugar candy (34.9), nutmeg (33.1)

Coriander (25.8)

WHF

Dried ginger (58.0), coriander (47.6), black pepper (37.1)

Indigenous sugar candy (20.9)

20–33% Ghee from cow’s milk (20.8)

10–20% Black soot (10.9), indigenous sugar (12.0), common tallow Laurel (14.8) Ghee from cow’s milk (18.2), wheat flour (18.2), black soot (11.8) Oriental cashew (15.9), singhmora (12.2), nutmeg (18.3)

Nutmeg (10.0)

Common tallow Laurel (14.1), traditional plaster (13.5), indigenous sugar (12.9), wheat flour (12.3), Commiphora mukul (12.3) Dactyloctenium grass (15.9), turmeric (13.1), fenugreek seed (12.1), mustard oil (11.2), wheat flour (10.2) Clove (15.3), common fig. (14.7), holy basil (13.4), cinnamon (12.2), date palm (10.4), millet flour (12.2) Hot milk (18.1), omum (18.1), date palm (17.1), holy (continued)

278

16 Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts

Table 16.3 (continued) S. no.

5

6

Health problem

Toothache

Bleeding due to injury

Type of villages

8

Constipation

Eye infection

9

10

Tobacco (43.3)

–

WHF

Tobacco (40.9)

HF

HF

Rifle/machine oil (57.6) Bristles of rachis from elephant grass (48.7) Cassia (42.9)

Yellow-berried night shade (23.6) Burnt cloth ash (24.3) Rifle oil (25.7)

WHF

–

HF

Alum (39.2)

WHF

Sweet basil leaves (50.0) Opium(55.1), curd (52.3)

–

WHF

Curd (75.0), spogel seeds (35.6), opium (31.7)

–

HF

–

WHF

–

Ghee from cow’s milk (24.7) Ghee from cow’s milk (28.9), soot from kitchen smoke (28.9), margosa (28.9)

11

HF WHF

Asafoetida (48.2)

HF

Single boil

Intestinal worms

20–33%

HF

WHF

7

Respondents (%) >33%

Chebulic myrobalan (29.5), Spogel seeds (30.0), Cassia (26.6), milk (20.2) –

–

Omum (20.5)

10–20% basil (16.1), nutmeg (14.2) Clove oil (19.1), alum (11.5), garlic (11.5), mustard oil (10.8), salt (10.8) Traditional healer (15.5), clove (13.6) Infant urine (11.8) Burnt cloth ash (15.0) Rock salt (22.3)

Castor seed oil (18.3), chebulic myrobalan (14.7), black salt (10.1) Ghee from cow’s milk (19.2), breast milk (13.3) Alum (16.0), pink colour (13.8) Turmeric (19.6), ghee from cow’s milk (12.1), millet (11.2), breast milk (10.3), Corchorus trilocularis (11.2) Ghee from cow’s milk (19.3), rice (18.3), turmeric (18.4), sago (10.6) Soot from kitchen smoke (19.1) Wheat flour (10.5), butter milk (10.5)

Black salt (16.9) Black salt (16.0) (continued)

16.3

Health Impact of Malaria

279

Table 16.3 (continued) S. no.

Health problem

Type of villages

12

Typhoid

HF

13

14

15

Multiple boils

Headache

Fever— Short duration

Respondents (%) >33% Omum (Trachyspermum ammi) (42.0), fenugreek seed (40.7), asafoetida (39.5) Indigofera (50.0)

WHF

Dried ginger (25.6), Indigofera (27.0)

HF

–

WHF

–

HF

–

WHF

Dried ginger (92.3), black pepper (87.1), coriander (79.4) Black pepper (94.4), dried ginger (68.5), coriander (62.9), indigenous sugar candy (55.5), nutmeg (38.8) Coriander (43.5), black pepper

HF

20–33%

10–20%

–

Gum arabic (18.9), indigenous sugar (19.0), indigenous sugar candy (19.0), nutmeg (13.9), black pepper (13.9), thymeleaved gratiola (13.9), Lippia (11.3), oriental cashew (11.3), coriander (11.3), black salt (10.1) Clove (17.56), holy basil (16.2), black pepper (16.2), omum (14.8), Indian long pepper (13.5), coriander (13.5), millet flour (10.8) Fagonia (17.8)

Margosa bark (28.8) Margosa leaves (68.8) Black pepper (25.0), coriander (23.6), dried ginger (22.2) –

–

–

Rohida tree bark (18.8) Desi misri (16.7), balm (12.5), inula (11.1)

Nutmeg (17.9), desi ghee (black salt 10.2), boiled water (10.2) Margosa leaves (14.8), millet (11.1), holy salt (11.1)

Calotropis (13.0) (continued)

280

16 Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts

Table 16.3 (continued) S. no.

16

Health problem

Fever— Long duration

Type of villages

HF

WHF

Respondents (%) >33%

20–33%

10–20%

(39.1), indigenous sugar candy (39.1), dried ginger (34.8) Latex from leaf nodes of Calotropis (38.4)

Sand (30.7), black pepper (23.0)

Coriander (15.3), dried ginger (15.3), millet (15.3), margosa leaves (15.3) Margosa leaves (15.3)

Black pepper (36.4), dried ginger (36.4)

Margosa leaves (27.3)

Table 16.4 List of health problems according to their frequency and type of treatment taken by respondents in the past 90 days

Health problem Cough and headache Fever with shivering Night blindness Asthma Abdominal pain Anaemia Pneumonia Premature ejaculation Bleeding from nose Piles Scorpion sting Jaundice Others Total

16.4

Type of treatment Ethnomedicine No. of cases 50 23 11 11 17 24 19 15 10 8 7 6 28 229

% 96.2 12.9 73.3 50.0 68.0 100.0 100.0 100.0 100.0 100.0 100.0 100.0 77.7 54.9

Allopathy No. of cases 2 155 4 11 8 0 0 0 0 0 0 0 8 188

% 3.8 87.1 26.7 50.0 32.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 22.3 45.1

Knowledge, Attitude and Practice of the Rural Population about Malaria in the Thar Desert

Tyagi and Yadav (1996b) and Yadav et al. (1999) conducted a study in four villages, two each from a recently canal-irrigated northern part of Jaisalmer district (Madasar and Awai villages) and the more desertic part of Jodhpur district (Kanasar and Khetusar villages), involving 345 persons (206 males and 139 females) with a history of malaria infection during the past 1 year, with a comparable control

16.4

Knowledge, Attitude and Practice of the Rural Population about Malaria. . .

281

120 100 80

% 60 40 20 0 1

2

3 WHF Villages

7

HF Villages

Days Fig. 16.2 Cumulative percentage of respondents seeking treatment of ethnomedicine by days

group without any history of malaria, following a malaria outbreak in the area during 1992–1993 (Fig. 16.3). These people represented different age groups and economic classes such as agriculturists (43.5%), agriculture labourers (10.4%) animal keepers (30.9%), daily wagers (5.5%) and miscellaneous including students, jobless and retired persons, etc. (9.7%). Females generally looked after household chores, besides children, animals and old family members, at times in addition to their full-time professional jobs. A majority of the respondents (88.0%) were married. Literacy rate was determined to be low among the respondents; those having acquired primary education were 11.4%, middle education 8%, high school 4.8% and higher education 3%. The remaining 18.8% respondents were literate but without any formal educational background. People were found to have very poor knowledge as to the real causation of the disease (97%), although the affected people knew better about the signs and symptoms of malaria. About 76% of malaria patients attributed fever with chill and sweating as the most important sign and symptoms of malaria. In contrast, 39% of healthy subjects associated malaria with fever, giddiness and rashes on the body as major signs and symptoms of malaria. More of the affected people acknowledged having used frequently prophylactic measures such as mosquito nets (98%), repellents like Odomos cream and different types of oils (29%) and fumigants (24%). The affected group (74%) showed better concern about management of malaria fever by primarily taking full course of chloroquine tablets during illness, although those who complained of some kind of uneasiness after consuming chloroquine were also not uncommon (67%). About 40% of affected women avoided the use of chloroquine during pregnancy (Fig. 16.4). According to Yadav and Tyagi (2000), in yet another study on women with malaria history in relation to family management and support, while 66.61% women

282

16 Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts

Fig. 16.3 Sketch showing sites for villages investigated in the highly irrigated Indira Gandhi Nahar Pariyojana command area (1 = Madassar village, 2 = Awai village), and in the truly desertic non-command area (3 = Kanasar village, 4 = Khetusar village) in Jaisalmer and Jodhpur districts, respectively, in the Thar Desert, north-western Rajasthan (India) (Source: Dr. B.K. Tyagi, personal archive)

resented the parturition-related management in villages, nearly 95% of the pregnant women had complained of not getting any major relief from the domestic works during malarial pyrexia. The impact of malaria on the health of rural people was clearly visible as 91% of the malaria patients reported their working capacity being reduced during indisposition. This led the rural-folk to following certain taboos since 49.6% of the respondents avoided fried foods but preferred ‘rabadi’ (local preparation made from millet flour and yogurt), ‘Khichchadi’ (a semi-liquid preparation from the mixture of rice and pulses) and ‘mateera’ (fruits of a cucurbitaceous plant akin to watermelon). The overall costs of malaria treatment were prohibitive to many of the affected people as 55% of malaria patients expressed their resentment for

16.4

Knowledge, Attitude and Practice of the Rural Population about Malaria. . .

283

Fig. 16.4 Awareness campaign in the Thar Desert village communities and schools (Source: Yadav and Tyagi 2000)

bearing a major part of the expenditure by themselves, though they were also appreciative of the anti-malaria campaigns by the government. Knowledge about vector mosquitoes was found to be better among the malaria patients (26%) as compared to the healthy subjects (14%). Nearly 28% of malaria patients knew about the feeding and resting habits of malaria mosquitoes. In the

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16 Agroeconomical and Eco-Bio-Social Aspects of Malaria in Deserts

same way, 29% of malaria patients also appeared to have better knowledge about their laying eggs and development of larvae. Since the ‘tanka’ was shown to be associated with the vector breeding, 23% of malaria patients acknowledged the fact that vector population could be reduced by properly covering the ‘tanka’.

Vector Identification and Malaria Diagnosis in Major Deserts

17.1

17

Introduction

Generally malaria is diagnosed in a community of arid environments on the basis of presence of parasite in the patient’s blood, clinical symptoms and vector incrimination with malaria parasite (Hay et al. 2010a, b). Of the three biological species in the epidemiological triad, anopheline vector mosquitoes and Plasmodium parasites are involved in the transmission of the disease to man. There are well over 400 Anopheles species throughout the world, but only less than 70 species participate in the mechanism of parasite transmission to humans. Likewise there are five Plasmodium species of human malaria, notwithstanding information on at least 11 Anopheles species capable to transmit human parasites. To manage control of malaria both in nature (i.e. mosquito control) and in infected human being, a proper, accurate and timely identification/diagnosis of the species of vectors and parasites is of paramount importance. Despite a large number of alternate technologies, insecticides continue to be the main pillar of control of vectors both in adult and aquatic stages, even though there are serious issues associated with human health and environment (Tyagi 2021). However, most vector species have developed resistance of some kind (mono-, multiple and cross-resistance) against the conventional insecticides rendering them ineffective (Nauen 2007). At the same time, Plasmodium parasites such as Plasmodium vivax have also widely developed resistance against the antimalarial drug of choice, chloroquine (Price et al. 2014).

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

India harbours 61 anopheline species of which six are primary vectors which are the Dominant Vector Species (DVS) in context with malaria in India and carry immense epidemiological importance. These are, namely, An. culicifacies, An. fluviatilis, An. stephensi, An. minimus, An. baimaii and An. sundaicus. Of these the most # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_17

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important vectors, viz. An. stephensi, An. culicifacies and An. fluviatilis, particularly the first two species, prevail in the Thar Desert. Besides, there are five secondary vector species which carry lesser epidemiological significance. These transmit malaria along with either one or two major vectors in different parts of the country. These are An. subpictus, An. annularis, An. nivipes, An. philippinensis and An. varuna. In addition to the magnum opus on Indian Anopheles by Christophers (1933), a large number of culicidologists have also offered annotated field guides for identification of anophelines, both larvae and adults, of the country (Puri 1960; Wattal 1963; Wattal and Kalra 1961; Das et al. 1990; Tyagi et al. 2012, 2014). However, there are no updated dichotomous keys available for the Thar Desert Anopheles species, and, therefore, it is considered most opportune to offer here detailed keys for their identification.

17.2.1 Fourth Instar Larvae of Malaria Vectors 1.

2 (1)

3 (2) 4 (3)

5 (2)

6 (5)

Bases of inner clypeal hairs much closer to one another than to outer clypeal hairs; antennal hair branched or simple (Fig. 17.1) Bases of inner clypeal hairs wide apart and closer to the bases of outer clypeal hairs; antennal hair simple (Fig. 17.2) Anterior tergal plates on abdominal segments III–VII very wide and enclosed the rounded median chitinous spot posteriorly (Fig. 17.3) Anterior tergal plates on abdominal segments III–VII not very wide and never enclosing the rounded median chitinous spot (Fig. 17.4) Inner and outer clypeal hairs simple (Fig. 17.5)

Subgenus Anopheles Subgenus Cellia (2) 3

Inner and outer clypeal hairs with short scattered branches (Fig. 17.5) A pair of minute hairs arising from the tergal plate on segments II–VIII (Fig. 17.6) The pair of minute hairs not arising from the tergal plate but lying external and a little posterior to the plate on each side (Fig. 17.7) Inner and outer clypeal hair simple or with short in inconspicuous lateral fraying Inner and outer clypeal hair with conspicuous lateral branches (Fig. 17.8) Mesothoracic pleural hairs all simple, with two long hairs (Fig. 17.9)

aconitus varuna

One of the long mesothoracic pleural hair pectinate others simple (Fig. 17.10) Meso- and metathoracic pleural hairs all simple (Fig. 17.11)

10

5 4

minimus and fluviatilis 6 12 7

11

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

287

Figs. 17.1–17.11 (1) Inner clypeal hairs, closure; (2) inner clypeal hairs, wider; (3) anterior tergal plates; (4) anterior tergal plates; (5) inner and outer clypeal hairs; (6) minute hairs in tergal plate; (7) minute hairs not in tergal plate; (8) inner and outer clypeal hairs with branches; (9) mesothoracic hairs simple; (10) mesothoracic hair with pectinate; (11) meso- and metathoracic hairs simple (Source: Tyagi 2020)

288

7 (6)

8 (7)

9 (7)

17

Vector Identification and Malaria Diagnosis in Major Deserts

Both the long metathoracic pleural hairs pectinate (Fig. 17.12); palmate hair on thorax not differentiated One of the long metathoracic pleural hair pectinate others simple (Fig. 17.13); palmate hair on thorax well differentiated Posterior clypeal hair short and placed very close to inner clypeal hair (Fig. 17.14) Posterior clypeal hair placed not very close to inner clypeal hair; mesothoracic hair four most often with three branches (2–4) from near the base (Fig. 17.15a, b) Posterior clypeal hair placed not very close to inner clypeal hair; mesothoracic hair four most often with two branches (1–3) from near the base (Figs. 17.15a and 17.16) Filaments of abdominal palmate hairs about half as long as the blades of leaflets; Seta 9-T with few branches, 10-T simple; only the end of outer submedio-dorsal caudal hairs curved to form hooks, the branches of inner hairs, fine and straight (Fig. 17.17a, b, c) Filaments of abdominal palmate hairs about half as long as the blades of leaflets; both the ends of inner and outer submedio- dorsal caudal hairs curved to form hooks, the branches of inner hairs stout (Figs. 17.17a and 17.18)

8 9 vagus sundaicus

subpictus

culicifacies

d’thali

Figs. 17.12–17.16 (12) Both the metathoracic hairs pectinate, (13) single metathoracic hair pectinate, (14) position of posterior clypeal hair, (15a) position of posterior clypeal hair, (15b) seta 4-M with three branches, (16) seta 4-M with two branches (Source: Tyagi 2020)

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

289

Figs. 17.17–17.18 (17a) Filaments of palmate hair, (17b) seta 9-T with few branches, (17c) outer submedio-dorsal caudal hairs. (18) Inner and outer submedio-dorsal caudal hairs (Source: Tyagi 2020)

10 (6)

11 (6)

12 (5)

Outer clypeal hairs always simple; abdominal seta 1-I with three to five branches; setae 9,10-T both branched (Fig. 17.19a) Inner and outer clypeal hairs finely frayed; filamentous of abdominal seta 1 with sharp point; seta 6-III with 20 or more branches (Fig. 17.20) Seta 1-P with two to five branches; abdominal seta 1-II with filamentous branches (Fig. 17.21a, b) Innermost submedian prothoracic hair (1-P) with more than four branches arising from a large root (Fig. 17.22) Outer clypeal hairs with a large no. of long branches forming a broomlike tuft; posterior clypeal hairs with two to five branches; filament of palmate hairs more than half or as long as blade of leaflet (Fig. 17.23a, b) Outer clypeal hairs with a large no. of long branches forming a broomlike tuft; posterior clypeal hairs with seven to ten branches; filament about ¼ length of leaflet (Fig. 17.24a)

stephensi maculatus tessellatus baimaii (=dirus D) pallidus

philippinensis

290

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Vector Identification and Malaria Diagnosis in Major Deserts

Figs. 17.19–17.24 (19a) Abdominal seta 1-I with three to five branches, (19b) setae 9,10-T both branched, (20) seta 6-III with 20 or more branches, (21a) seta 1-P with two to five branches, (21b) abdominal seta 1-II with many branches, (22) 1-P with more than four branches, (23a) posterior clypeal hairs with two to five branches, (23b) filaments of palmate hair, (24a) posterior clypeal hairs with seven to ten branches, (24b) filaments of palmate hair (Source: Tyagi 2020)

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

291

17.2.2 Adults of Vector Mosquitoes 1

Scutellum evenly rounded; palpus about equal to the length of proboscis (Fig. 17.25a, b); abdomen with sterna and usually terga largely or wholly devoid of scales

Fig. 17.25 Anopheles palpi and proboscis (a) and Anopheles scutellum (b) (Source: Tyagi 2020)

Anopheles

292

1 2(1) 3(2)

4 (3)

5 (3)

17

Vector Identification and Malaria Diagnosis in Major Deserts

Wings with four or more dark spots on costa (Fig. 17.26) Femur and tibia speckled (Fig. 17.27) Femur and tibia not speckled (Fig. 17.28) Hind tarsomere 5 not white (Fig. 17.28) Hind tarsomere 5 white (Fig. 17.29) Palpi with three pale bands (Fig. 17.30) Palpi with four pale bands (Fig. 17.31)

(Subgenus Cellia) 2 7 3 6 4 5

Apical and subapical pale bands of palpi equal; palpi speckled (Fig. 17.32)

stephensi

Apical and subapical pale bands of palpi unequal; palpi not speckled (Fig. 17.33) Hind leg with a broad white band at the tibio-tarsal joint; presector dark mark on vein 1 without any pale interruption; apical pale band on hind tibia with a longitudinal basal dark stripe on ventral aspect (Figs. 17.34 and 17.35)

sundaicus

Hind leg with a broad white band at the tibio-tarsal joint; presector dark mark on vein 1 with one or more pale interruption; apical pale band on hind tibia without a ventral dark stripe (Figs. 17.36 and 17.37)

6 (2) 7 (1)

8 (7) 9 (8)

baimaii

(=dirus D) elegans

Abdominal terga II–VIII shiny, with no pale scales (Fig. 17.38)

pseudowillmori

Abdominal terga IV–VIII with a few pale scales (Fig. 17.39) Hind tarsomere 5, 4 and 3 completely white; apex of hind tarsomere 1 usually with white band; wing vein 5 mainly white, no dark spot at the point of bifurcation (Fig. 17.40) Hind tarsomere not white; fore tarsi with narrow pale bands (Figs. 17.41 and 17.42)

maculatus philippinensis

8

Wing vein 3 mainly dark; inner quarter costa usually with pale interruption (Fig. 17.43) Wing vein 3 mainly white (Fig. 17.44) Female palpi with both apical and subapical pale bands as broad as or broader than subapical dark band; basal third of costa with white interruption; fore tarsomere 1–4 with very small dorso-apical pale patches (Fig. 17.45) Female palpi with subapical pale band, narrow and subapical dark band much broader; vein 6 with two dark spots, distal half mainly dark; hind tarsomeres uniformly dark (Fig. 17.46)

culicifacies 9 minimus

fluviatilis

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

293

Figs. 17.26–17.31 (26) wings with four or more dark spots on costa, (27) femur and tibia speckled, (28) femur and tibia not speckled, (29) Hind tarsomere 5 white, (30) palpi with three pale bands, (31) palpi with four pale bands (Source: Tyagi 2020)

294

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Figs. 17.32–17.37 (32) palpi with speckling, (33) palpi without speckling, (34) hindleg with broad white band at tibio-tarsal joint, (35) presector dark mark on vein 1 without pale interruption, (36) hind tibia without ventral dark stripe, (37) presector dark mark on vein 1 with pale interruption (Source: Tyagi 2020)

17.2

Dichotomous Keys for Identification of Vectors of Malaria in India

295

Figs. 17.38–17.42 (38) abdominal terga II–VIII without pale scales, (39) abdominal terga IV– VIII with few pale scales, (40) hind tarsomere 1 with white band, (41) wing vein 5 white no dark spot at the point of bifurcation, (42) fore tarsi with narrow pale band (Source: Tyagi 2020)

296

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Vector Identification and Malaria Diagnosis in Major Deserts

Figs. 17.43–17.46 (43) wing vein 3 mainly dark, (44) wing vein 3 mainly white, (45) palpisubapical pale band narrow and subapical dark band broader, (46) hind tarsomere uniformly dark (Source: Tyagi 2020)

17.3

Distinctive Taxonomic Characters of the World’s Two Major Malaria Vectors in Desert Environments, Anopheles stephensi Liston (1901) and Anopheles arabiensis Patton (1905)

About ‘the identification of An. stephensi’, the world famous culicidologist Dr S.R. Christophers, who composed his magnum opus on Tribe Anophelini under the famous The British India series (Christophers 1933), ‘There is no species with

17.3

Distinctive Taxonomic Characters of the World’s Two Major Malaria. . .

297

which this can well be confused; it is the only Indian species with broad thoracic scaling and a double broad pale band on the palpi in which the hind legs are not conspicuously marked with white’. Notwithstanding irrefutable attributes of identification characters of An. stephensi, however, for reasons of posterity, it is considered highly opportune to give hereunder, as an example, a set of distinguishing features of the two major desert specialists, An. stephensi and An. arabiensis, for a better understanding and diagnosis. Both these species can be identified using microscopy, Polymerase chain reaction (PCR method) and TaqMan single nucleotide polymorphism genotyping (SNP).

17.3.1 Morphological Anopheles stephensi is rather more characteristically distinguishable from the rest of species, including An. arabiensis, by a combination of the following characters (Christophers 1933): palpi apical segment all pale, forming, with apex of next segment, a broad pale apical band; a broad apical and basal pale band at 3–4, the dark intervening area narrower than either band; a narrow pale band at 2–3 and some spots formed by patches of white or pale scales on dorsum of segment 3; dorsum of thorax with a conspicuous mat of white scales; and legs with femur, tibia and tarsi characteristically white-spotted (Fig. 17.47). In contrast, Anopheles arabiensis, which was discovered from Aden Hinterland (West Aden Protectorate = Yemen), belongs to the An. gambiae complex whose members are morphologically indistinguishable from another, although it is possible for larvae and adult females which exhibit different behavioural traits for each species. Although close to An. stephensi in appearance, it is nevertheless distinguishable by a set of characteristic features on the head, thorax, wings and legs. Anopheles arabiensis, together with other members of the group, can be identified using the molecular methods of Fanello et al. (2002). Recently, a solution to more precise and foolproof identification of An. arabiensis by TaqMan single nucleotide polymorphism genotyping (SNP) was offered by Walker et al. (2007).

17.3.2 Chromosomal Anopheles stephensi has a 2n = 6 (two pairs of autosomes and one pair of heterogamous sex chromosomes, X and Y). The chromosomes exist as five units, the telocentric X chromosome and two metacentric autosomes. Chromosome 2 has arms of unequal lengths. Chromosome 3 has arms of equal lengths (Sharma et al. 1969). The mosquito has three major gene-rich chromosomes (X, 2, 3) and a genepoor, heterochromatic and smaller Y chromosome (Chakraborty et al. 2021). The best identification markers are offered by polytene chromosomes. These are most readably produced from the late 3rd/early 4th instar larval salivary glands and the ovarian germinal cell line.

298

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Vector Identification and Malaria Diagnosis in Major Deserts

Fig. 17.47 Three major distinguishable characteristics of An. stephensi: (a) Apical and subapical white bands of equal length, (b) broad-scaled dorsum of thorax, and (c) all legs pronouncedly whitespeckled (in view hindleg) (Source: Tyagi et al. 1991)

17.3.3 Polymerase Chain Reaction (PCR) In many countries An. stephensi has been subjected to polymerase chain reaction (PCR) for confirming the species and/or its subspecies/sibling species. In Eastern Ethiopia Balkew et al. (2020) sampled a total of 2231 morphologically identified An. stephensi and resorted to further confirmation through a molecular approach incorporating both PCR endpoint assay and sequencing of portions of the internal transcribed spacer 2 (ITS2) and cytochrome c oxidase subunit 1 (cox1) loci and eventually confirmed the identity of the An. stephensi in most cases (119/124; where 119 were PCR confirmed out of the morphologically identified An. stephensi, 124).

17.5

Clinical Diagnosis

299

Khan et al. (2020, 2022) identified the members of the China’s laboratory-reared An. stephensi species complex using genetic markers such as AnsteObp1 (An. stephensi odourant binding protein 1), mitochondrial oxidases subunit 1 and 2 (COI and COII) and nuclear internal transcribed spacer 2 locus (ITS2). Chavshin et al. (2014), in Iran, molecularly characterized biological forms and sporozoite rate of Anopheles stephensi. They first identified biological forms on the basis of number of egg ridges and then sequenced the mitochondrial cytochrome oxidase subunit I and II (mtDNACOI/COII). Further employing species-specific nested PCR method diagnosis of Plasmodium infection was confirmed in the wild female specimens.

17.4

Parasite Diagnosis

17.4.1 Microscopic Despite huge advancements in diagnosing malarial parasites, microscopy is still considered of super value, ‘the Golden Standard’, in the realms of parasitic diagnosis. Several stains of varying attributions are used to highlight morphological features in stark contrasting manner. The most common stain used in dying the parasite is Giemsa stain. It is the preferred method for thick smear where the focus is to easily detect the parasite of parasite and to increase the sensitivity, while Leishman stain is recommended for thin smears for identification of species. In India, and in its Thar Desert ecosystem, a combination of stains named JSB, after its discoverers, Jaswant Singh and Bhattacharji, is used with absolute caution for pH of stains (7.2) (Fig. 17.48). The microscopy is used all over the world, albeit availability of other fast-result yielding tools.

17.4.2 Rapid Diagnostic Test For almost four decades the rapid diagnostic tests (RDTs) have been in use for detecting quickly the presence of a given malaria parasite in an infected human blood, especially P. falciparum, because of requirement of an early decision to manage the case. Rapid diagnostic tests (RDTs) for malaria assist in the diagnosis of malaria by detecting evidence of malaria parasites (antigens) in human blood. These tests require a drop of peripheral blood, normally collected from a finger or heel prick. Visual read-outs are available typically within 20 mins or less.

17.5

Clinical Diagnosis

Malaria is one of the main motives for outpatient consultation and hospitalization worldwide, especially the desert nations or regions due to operational constraints in the inhospitable environments including the mobile and hard-to-reach human populations with inherent migratory attributions. However, its incidence remains

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Fig. 17.48 A thick blood smear using JSB stain showing ring and other stages of Plasmodium falciparum (marked with arrows) (Source: Dr. B.K. Tyagi, personal archive)

unclear because of diagnostic problems and insufficient epidemiological data. Lekweiry et al. (2009) studied on malaria incidence in 237 febrile outpatients attending the two main hospitals of Nouakchott city, Mauritania, during April– August 2007. They diagnosed malaria in patients through the gold standard method of finger prick to prepare thick and thin films and blood-dried filter paper samples for performing nested PCR for malaria parasite species identification and density. The clinical symptoms of fever and other malaria suggestive symptoms recorded by clinicians for initiating ‘presumptive treatment’ further suggested the accuracy of diagnosis. Entomological investigations based on morphological and molecular characterization of anopheline species were conducted in Dar Naïm district. The prevalence of malaria in patients was 25.7%, which mostly comprised Plasmodium vivax 70.5% (43/61), followed by P. ovale 24.6%. Of the total individuals enrolled in the survey, 97.5% were clinically diagnosed malaria and treated accordingly. However, only 26.4% of the clinically diagnosed cases were tested positive. Thus, falsepositive cases (73.6%) among the clinically diagnosed malaria cases were obvious in their investigation. The search for mosquito vectors in Dar Naïm district allowed morphological and molecular identification of Anopheles arabiensis and An. pharoensis.

Malaria Immunity in Desert Populations and Development of Resistance in Parasites against Antimalarials

18.1

18

Introduction

Although several virgin deserts have in recent past exhibited several outbreaks of malaria, yet very few scientific investigations were made on immunity level of the affected communities in such arid environments—the terra incognita for malaria infection—so far and the level of susceptibility/resistance in malarial parasites against the antimalarials in vogue! To understand the mechanism behind the process of immunity development in humans, it is inevitably indispensable to first comprehend the biology of malaria parasite in response to the human immunity (Burrows et al. 2013, 2017a, b) (Fig. 18.1). All people living in malaria endemic areas across the world do get infected by a positive mosquito bite, but the response by individuals, and sometimes specific communities (vide supra), against the malaria parasites may vary a great deal, depending largely on the Plasmodium species, load of infection and host factors, including the level of immunity of the host whose extent of past exposure to the parasite is the driving force behind falling prey or otherwise to the mosquito bite. Many a time persons who got an infective mosquito bite do not exhibit any symptoms of the disease, albeit being positive, and then such people are called asymptomatic carriers. Such masses of silent infection carriers, although possibly immune to pathologic consequences of the malarial parasitic infection, are a dangerous source of future regulation of parasite within the community, if a strongly anthropophilic mosquito like An. gambiae, An. arabiensis or An. stephensi is occurring among them. Uncomplicated malaria in individuals is something which is easily treatable, and the affected persons can go home after successful treatment. However, the most threatening of all is the severe (complicated) malaria which inevitably requires timely hospitalization and treatment procedure followed under constant care of specialist medical personnel. Often severe malaria turns out to be deadly. Severe anaemia and multi-organ damage in varying manners, including cerebral malaria, are brought about by microvascular obstruction by the infected

# The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_18

301

302

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Malaria Immunity in Desert Populations and Development of Resistance. . .

Fig. 18.1 The life cycle of malaria parasites in the mosquito (sexual phase) and in the human host (asexual phase), according to present views on the exo-erythrocytic schizogony (Free Wikipedia)

red blood in finer capillaries—a characteristic feature for P. falciparum, but also likely in case of P. vivax.

18.2

Malaria Endemicity and Immunity Development

Among all vector-borne human diseases, malaria offers a well-defined pathway for evolution of immunity in the affected person or community, albeit repetitive recurrence of episodes by malaria particularly engineered by Plasmodium vivax which can remain dormant in the liver cells for weeks, months or even years (Bruce-Chwatt 1985). Malaria is also one of the oldest communicable diseases known to human being inhabiting especially the tropical and subtropical regions of the world. Due to long exposure to malaria infections the affected communities, such as those in Africa and in India’s state of Odisha (old name Orissa) where proportion of P. falciparum among infected people is more than 90%, peoples’ immunity against the infection rose a very great deal. Malaria has in fact been eventful in dictating the psyche of nations reeling under its catastrophic impacts making people physically weak, mentally feeble and economically impoverished, and despite maximum global and national campaigns to wipe it off from the face of the world, it still continues to be one of the most serious, life-threatening infectious diseases.

18.3

Biology of Malaria Parasites

Five protozoan parasites cause malaria to humans, viz. the Plasmodium vivax, P. falciparum, P. malariae, P. ovale and P. knowlesi, implying different immunity types by them in the affected communities. Globally P. vivax is the most common parasite responsible for the largest public health burden particularly in Asia and South America; in Africa it is P. falciparum which abounds and causes maximum

18.3

Biology of Malaria Parasites

303

illnesses and deaths especially among children below 5 years of age and the pregnant women. During a blood meal on a healthy human being—the main and final host—an infected Anopheles mosquito bite introduces, along with the saliva having anticoagulating properties, the malaria parasite (sporozoite stage of Plasmodium) into the human blood vascular system. As soon as sporozoites—spindle-shaped, motile and infective—enter the human body, a large proportion is either destroyed by phagocytes or other mechanism; however those, still in thousands, are able to complete their peregrination within 30–60 minutes. These sporozoites, which are injected in to thousands per bite, encounter an array of challenges for their survival in the human body. Genetically guided to reach their earliest destination, i.e. hepatocytes, sporozoites travel a lot crossing over the skin, lymphatics and other organs and finally into the liver. Here sporozoites, by a process of asexual binary fission (schizogony), transform into round-shaped bodies called (primary) schizonts harbouring tens of thousands of smaller form of the parasite, the merozoites (the stage that results from multiple of a sporozoite within the body of the host). Upon reaching a stage of maturation these schizonts burst out due to growing inner pressure of fissions and release merozoites into the bloodstream where they, by a very intricately designed modus operandi, enter red blood cells to complete an important part of the parasite biology, heralding the symptomatic stage of the disease. Symptoms develop 4–8 days after the initial red blood cell invasion. The replication cycle of the merozoites within the red blood cells lasts 36–72 hours (from red blood cell invasion to haemolysis). Thus, in synchronous infections (infections that originate from a single infectious bite), fever occurs every 36–72 hours, when the infected red blood cells lyse and release endotoxins en masse. Here in the red blood cells merozoites live and replicate (erythrocytic schizogony) on the cost of haemoglobin, causing severe anaemia in people with heavy infection, on one hand, and a fraction of them (i.e. those that are inherently bound to commit sexually later in the vector mosquito’s body) differentiate and mature into male and female gametocytes, ready to be picked up by the mosquito during feeding and infect the new host, mosquito. The transcription factor AP2-G regulates the commitment to gametocytogenesis. The duration of gametogenesis differs by species. After completing a highly fascinating extrinsic (sporogony) stage of its life cycle in the mosquito host, the male (following a spectacular event of exflagellation, a phenomenon producing eight microgametes after three rounds of mitosis) and female (attaining more or less a receptive roundish form called macrogamete) gametocytes fuse to form a diploid zygote in mosquito that soon transforms to a motile and injectable parasite stage able to bore through the inner wall of the gut. The parasite then moves further across the wall to form round-shaped oocysts on the outer wall of the gut. Each oocyst is generating tens of fine, spindle-shaped sporozoites. When these oocysts burst, the sporozoites are released into an unknown world of body cavity (hemocoel), but they make it to their final destination in the invertebrate host, the salivary glands. The maturation of sporozoites in the gut of the mosquito is highly temperature-dependent. The entire duration of extrinsic cycle may take about 7–15 days depending on temperature and other abiotic factors.

304

18.4

18

Malaria Immunity in Desert Populations and Development of Resistance. . .

Clinical Symptoms and Treatments

The clinical symptoms of malaria, after a successful infective mosquito bite, may generally appear in 7–10 days. Typical initial symptoms are low-grade fever, shaking chills, muscle aches and, in children, digestive symptoms. These symptoms can present suddenly (paroxysms) and then progress to drenching sweats, high fever and exhaustion. Malaria paroxysmal symptoms manifest after the haemolysis of Plasmodium spp.-invaded red blood cells. The human malaria parasites P. vivax and P. ovale also have dormant stages called hypnozoites or secondary schizonts which can be activated and emerge from the liver months or even years after the initial infection, leading to relapse of the infection if not treated properly. The 4-aminoquinoles (e.g. chloroquine) are administered to treat erythrocytic stages of parasites, and 8-minoquinolones (e.g. primaquine), under strict instructions of the physician, are provided to treat liver schizont (primary and secondary) as well as the gametocyte stages of Plasmodium vivax. In case of an infection with P. vivax, a 3-day chloroquine and 14-day primaquine are administered. When infection is by P. falciparum, then the patient is treated with ACT-L (artemether-lumefantrine), in northeastern states of India, and ACT-SP (artesunate + sulphadoxine pyrimethamine) in the rest of India. Intramuscular (IM) administration of selective antimalarials such as quinine (or quinidine) and/or injectable form of artemisinin derivatives, e.g. artesunate (AS) and artemether (AM), may be used for the management of severe and complicated malaria cases (adults and non-pregnant women only) in the dosage given below: artesunate, 2.4 mg/kg bw IM/IV followed by 1.2 mg/kg bw after 12 hours and then 1.2 mg/kg bw once daily for total duration of 5 days. Only qualified clinician is to decide the course of treatment.

18.5

Parasite Resistance against Antimalarials

The parasite is considered susceptible if no parasite is found on day 6 following chloroquine treatment and none is present on day 7, provided there is complete failure of parasites to reappear by day 28 on a month-long follow-up. If asexual parasites disappear for at least 2 consecutive days following treatment but return and are present on day 7, they are resistant at Ri level (7 day test); any recrudescence of asexual parasites within 28 days (extended test) also indicates an Rl response. In present context, a parasite is said to be resistant only when it shows resistance at the level of Riii (Table 18.1). There is very little information available on the development of resistance in P. falciparum against any antimalarial drug in the deserts, and the Thar Desert region is no exception, and what is known till date is but for chloroquine (Sharma et al. 1995; Tyagi and Chaudhary 1997). Earliest in vivo investigations carried out in south-western Rajasthan between 1981 and 1984 indicated 100% parasite susceptibility to chloroquine 600 mg base (Khatri 1991). As presented in Table 18.1, however, the parasite was shown to have developed resistance in course of time in many desert districts at all of the Ri, Rii and Riii levels, besides in some non-desert

18.5

Parasite Resistance against Antimalarials

305

Table 18.1 Chloroquine sensitivity results against P. falciparum in the Thar Desert districts District Bikaner Jodhpur Jaisalmer Barmer

Jalore

Year 1992 1991 1990 1994 1990 1992 1994 1993

No. tested 20 11 20 12 59 33 12 35

No. susceptible 5 0 9 0 11 0 0 6

S/R 10 0 2 2 4 29 8 7

Ri 5 5 90 38 1 0 18

Rii 0 2 0 0 2 2 4 4

Riii 0 4 0 0 4 1 0 0

% Riii 0 36.4 0 0 3.8 3.0 0 0

S = Susceptible; R = Resistant; R i-iii = Resistant status Table 18.2 Results of a study on chloroquine resistance development in P. falciparum carried out in certain Thar Desert districts in October 1994 District Barmer Jaisalmer

PHC Baitu Pokaran

No. of cases examined 12 12

S/Ri (%) 8 (66.6) 12 (100,0)

Rii (%) 4 (33.3) 0 (0.0)

Riii (%) 0 (0.0) 0 (0.0)

districts as well (Sharma et al. 1995). In as far as Thar Desert is concerned, P. falciparum resistance development against chloroquine was demonstrated in at least five districts, viz. Barmer, Bikaner, Jaisalmer, Jalore and Jodhpur. In two of these, namely, Barmer and Jodhpur districts, all the Ri–Riii level resistance had been detected, although the Riii, in particular, was on an average more strongly represented in Jaisalmer district (36.4%) than in Barmer district (3.3%). While frequency of resistance development in P. falciparum appeared stronger in Jalore district with both Ri and Rii already manifested, it is still restricted to Ri level in both Jaisalmer and Bikaner districts. Recently, in 1994, in a small sample of 12 cases studied in both Barmer and Jaisalmer (Table 18.2), 100% susceptibility was observed in the latter district, while 66.6% susceptibility and 33.3% Ri level were obtained in the former (cf. Sharma et al. 1995). In spite of availability of above data, it has been argued if the drug resistance had actually evolved in the parasite. Two observations worth considering are: (i) These results were based on small samples, and therefore it is difficult to implicate marked degree of resistance development; also all these observations were based on in vivo studies which might not be free from certain natural deficiencies generally encountered in field investigations. (ii) Many of these studies have been done with 1500 mg of chloroquine while the prescribed dose for presumptive treatment of malaria is only 600 mg of chloroquine. Even so there is no room for complacency with respect to low level of drug resistance in the Thar Desert district because many of the neighbouring non-desert districts exhibit even Riii level of resistance in P. falciparum which can easily disseminate to the Thar region.

306

18.6

18

Malaria Immunity in Desert Populations and Development of Resistance. . .

Malaria Treatment and Immunity

Extremely few studies have so far been made on the subject of treatment management of malaria, particularly falciparum malaria, and the role of immunity in the rural Thar Desert community in combating the invasion of disease (Bhu 1972; Panagaria and Mehta 1975; Tamboli and Bolya 1981). While general chemoprophylaxis of malaria in Rajasthan was highlighted by Chandra (1981), ways to manage severe falciparum malaria in children were discussed by Mathur (1990). While treating cerebral malaria patients in Bikaner, Kochar (2001) had suggested that intramuscular injection of phenobarbitone helped reduce the incidence of convulsions from 12.3% to 2.9% in comparison to 23% in those who did not receive phenobarbitone. Kochar et al. (1999) also studied the effect of intramuscular arteether (150 mg daily for 3 days) on electrocardiogram in 16 patients from Bikaner suffering with falciparum malaria (three patients having jaundice, three with cerebral malaria and ten uncomplicated malaria). Before treating with arteether five patients had tachycardia. The mean RR interval before starting the treatment was 0.59 sec which increased progressively till the third day after the treatment. No significant differences were detected in the mean corrected QT interval, PR interval, QRS duration and diastolic BP before initiating the treatment and at the end of the treatment on the third day. The profile of ECG changes did not differ between patients of uncomplicated and complicated malaria. It was advocated, therefore, that absence of any significant effect on BP and ECG changes precludes the significant effect of arteether on the cardiovascular system when compared to quinine which might cause hypotension, arrhythmia and QTc prolongation. That falciparum malaria presenting with bilateral gangrene of feet could develop arrhythmia/ventricular fibrillation after subjecting to the quinine therapy was discussed by Kochar et al. (1998a, b, c). The true status of immunity level of the Thar population is not known, although malaria has been existing there for decades. Following the massive 1994 outbreak of malaria in the Thar Desert, Sharma (1995) had suggested that the onslaught on the immune system of the local population was responsible for large number of deaths in the desert. His theory is based or the fact of isolation and sequencing of the knob protein gene that induces protuberances on the surface of infected erythrocytes through which they adhere to the cerebral capillaries and are thus partly responsible for cerebral malaria. The knob protein gene shows that there are at least two alleles of the gene in the Indian P. falciparum isolates. One of these alleles is rare whereas the other has a frequency of at least 1:8. The major sequence variations occur in the immunogenic domain, but there are also certain random point mutations. A foolproof correlation of these alleles with the strain of cerebral malaria in the Thar Desert or even Rajasthan state is yet to be established.

Malaria and Climate Change

19.1

19

Introduction

Climate change is a global phenomenon which has affected virtually everything biotic and abiotic on earth. In context with public health the phenomenon of climate change is always seen from the angle of human intervention called anthropization comprising an array of activities such as population explosion, migration en masse, massive forest fire, long-time pesticide deployment in agro-forestry and public health programmes, devastating droughts and floods, tsunamis and earthquakes, etc. Human population boom is the root cause of many ill-effects that emerged out of schemes otherwise planned for human development and growth. It is notable that, in contrast to resources available for sustenance, the human population has rapidly grown particularly since 1950, from 2.5 billion to 7.8 billion in 2020, viz. the overall burden of population has increased by 206.8%, with their pets and those in the wild, having multiplied even more, but at the same time many of which are essential for maintaining life cycle of a large number of hematophagous vectors and even zoonoses. Under the pressure of population build-up, the climate has directly or indirectly affected human behaviour per force and driven humans to, besides mushrooming urbanization, multilevel buildings, development schemes such as hydro-agriculture, quarry-mining, etc., practise container-associated water-storing habits—a major reason for attraction to several human health-related issues correlated to vector- and water-borne diseases, food and drinking water insufficiency, and heatstroke, respiratory and mental health-related disorders arising out of natural disasters, e.g. tsunamis, earthquakes, droughts, floods, etc. (Patz et al. 2014). Temperature is the most important of all abiotic factors influencing the epidemiology of vector-borne diseases. Therefore, it is not surprising to correlate an explosive expansion of Aedes albopictus, along with chikungunya it transmitted virulently, from Asia and Africa to most of Europe and the Americas post-2005/ 2006 epidemics in the Indian Ocean island territories, perhaps in the wake of a temperature rise by merely 1 °C. A similar inference involving anthropization-driven # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_19

307

308

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Malaria and Climate Change

climate change can be drawn for recent expansion of the malaria vector, Anopheles stephensi, an Indian species, towards Sri Lanka in south and to Africa in west during the past one decade—all these nations being terra incognita for the species until early 2000. Sri Lanka which was declared malaria-free recently is threatened by a relapse of the disease, whereas African countries which have witnessed the unwelcome entry of An. stephensi, credited for its high potential for Plasmodium falciparum transmission, fear unprecedented exacerbation of malaria cases, with severe epidemics, in several nations adjoining the Horn of Africa (Sinka et al. 2020). Malaria, being an important public health problem in spite of considerable success achieved in reducing the disease burden over the years, particularly in a hyperendemic country like India where 100 million cases, and about 100,000 deaths, used to occur every year by the first quarter of the twentieth century, is highly sensitive to environmental vicissitudes and is often irreversibly influenced by the dynamic climate change (Caminade et al. 2014; Parham and Michael 2010). Climate change affects both the density build-up and distribution of malaria vectors. Malaria vectors’ feeding and transmission patterns of parasites may also be affected by the climate change particularly in exophagic climate generalists. As a consequence of global warming, the ambient temperature on an average basis has already risen by around 1 °C since pre-industrial times. Worldwide emissions of greenhouse gases (GHGs), aerosols, large-scale deforestation and changes in land use and land cover (LULC) are significant non-stationary drivers for the climate change, which in turn substantially altered the atmospheric composition and consequently the planetary energy balance in favour of the spread of vector-borne diseases, especially malaria. A temperature increase could, however, also increase malaria transmission in colder regions such as the plateaus of East Africa (Kifle et al. 2019). Post-1950 climatic oscillations intensified many environmental phenomena to their extremes such as heat waves, droughts, severe cyclones, changes in precipitation and wind patterns, acidification of the global oceans, melting of sea ice and glaciers, rising sea levels and changes in marine and terrestrial ecosystems, etc. Desert ecosystems, too, have been highly vulnerable to climate change, and any alteration in either temperature or rainfall in the Thar Desert’s IGNP (Indira Gandhi Nehar Pariyojana) command area, endowed with copious greenery and water, is clearly discernible in context with life cycles of both vectors and parasites involved in vector-borne and zoonotic diseases, of which malaria is the deadliest. As far as deserts are concerned, desert margins, where millions of people live in tropical Africa, Asia and South America, are the most vulnerable ecosystems for malaria parasite and vector population development under the impact of seasonal environmental conditions. Desert marginal areas are also highly susceptible to seasonal epidemic malaria. These desert margins are actually buffer areas between rain-deficient arid and rain-abundant non-desert regions. Although, due to high temperature and low humidity in these marginal areas, the development and productivity of both vectors and the parasites within it is generally limited, nevertheless the climate variability brings about the highest potential to strongly impact disease dynamics in the desert margins. Thus, climate variability is the key to the

19.2

The Sahara Desert

309

fulmination or exacerbation of malaria in the desert margins where they can be used as early-warning tools. Long-time data assimilation on impact of climate on malaria may be developed into important malaria early warning systems (MEWS). Multiyear non-stationarities of various interventions in malaria control such as that in India, where improved socio-economic conditions and disease control policies involving use of rapid diagnostic kits and indoor residual spraying (IRS) have been revised every few years, are often reflected in the shifting patterns of malaria incidence, hence a challenge to predictability or early warning mechanisms. Land-use change associated with irrigation projects like the famous Indira Gandhi Nehar Pariyojana (IGNP) is an important driver of malaria non-stationarity in arid northwest India which has enhanced the extent of multi-vector environment in varied breeding sites. To develop an operational early warning system, which itself functions on multiple time scales, all the relevant factors including interventional efforts and socioeconomic conditions, in addition to vector bioecology, need to be considered. More studies need to be done on the underlying factors, both abiotic and biotic, which facilitate a commensurate rate of development of vectors as well as parasites within the invertebrate host. Baeza et al. (2013), citing the phenomenal works of Bouma and van der Kaay (1994, 1995, 1996), Bouma et al. (1994a, b), Tyagi (1995a) and Tyagi et al. (1995, 2002), have made a very interesting observation pertaining to long-lasting transition towards sustainable elimination of desert malaria under irrigation development, with special reference to the Thar Desert in western India. They deduced that in arid areas, people living in the proximity of irrigation infrastructure are potentially exposed to a higher risk of malaria due to changes in ecohydrological conditions that lead to increased vector abundance, blood-feeding and breeding galore. However, irrigation provides a pathway to economic prosperity that over longer time scales is expected to counteract these negative effects, provided all involved stakeholders play their roles meticulously and keep malaria at bay through proper water management (Tyagi 2004a, b).

19.2

The Sahara Desert

Climate change will probably alter the spread and transmission intensity of malaria in Africa. Driven by humongous greenhouse gas and land-use changes in Africa, it is being constantly felt that climate changes will in recent future significantly affect the spread of malaria in tropical Africa well before 2050, impacting the vast ranges of Sahara as well. The geographic distribution of areas where malaria is epidemic might have to be significantly altered in the coming decades (Ermert et al. 2012). Indirect effects of climate change on malaria might be more important than direct effects (Saugeon et al. 2009). The sensitivity of vector-borne diseases like malaria to climate continues to raise considerable concern over the implications of climate change on future disease dynamics. The problem of malaria vectors shifting from their traditional locations to invade new zones is of important concern, e.g. Anopheles arabiensis, which probably originally belonged to the Arabian deserts, and An.

310

19

Malaria and Climate Change

stephensi, an Indian mosquito which invaded Africa during last decade only. A mathematical model incorporating rainfall and temperature is constructed to study the transmission dynamics of malaria. The reproduction number obtained is applied to gridded temperature and rainfall datasets for baseline climate and future climate with aid of GIS. Gething et al. (2011) highlighted the transmission intensity of falciparum malaria in context with geographic patterns and observed highest transmission intensity in the tropics as well as the coastal areas of East Africa as compared to subtropics where low levels of transmission intensity occurred.

19.3

The Thar Desert

The Thar Desert is among the youngest deserts in the world as well as built over the once probably a sea coast meeting the mouth of a unified and richly flowing Saraswati river, now completely extinct, together with currently partially extant Ghaggar river on the northeastern margin of the desert and the distantly drifted eastwardly Yamuna river, now bracing scores of kilometres away the capital city Delhi. Yet, the Thar Desert hides within its expansive breadth rare and copious antiquities revelation of which is gradually surfacing to comprehend the extent of metamorphosis the desert has so far undergone.

19.3.1 Physical Transformation in the Thar Desert Climate Thar Desert of today was certainly not so in the remote past; its topography, ecology and physiography vastly changed during the last 60–80 years following the entry of three major canal water systems that converted the desertic surroundings of the desert, in the canal-water rich areas, into verdure, greatly affecting the epidemiology of a disease like malaria.

19.3.1.1 Rainfall The Thar Desert, like most other deserts of world, endured truly desertic and arid environments till the close of first quarter of the twentieth century whereafter, owing largely to initiation of hydro-agriculture development programmes to bring water from Punjab to the Thar Desert for mainly improving land productivity for agriculture and quenching the thirst of its inhabitants, transformed at least partially into a verdant area attracting higher amount of rainfall, lowering of ambient temperature and enhancing per capita income in Sri Ganganagar district that surpassed any of the other desert districts. In contradiction to the findings by Winstanley (1973a, b), Pant and Hingane (1988) analysed rainfall and temperature during 1901–1982 and found an increasing trend in mean annual rainfall (141.3 mm for 100 years) and a decreasing trend in air temperature (-0.52 °C for 100 years). Later, Ramakrishana and Rao (1991) studied increase in the mean decadal rainfall in a canal-irrigated district for a considerable period.

19.3

The Thar Desert

311

Three of the 12 desert districts have been greatly benefitted with the supply of canal waters since the beginning, viz. Sri Ganganagar (irrigating 708,775 ha of land), Bikaner (irrigating 37,022 ha of land) and Jaisalmer (irrigating 84 ha of land), with the Gang Canal and the Indira Gandhi Canal projects aiming to utilize 7.59 MAF of water to irrigate about 1.143 mill-ha area (Roy 1983). Sri Ganganagar district which earlier received an annual rainfall of 243 mm per year, following the mega IGNP project in the Thar Desert, enjoyed an increasing trend of rainfall, at the rate of 1029 mm year/year, during the period 1926–1993.

19.3.1.2 Air Temperature Due to change in rainfall and its trend over a considerable area in the IGNP command area, air temperature too presented generally a decreasing trend in Ganganagar (by 0.0393 °C year-1), Bikaner (by 0. 0233 °C year-1) and at Jaisalmer (by 0.0093 °C year-1) (Rao 1996). 19.3.1.3 Relative Humidity High rainfall and lower ambient temperature trends also influenced humidity which was recorded 5–10% higher in the IGNP’s cropped surfaces at 1 m height in the irrigated villages compared to that in the unirrigated cropped surfaces (Rao 1996). In conclusion, it is more than obvious that the Thar Desert has undergone a considerable change in its physiography particularly after the initiation of the three major canalized irrigation systems, particularly the IGNP, although Tewari (2021) has sounded a warning in the wake of global warming and suggested on the grounds of a joint study conducted by the Birbal Sahni Institute of Palaeosciences, Lucknow, and Jawaharlal Nehru University, Delhi, that the climate change had already resulted in the monsoon shifting towards a drier Thar Desert in Rajasthan and Gujarat leading to frequent floods in the two states along with erratic rainfall events over all the places. Bouma and Van Der Kaay (1995), on the other hand, highlighted the role of El Nino in accentuating the malaria incidence and emergence of outbreaks in the Thar Desert. Tyagi et al. (1995) disagreed with the El Nino theory and instead put forth their theory of ‘vectorism’, i.e. co-occurrence of multiple vectors (e.g. An. stephensi, An. culicifacies and An. subpictus) in a single ecosystem otherwise harbouring nominal representation (e.g. An. stephensi).

19.3.2 Malariological Transformation in the Thar Desert Climate The Thar Desert region was defined as an area with low and unstable malaria with occasional outbreaks. After initiation of the three major canal systems, viz. Gang Canal (1923), Sirhind Canal (1955) and the Indira Gandhi Canal (1958; water began to flow only in 1962), the ecology and physiography of the canal-impacted region (10–15% of the Thar land) greatly altered, triggering an anthropization-linked permanent changes in the climate pattern which favoured the formation of the extensive mosquito breeding habitats of varying nature, high-vector densities and intrusion of new malaria mosquitoes earlier unknown for the region. Consequently,

312

19

Malaria and Climate Change

having changed a great deal for the worse malariologically, the Thar Desert witnessed a high prevalence of disease, with several epidemics, reported in the desert during last 30 years. It is evident from data for the period 1961–1994 that not only has the slide positivity rate in the desert region increased 3.5-fold, but Plasmodium falciparum incidence also increased as much. Along with Anopheles stephensi, the traditional malaria vector in the xeric environment, another significant vector of the Indian mainland, An. culicifacies, has also established itself in the areas extensively irrigated through canals. To prove point that malaria is influenced by anthropogenic activity-driven climate change, Tyagi et al. (1994) conducted entomological and parasitological investigations in four Thar Desert villages, viz. Madassar and Awai (ambient temperature and relative humidity about 22 °C and 50–60%, respectively), situated in the IGNP command area in the Jaisalmer district, and Kanasar and Khetusar (with ambient temperatures and the relative humidity in summer averaging around 35–40 ° C and 25–30%, respectively), scores of kilometres away from the Indira Gandhi canal in the uncanalized area (Fig. 19.1). To conduct socio-epidemiological studies, in the outset itself all the houses in the study villages were numbered, population per house enumerated and family details recorded on pretested proformas (Black 1968).

19.3.2.1 Entomological Investigations (i). Results on Immature Surveys For sampling larvae from shallow sources of water, a long handle dipper was used (10 dips); larvae were then transferred to enamel trays for calibration, and the fourth instar and/or pupae were transferred to individual test tubes with small amount of water for allowing emergence. The test tubes were closed at the mouth with a piece of cotton to prevent escape of the emerged adult. The larvae were sampled from ‘Tanka’ and ‘Beri’ with the help of a 5 lit. Bucket (Tyagi 1998a, b). Immatures were identified using Puri (1960). Larval instars belonging to An. culicifacies, An. stephensi, An. subpictus and An. annularis were sampled from a variety of breeding habitats including irrigation canals, ponds, ‘khadin’, ‘nadi’, ‘tanka’ and ‘beri’. Only An. stephensi bred in the ‘tanka’ and ‘beri’, while An. culicifacies was dominant in irrigation channels, stagnant water along the canals and the swamp. Anopheles subpictus was found breeding in the post-monsoon open-ground pools and the cement tanks filled with water for cattle drinking. (ii). Results of Indoor and Outdoor Resting Vector Mosquitoes Indoor and outdoor sampling of adult mosquitoes was carried out in randomly selected six human dwellings and six cattle sheds in each of the four villages between 0600 h and 1000 h, using mouth-operated aspirators and torch lights (Fig. 19.2). A small field laboratory was set up for preparing parasitological microslides, dissecting mosquitoes and identifying microscopically both the vectors and parasites by species. While the adults were processed for specific identification

19.3

The Thar Desert

313

Fig. 19.1 Location of study villages in the IGNP command area (1 = Madassar village, 2 = Awai village) in Jaisalmer and desertic non-command area (3 = Kanasar village, 4 = Khetusar village) in Jodhpur districts, in the Thar Desert, north-western Rajasthan (India)

following Christophers (1933) and Harrison and Scanlon (1975), they were also additionally classified for their abdominal (unfed or fully fed) condition and follicular status to determine parity rate. Malaria parasites were diagnosed on the basis of characteristic features of different parasitic stages particularly the ring and gametocytes. A report on diagnosis of positive cases was passed on to the auxiliary nurse midwife (ANM) for dealing with these cases. A total of eight Anopheles species were sampled from all types of collection (Table 19.1) among which Anopheles stephensi dominated the collection from human dwellings and cattle sheds in all the villages in irrigated and unirrigated villages, followed by An. culicifacies, An. subpictus, An. annularis, An. nigerrimus, An. vagus, An. splendidus and An. d’thali. Anopheles nigerrimus pronouncedly oriented during dusk in collections in the vicinity of the forest along the Indira

314

19

Malaria and Climate Change

Fig. 19.2 Adults of Anopheles stephensi captured in the Thar Desert villages during (a) dawn and (b) dusk (Source: Dr. B.K. Tyagi, personal archive)

Gandhi main canal, as it was attracted towards the light of torches and vehicle headlights. The relative density, expressed as the number of females collected by one man during a 1 h period, is graphically presented in Fig. 19.3. The average density per man-hour of An. stephensi (17.1; range 0.0–47.2) was the highest, with maximum density in April and minimum in January. Another important vector, A. culicifacies (average pmh 3.3; range 0.0–14.1), showed maximum density during the monsoon

19.3

The Thar Desert

315

Table 19.1 Females of anopheline species collected in the irrigated and unirrigated villages (HD = human dwelling; CS = cattle shed; PMH = per man-hour density; other species = Anopheles vagus, An. splendidus and An. d’thali)

Species An. stephensi An. culicifacies An. subpictus An. annularis An. nigerrimus Other species

Irrigated villages Indoor collection HD CS Total (%) 635 588 1223 (29.6)

Unirrigated villages Indoor collection HD CS Total (%) 230 200 430 (10.4)

PMH Density 23.8

316

342

658 (15.9)

13.5

0

0

0

0.0

479

606

1085 (26.2)

22.6

24

31

55 (1.3)

1.1

257

236

493 (11.9)

10.2

0

0

0

0.0

29

23

52 (1.2)

1.0

0

0

0

0.0

99

47

146 (3.5)

2.8

0

0

0

0.0

May

Jun

Nov

Dec

PMH Density 8.1

Per man-hour density

50 40 30 20 10 0 Apr

Jul

Aug

Sep Oct Month

Jan

Feb

Mar

Fig. 19.3 Comparison of the relative density (per man-hour density) among Anopheles stephensi, A. culicifacies and A. subpictus in the irrigated and unirrigated villages (1993–1994); A. subpictus; An. stephensi; A. culicifacies; An. stephensi A. culicifacies; A. subpictus (Source: Tyagi 2002)

months of July–September. Anopheles subpictus rose in density with the onset of the monsoon in late June due to the existence of rainwater-fed surface breeding habitats and remained abundant until December (average pmh 11.6; range 9.7–33.1). Anopheles stephensi is conspicuous by its constant presence in unirrigated villages despite extremes of ambient temperature (average pmh 7–0; range 0.0–18.7). In these villages An. subpictus also occurred in low densities between August and December (average pmh 1.1; range 0.0–7.0), but An. culicifacies was characteristically absent throughout.

316 Table 19.2 Anopheline species collected simultaneously from man and cattle to show anthropophily/ zoophily of five of the eight species

19

Species Anopheles stephensi Anopheles culicifacies Anopheles annularis Anopheles subpictus Anopheles nigerrimus

Malaria and Climate Change

Number of females collected Man (%) Cattle (%) 151 (52.2) 138 (47.8) 78 (26.8) 213 (73.2) 2 (3.7) 51 (96.3) 11 (4.8) 215 (95.2) 71 (98.6) 1 (1.4)

(iii). Simultaneous Collection of Biting Mosquitoes from Cattle and Humans In order to establish proclivity for feeding on either animals, humans or both, adult females were simultaneously captured prior to initiate feeding on a human volunteer who was made to lie down on a cot near a buffalo calf tethered at a distance of 3 m, between 1900 h and 2100 h. Collection of pre-biting female adults from a human volunteer and a buffalo calf was carried out by two different insect collectors. Results of collections showed An. stephensi was collected about equally from each (Table 19.2). Surprisingly, An. nigerrimus showed the strongest preference for orientation on the human, but only in the presence of flashlights. It did not, however, feed preferably on human blood. Anopheles culicifacies proved to be zoophilic, like An. annularis and An. subpictus. (iv). All-Night Human Biting Collection of Mosquitoes Further, in order to determine peak biting periods of the various vector mosquitoes, sampling of biting mosquitoes was also made overnight (1800–0600 h) from two sleeping volunteers. The overnight collection per human volunteer was made by two insect collectors, taking turns to not exceed 2 hours of collection per insect collector at a stretch. Four species, namely, An. stephensi, An. culicifacies, An. subpictus and An. Nigerrimus, were captured during the night biting collection. Characteristically both An. stephensi and An. culicifacies exhibited two feeding peaks, one early in the night and the other just before the dawn (Fig. 19.4), the knowledge of which carry a great epidemiological significance from control point of view. Anopheles culicifacies fed earlier than An. stephensi and stayed in higher densities until just before drawn. In contrast, An. stephensi exhibited a better adjustment to ambient temperature and remained active throughout the night. Apparently attracted to the flashlights, Anopheles nigerrimus was collected in large numbers in the early hours of the night only. Diagnosis of blood meal indicated An. stephensi to have a greater preference for human blood (58.2%) compared to that of either An. culicifacies (23.4%) or An. subpictus (13.4%). (v). Vector Incrimination with Malaria Parasite The female mosquitoes (total # 2625) belonging to eight Anopheles species were processed for vector incrimination. For this, they were dissected in normal saline for the examination of parasitization in either or both gut and the salivary glands. The

19.3

The Thar Desert

317

No. of females collected

60 50 40 30 20 10 0 18–19 19–20 20–21 21–22 22–23 23–24 24–01 01–02 02–03 03–04 04–05 05–06 Hour duration

Fig. 19.4 Graph showing orientation of four important anopheline species for anthropophily during all-night human-bait collection (note characteristic twin peaks for orientation of the vector Anopheles stephensi and A. culicifacies, in particular); An. stephensi; A. culicifacies; A. subpictus; A. nigerrimus (Source: Tyagi 2002)

Table 19.3 Anopheline species naturally incriminated with malaria parasite (SG +ve = salivary gland positive for sporozoite; G +ve = gut positive for oocyst)

Species Anopheles stephensi Anopheles culicifacies Anopheles subpictus Anopheles nigerrimus

Irrigated villages No. SG dissected +ve 850 3

G +ve 0

Unirrigated villages No. SG dissected +ve 102 1

Total 3

938

1

6

7

0

451

1

1

2

40

0

0

0

G +ve 1

Total 2

0

0

0

284

0

1

1

0

0

0

0

infected mosquitoes were preserved for future reference. Only An. stephensi, An. culicifacies and An. subpictus, sampled during dawn and dusk collections, could be incriminated (for salivary glands, p-test or ϰ2 = 1.768; for gut, ϰ2 = 0.36) (Table 19.3). Anopheles stephensi is a truly original desert species, ecologically best adapted to arid environments of the Thar Desert (Zahar 1990a, b; Tyagi 1994a, 1995a, 2002). Although A. culicifacies, A. subpictus and A. annularis were reported earlier from the urban limits of Bikaner (MacDonald 1931), none were parasitologically proved then to be a vector in the desert. For the first time, therefore, An. culicifacies has been shown to be a vector in the highly canal-irrigated Sri Ganganagar district (Tyagi and Verma 1991), while An. stephensi was proved to be the sole vector in the xeric

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Malaria and Climate Change

Jodhpur district (Tyagi and Yadav 1994). Anopheles subpictus, occurring in both irrigated and unirrigated villages, was incriminated only in the IGNP command area in the eastern Jaisalmer (Tyagi 1996g). This situation calls for a strong effort to annihilate vector populations before the situation worsens.

19.3.2.2 Parasitological Investigations To determine the load of malaria parasitic infection in the rural community, monthly fever surveys of all febrile cases were conducted in all villages. Blood sample, using finger-prick method involving a fresh medical lancet, was collected from febrile cases contacted door to door, with history of their sickness recoded. The slides with both thick and thin blood films were stained either in Giemsa or JSB (Jaswant SinghBhattacharji) for differential characterization of parasites. Later, after confirmation of positive blood sample, the concerned patient was also given radical treatment according to the national policy through either the auxiliary nurse midwife (ANM) or the multi-purpose worker (MPW) present in the village. A clear impact of canalized irrigation in the desert was visible after a careful scrutiny of results. Following a rapid mass blood survey immediately after the epidemic in the late autumn of 1992 in the two IGNP command villages (Pv 11.1%, Pf 88.7%) and two unirrigated villages (Pv 17.1%, Pf 82.7%), fever surveys were conducted in all the four desert villages during April 1993–March 1994. Results showed a slightly higher slide positivity rate in the IGNP villages (32, 3%) than in the unirrigated villages (25, 5%), but a significantly higher proportion of P. falciparum in the IGNP villages (76.6%) compared to that in the unirrigated villages (16.6%) (Table 19.4). Plasmodium falciparum exhibited two distinct peaks: first, during the summer months of March–April and, second, during December– January (Fig. 19.5). Mixed infections were common in all villages, with a marginally higher proportion in the unirrigated villages (11.5%) than the other two villages (3.2%). Notably the IGNP command villages harboured more gametocyte carriers (16, 17.8%) compared to the unirrigated villages (2, 8.3%). Cumulatively, 73.7% of all the positive cases were found in children of less than 14 years of age. The male population (68.4%) suffered more than the females (31.5%). Male human population was found more parasitized than the females in all villages regardless of the irrigation facility. The reason for more males suffering with infection may be due to their different sleeping and clothing habits, as they prefer to sleep outdoors at night, with fewer clothes covering their skin, as compared to females who essentially sleep indoors while more or less completely covered with the traditional clothes they wear. This difference in sleeping and clothing habits determines the extent and magnitude of exposure of a person to the biting vectors during sleep. Similarly, the adolescent and the adult working age groups were found more positive than the other preceding age groups (Table 19.4).

Mix Gametocyte Pf (%) Pv (%) (%) (%) 42 8 (15.3) 2 (3.8) 12 (80.0) (23.0) 27 10 1 (2.6) 4 (71.0) (26.6) (10.5) 4 13 1 (5.5) 2 (22.2) (72.2) (11.6) 0 (0.0) 5 (83.3) 1 0 (16.6) (0.0) 73 36 5 (4.3) 18 (64.0) (31.5) (15.8)

Source: Tyagi and Yadav (2001a, b)

BSC/ Positive Village BSE (%) Madassar 177 52 (29.3) Awai 101 38 (37.6) Kanasar 65 18 (27.6) Khetusar 29 6 (20.6) 372 114 (30.6)

Prevalence of positives by age groups 12– 5–9 10–14 15 yr 16 (30.7) 10 (26.3) 2 (11.1)

5.0

2.4

18.0

12.2

4.4

5.9

32.9

8.8

ABER API 7.1 20.8

Table 19.4 Results of fever surveys in the four study villages from April 1993 to March 1994 (BSC/BSE—blood slide collected/examined; Pf—Plasmodium falciparum; Pv—Plasmodium vivax; M—male; F—female; ABER - annual blood examination rate, i.e. slides examined as % of population; API—annual parasite incidence, i.e. slide positive cases per 1000 population; m—month; yr—year)

19.3 The Thar Desert 319

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Malaria and Climate Change

16 14 12 Cases

10 8 6 4 2 0 Apr

May

Jun

Jul

Aug

Sep Oct Month

Nov

Dec

Jan

Feb

Mar

Fig. 19.5 Graph showing the relative number of Plasmodium vivax and P. falciparum cases in both irrigated and unirrigated villages (note the high prevalence of P. falciparum in the irrigated ) irrigated villages, ( ) unirrigated villages; villages), during 1993/1994; P. falciparum: ( P. vivax: ( ) irrigated villages, ( ) unirrigated villages (Source: Tyagi 2002)

19.4

Where Is the Thar Desert Heading to Malariologically under Climate Change

Epidemiologically, the Great Indian Thar Desert had been regarded as a region with low and unstable malaria with occasional outbreaks (Sharma 1986a, b). Tyagi et al. (1995), Tyagi et al. (1995), and Tyagi and Chaudhary (1997), however, carried out thorough investigations into the transformation of Thar Desert’s eco-physiography, in the wake of extensive canalized irrigation, particularly the Indira Gandhi Nehar Pariyojana—the largest in Asia with approximately 10,000 km of network of distributaries when completed fully and one of its kind in the whole world in a desert ecosystem—and its impact on malaria conflagration with cyclic epidemics and exceptionally high morbidity and mortality due to P. falciparum, in recent years. Tyagi (2004a) pointed out that the mismanagement of water under the IGNP was a major factor for exacerbating malaria in the Thar Desert. Bouma and Van Der Kaay (1995) inferred that the El Nino phenomenon in the Pacific Ocean played a key role in erring the monsoon trend in India, and the highly erratic rainfall in the Thar Desert had actually accentuated possibilities of the unwelcome outbreaks. Tyagi et al. (1995) questioned the validity of Bouma-van der Kaay’s El Nino Southern Oscillation (ENSO) theory as an early warning system for future epidemics and instead propounded their own theory of ‘vectorism’—a phenomenon that has mushroomed from the ‘desert malaria’—being responsible behind a series of malaria epidemics in the Great Indian Thar Desert in western Rajasthan, India (Tyagi 1997b). During the early twentieth century when the whole country was reeling under the catastrophic impact of malaria epidemics, the Thar Desert in western Rajasthan reported fragmentary cases now and then. In fact, the earliest report of malaria

19.4

Where Is the Thar Desert Heading to Malariologically under Climate Change

321

cases from any part of Rajasthan is from 1909 when 134 hospital admissions were registered, of which 10% were P. falciparum (Green 1911). Sri Ganganagar district in the northern Thar Desert was the first to experience the first major outbreak during 1983/1984. Following heavy rains (average 450 mm; maximum 960 mm) in 1990, the southern parts of the Thar including Barmer, Jodhpur and Pali districts faced a severe malaria epidemic and heavy rains and floods were blamed for the disease outbreak (Mathur et al. 1992; Tyagi et al. 1995; Tyagi 2002). ‘Vectorism’ in the southwestern districts of the Thar Desert built up so heavily in a short time that once again a very severe epidemic broke out in 1992 in the Jodhpur, Bikaner and Jaisalmer districts under the IGNP command area (Tyagi 1994a). The worst of all malaria epidemics in the entire history of the Thar Desert happened in 1994 when more than 300 people succumbed to malaria and several thousands of people became sick due to malaria, mostly P. falciparum (Tyagi 1995a, b). Ever since the Thar Desert has been reporting malaria epidemics and reporting considerable cases every year. Lack of sustained vector control efforts through indoor residual insecticide spraying has been a major drawback, coupled with a moderate to high degree of tolerance/resistance by vector species to DDT, the only insecticide used extensively over the past three decades in the Thar Desert. Taking account of the fact that the Thar Desert is a very different ecosystem from the rest of the country where mostly the local folks suffering with malarial fevers are hard to approach and deliver health care in time, the problem of malaria control has to be tackled with an improvised vector containment methodology which must essentially suit the local conditions, including human behaviour, but must also effectively dissipate vector populations and the disease burden.

Anopheles stephensi: The First Vector to Show an Evolutionary Response to Rapid Climate Change

20.1

20

Introduction

Anopheles stephensi Liston (1901), described primo temporis from its type locality, Ellichpur* (Amroati district, Central Provinces*; Ellichpur is currently known as Achalpur, a city and a municipal council in Amravati district in the state of Maharashtra), India, was regarded by Christophers (1933) as ‘Indian’ and not ‘Oriental’ or even ‘Asian’, in terms of origin, notwithstanding its appreciable range extending eastwards through the Malay states and the East Indies and westwards through Southern Mesopotamia (present-day Iraq and Kuwait and parts of present-day Iran, Syria and Turkey) to as far as the Horn of Africa (Rao 1984; Surendran et al. 2019; Sinka et al. 2020; Dev 2020a, b) (Fig. 20.1). The incursion of An. stephensi into Africa is particularly worrying; over 40% of sub-Saharan Africans live in urban environments, prompting the World Health Organization (WHO) to issue a vector alert: ‘Anopheles stephensi . . . a major threat to malaria control and elimination in Africa. . .’, putting urban populations at significantly increased and potentially new risk of malaria transmission. With African cities growing at an extraordinary rate and 43% of Africans now living in urban areas, the movement of people into urban sites and the observation that An. stephensi are spreading via key transportation routes, meaning it is not inconceivable that this species could be transported large distances and that this may not remain a problem centred on the Horn of Africa. Sinka et al. (2020) felt many cities across the whole of Africa contain potentially suitable habitats for An. stephensi. For example, due to its high population density, Nigeria, appears to be particularly suitable. The most invasive, incursive and ‘silent’ malaria vector mosquito on earth is on the move, and once established, An. stephensi is difficult to control. If it invades large cities, such as Khartoum, Sudan; Mombasa, Kenya; and Dar es Salaam, the region could face malaria outbreaks of unprecedented size. The traditional mosquito interventions via indoor residual spraying and treated bed nets are notably more difficult to implement in cities, and the crepuscular biting habits of An. stephensi suggest they may have less impact on this species than the dominant African vectors. # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_20

323

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Anopheles stephensi: The First Vector to Show an. . .

Fig. 20.1 Geographic range of Anopheles stephensi expanding southwards to Sri Lanka, eastwards through the Malay states and the East Indies, as well as westwards to Southern Mesopotamia and recently far beyond to the Horn of Africa (Source: Adapted and modified from Dev 2020a, b)

Taking cues from the postulation put forth by Christophers (1933), I am of the opinion that there seems to be enough prima facie proof of evidence to propose here in following pages a theory about the cradle of An. stephensi in the Thar Desert in northwest India (see Chap. 10).

20.2

The Principle

Despite a well-recognized geographic expansion to the far-off new regions (Sinka et al. 2020), a terra incognita thus far for the species Anopheles stephensi, the main factor behind its extraterritorial distribution, i.e., anthropically driven or urbanization-based zoogeography, has never been highlighted or focused upon in context with climate change. Urbanization is regarded humongous concentration of humans and habitats, often in multilevel buildings, with enormous load on water intake and, consequently, container-water storage to tide over shortfall in groundwater supply or availability. Thus, diametric or radial mushrooming of new urban centres around the Thar Desert (western India) evolved as a precursor to attraction to An. stephensi for outward peregrinations to explore for establishment in new areas, sometimes eco-physiographically dissimilar to the point of origin. For the first time, therefore, a new adaptive evolution theory implicating direct relationship between the malaria vector, An. stephensi and climate change-impacted urbanization phenomenon is being propounded to explain the possible pathways and genetics of dispersal of the vector species. In this manner, the inextricable relationship between An. stephensi and urbanization also offers a direct evidence to the ongoing dynamic

20.3

The Basis

325

change in the climate, which carries significant ramifications for future understanding of vector distribution and malaria epidemics in the hitherto non-malarious areas of the world.

20.3

The Basis

Earlier, the only other mosquito—also the first ever animal model—which exhibited a direct linkage with climate change or global warming was Wyeomyia smithii, invariably breeding in the pitcher plant, Sarracenia purpurea Linn. (Bradshaw and Holzapfel 2001, 2010). The pitcher-breeding mosquito W. smithii has moved from the eastern America to the central and western parts of North America with the shifting of the plant, S. purpurea—by using the length of day (photoperiodism) to anticipate and prepare for seasonal transitions of major events in its biology. In case of ectotherms like W. smithii, or in our case even An. stephensi, photoperiod ensures successful utility of available events in distant time or space such as thermal environment, food and other ecological conditions which become a reality in open ambience, e.g. swarming, mating, blood-feeding, egg-laying, etc. Anopheles stephensi, a strictly container breeder likewise, utilizes its adaptive prowess to photoperiodism, especially with reference to the Thar Desert’s ‘Tanka’ and ‘Beri’, to migrate, reproduce, develop and prosper numerally to sustain. A few advantageous factors An. stephensi absorbs during the inevitable contained environment of ‘Tanka’ and ‘Beri’ are: (i) While the temperature and humidity remain almost invariant, the mosquito, An. stephensi, appears to sense photoperiodism or the day length and, therefore, provides a highly dependable anticipatory cue for future seasonal conditions (cf. Tyagi and Yadav 1996a, b, c). (ii) Anopheles stephensi, with its three subspecies on the evolutionary pathway, is capable to overwinter or aestivate during extreme ambient temperatures—a clearly specific photoperiodic response based on selection through evolutionary time for the optimal development, migration, reproduction and/or dormancy. (iii) Being contained over long periods of time, An. stephensi inherently follows, via ‘a genetic switch’, the go/no-go response of photoperiodism and is able to regulate optimally all its physiological, developmental or reproductive processes after the completion of the seasonal event under selection pressure. (iv) Being an ectotherm and adapted to spend a good deal of contained lifetime in the ‘Tanka’ or ‘Beri’, the desert specialist species, An. stephensi, has also learnt to fine-tune the actual timing of the seasonal event in a thermal environment (i.e. under thermal stress) that varies from year to year. (v) Anopheles stephensi is able to respond to both total and dynamic photoperiodism. (vi) Chronobiologically, the external environmental cues reset the internal body clock, and, thus, the naturally occurring light is the strongest zeitgeber (i.e. environmental time cues such as sunlight, alarm clocks or social interaction

326

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Anopheles stephensi: The First Vector to Show an. . .

that helps trigger an organism to entrainment to a 24-h cycle) for An. stephensi, which can adopt both circadian (endogenously generated biological rhythm with a period length approximating to 1 day) and circannual (endogenously generated biological rhythm with a period length approximating to 1 year) rhythmicities corresponding with hard periods to keep track of seasonal time, for example, a winter hibernacula, during migration through changed physiography of territorial zones. A major trait of W. smithii by which it can be paralleled with An. stephensi is the common character of ‘container’ breeding. However, unlike W. smithii, the Indian mosquito, An. stephensi, exercises a great diversity in breeding habitats in and around human habitations such as wells, borewells, underground and overhead water tanks, cisterns, roof gutters in factories, barrels, buckets, ornamental tanks, pitchers and vases, besides of course ‘Beri’ and ‘Tanka’ in the Thar Desert (Rao 1984; Tyagi 2002), which give the vector species an additional power to diverge and adapt in the changed climate. Anopheles stephensi finds it convenient to explore new niches and habitats with the growing urbanization where water-storing practice in a variety of containers is spontaneously acquired due to immense pressure on the drinkable groundwater sources. Kerala state in peninsular India presents a glittering example to this rule. Kerala had been the first state in the country to achieve the eradication of malaria as early as 1965. However, the euphoria was short-lived, and the slackening of vector-control activities and the importation of malaria from other states re-introduced the disease in Kerala soon thereafter, and from 1975 onwards malaria once again became a regular illness in the state. Through the early twentieth century Kerala enjoyed a vibrant accumulation of 44 perennial rivers, but after almost a century, by 2001, it began to witness only three live rivers. Thiruvananthapuram, the capital city, located near its southern tip, had likewise plenty of water at the doorstep of the inhabitants in the past, however, by 1980s, it fell gravely short of groundwater so much that, for the first time in Kerala’s history, people began to store water in pots to meet out their daily chores! The opportunistic An. stephensi, which had already intruded Kerala through Kasaragod district in the north, soon found out commensurate environment to breed prolifically in Thiruvananthapuram, not without ushering the first ever malaria outbreak on close heels! Additionally, it is now well documented that An. stephensi has subsequently invaded Lakshadweep ils. (India) in the Arabian sea and the Rameswaram il. (India) and the neighbouring country of Sri Lanka in the Indian Ocean. In all above examples, urbanization with waterstoring habits by people was the single most dominating character common to all.

20.4

20.4

Population, Urbanization, Anthropization and Climate Change in the Thar Desert

327

Population, Urbanization, Anthropization and Climate Change in the Thar Desert

Thar Desert constitutes the eastern end of the great Saharo-Arabian mid-latitude desert belt that owes its existence to the anti-cyclonic, subsiding dry continental air regime (Roy and Pandey 1970). Till recently widely divergent views prevailed regarding the antiquity of the Thar—some making it a recent phenomenon and some as old as the Miocene (Dhir and Singhvi 2012). While Wadia (1960) postulated about post-glacial aridity for Central Asia, including the Thar Desert, Piggot (1950) and several others used the presence of flourishing Harappan and subsequent civilizations within the Thar some 5000 to 2000 years ago as an evidence of a recent origin of the Thar Desert. The mention in the scriptures of a mighty river in the Thar in the Vedic times and the same as a dying river later reinforced this view further. Bryson and Barreis (1967) advocated a more younger age for the Thar by attributing its formation to rainfall prevention by dust in the atmosphere originating from degradation of landscape caused by intense biotic pressure. Whatever the antiquity the Thar Desert appears to be a much recent happening, just like An. stephensi which is likely still evolving with the three subspecies or races. Considering that An. stephensi was born in the Thar Desert, an attempt is made here to demonstrate that population boom in urban centres around it in India, mainland or islands and far off to distant Sri Lanka, the Mesopotamia, Arabian Peninsula and, finally, the Africa continent galvanized the vector species to gravitate into their contained water environment. Demographic annals of yore hint at a very low population of possibly two to five persons per square kilometres and human population influx into the Thar Desert, called Marusthali, started soon after the famous battle between the invader Alexander of Greece and the Indian king, Porus, of Punjab in 327 BC (Dhir 2003). Since then human settlements have made inroads from the less inhospitable eastern margin to the more desert westward. However, right up to the beginning of the twentieth century, the population was thin, with hardly any growth (Dhir 1982; Dhir and Kolarkar 1977). Since 1921 the population doubled in the next 35 years and doubled again in less than three decades. The growth rate was all the time higher than that of the Rajasthan state as a whole or the country (Fig. 20.2). By 2001 the Thar Desert emerged as the most widely populated desert in the world, with a population density of 110 people per km2 (Dhir 2005; Singh 2007). It is to be reminded here that An. stephensi, in which Ross (1897) has noticed primo temporis the spectacular black bodies, the round-shaped oocysts of the malaria parasite, on the outer gut wall, and laboriously discovered an inextricable link between mosquito and malaria parasite, whereby he founded his irrevocable theory that mosquito transmits malaria which ultimately won him the Nobel Prize in 1902, was till the beginning of the twentieth century the only anopheline mosquito in the Thar Desert (Tyagi 2004a, b). Now, if the population growth trend in the Thar Desert is carefully examined, it will become more than clear that the mosquito, An. stephensi, tended to diverge from the penetralium of the Thar first towards the eastern edge of the desert where human settlements sprang up early. While

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Anopheles stephensi: The First Vector to Show an. . .

Fig. 20.2 Human population growth over the years (Census Year 1901 = 100). Note that the arid zone (Thar Desert) has recorded a far greater growth than in the Rajasthan state or India (Source: Tyagi and Baqri 2005)

urbanization in the rural xeric environments was still unheard by the close of the first quarter of the last century, elsewhere in India, including Rajasthan’s non-desertic lands, urbanization phenomenon had already set in as towns and cities, some of them soon to be metamorphosed into metropolises (23) and/or megapolises by the end of the twentieth century (Bombay, Calcutta, Madras and Delhi all of which, except Delhi, were rechristened recently as Mumbai, Kolkata and Chennai). The turning point in this transformation from a majority rural India converting into a dominant urban India came in by the late 1990s when the urban population surpassed the rural population. At present, India has 48 cities with >1 mill. people, 405 cities with 100,000 and 1 million people and 2500 cities with between 10,000 and 100,000 people. Mumbai is the largest city (megapolis) in India with a population of 12,691,836, followed closely by Delhi with 10,927,986 people. Both these megapolises, together with Chennai and Kolkata, are known from the early twentieth century having a An. stephensi-transmitted malaria (Covell 1928; Christophers et al. 1928; Simmons and Upholt 1951; Watts 1999) (Fig. 20.3). The rate and growth of population in India has been phenomenal. The total population of India in 1901 was about 238 million which catapulted to 361 million in 1951 and 843 million in 1991, whereas in 2001 India’s population was 1027 million which rose to 1210 million in 2011. While during 1901–1911 the decadal growth rate was only 5.75%, the same had shot up to 17.64% during 2001–2011. Bigger cities mean huge population, which not only generate ‘heat islands’ in urban centres but also essential water-storing practice due to excessive pressure on groundwater resources and, consequently, shortage in public supply. Thus, the urbanization scenarios set a perfect stage for attracting An. stephensi.

20.5

Urbanization-Driven Climate Change and Effluxes of Anopheles. . .

329

Fig. 20.3 Hot Thar Desert (arid) and semi-arid regions, along with cold desert, with important mountain ranges as barriers in the distribution of Anopheles stephensi from the penetralium in the Thar Desert (red spot) to other parts undergoing swift process of urbanization within India

20.5

Urbanization-Driven Climate Change and Effluxes of Anopheles stephensi from the Thar Desert to In-Country and Extraterritorial Regions

The efflux of Anopheles stephensi from the Thar Desert to several other in-country as well as extraterritorial regions is attributed to the favourable conditions created by rapid social development and urbanization, with inbuilt excessive water storage practices.

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Anopheles stephensi: The First Vector to Show an. . .

Table 20.1 Chronology of in-country and extraterritorial expansion of the desert specialist malaria vector Anopheles stephensi in the post-1950 era Year of entry 1970s

India Mainland Goa

1980s

Kanyakumari

1992

Kochi (Kerala)

Islands

1956 2001 2001

Outside India expansion in countries

Eastern Saudi Arabia Rameswaram il. Lakshadweep ils.

2012 2016 2016

Djibouti Ethiopia Sri Lanka

2019

Sudan

References Sharma and Hamzakoya (2001) Sharma and Hamzakoya (2001) Raveendran et al. (2016) Al Kuriji et al. (2007) B.K. Tyagi (pers. observation) Sharma and Hamzakoya (2001) Faulde et al. (2014) Carter et al. (2018) Dharmasiri et al. (2017) Ahmed et al. (2021)

The Thar Desert’s aridity stretches quite close to Delhi; therefore when Delhi was being transformed into New Delhi by shifting India’s capital from Kolkata in 1911, the mosaic town witnessed a huge expanse of building construction, establishment of industries and, consequently, phenomenal rise in population. It seems, therefore, that An. stephensi first intruded Delhi since the Thar Desert connected with it well. Also any divergence attempt by the mosquito was likely thwarted by the parallelly running Aravalli mountain ranges (Table 20.1). As far as Mumbai (old Bombay, Maharashtra state) is concerned, it can be most commensurably assumed that the vector, An. stephensi¸ might have soon inveigled into the city through Ellichpur (Achalpur) in Amravati (also in Maharashtra state) where it was discovered (Liston 1901), largely because of the sprawling port township with essentially water-storing practices and the rains in plenty. Whatever time lapsed between the cities was possibly due to a natural barrier in the form of Vindhyachal mountain and Satpura mountain ranges which ecologically transact the country into north and south India. To Chennai and Kolkata, the species had likely moved from either Achalpur, Delhi or Mumbai, in that order. It arrived Goa in the 1970s, Kanyakumari in 1980s and lastly, outside the mainland and east of Kerala, the Lakshadweep islands in the Arabian Sea in 2001. Anopheles stephensi is still not recorded from Andaman and Nicobar ils., but in view of the intrusive behaviour of the species, it is safely presumed that it is but a matter of time before the island will make an addition to the growing list of invasion by the vector. Having established deeply in both Kerala and Tamil Nadu, it seems the species has made headways to Rameswaram island township during early 2000s (pers.

20.6

Conclusion

331

observ.), either solely or in association with the species already prospering in these states, taking the advantage of heavy human movement during pilgrimage. The island of Mannar in the Northern Province of Sri Lanka is only 125 km from Rameswaram, and a lot of people’s movement is regularly happening between the two countries, hence a rather belated but sure first time entry into the country in 2016. Soon, however, the vector intruded the neighbouring Jaffna city in 2018 in the pearl island nation, with a genotype consistent with an origin in Tamil Nadu (Surendran et al. 2019). Even though Thar is connected thinly with the Saharo-Arabian deserts, An. stephensi was already present in the historical Mesopotamia (Iraq and Kuwait and parts of Iran, Syria and Turkey) before the construction of Suez Canal in 1869, to connect Mediterranean Sea with the Red Sea. The Suez Canal site was not only malaria-free, but it also entertained no Anopheles species, albeit presence of mosquitoes of the genus Culex and possibly Aedes (Ross 1903). During the past nearly two decades, An. stephensi has invaded several countries in Africa and Arabian Peninsula such as in Saudi Arabia in 1956—first in the Riyadh’s eastern region in 2007 and subsequently in the western region in 2008. After intrusion to the Arabian Peninsula, An. stephensi invaded Djibouti, a developing seaport township in the Horn of Africa loaded with heavy transportation of goods and movement of refugees returning from Oman. Next in line of invasion soon were Ethiopia, Somalia, Sudan, Eritrea etc. Sinka et al. (2020) have worked on global data of prevalence and distribution of An. stephensi and postulated a large number of neighbouring countries and millions of African population reeling under the continuous threat of descendance of the vector in the next few decades.

20.6

Conclusion

There is clear evidence that urbanization affects anopheline species in the environment—diversity, numbers, survival rates, infection rates with P. falciparum and the frequency of biting people, all are influenced. Invasion by An. stephensi in Sri Lanka and Africa during the past one decade, besides a couple of island territories in India, has attracted global attention, and the World Health Organization issued an alert for the future. Mushrooming urbanization with inextricable water-storage practices by the urban population is singularly the most plausible cause of attraction to An. stephensi in all these new areas otherwise terra incognita for the species in past. Africa’s case of An. stephensi intrusion is particularly interesting due to arid environments of the expansive Sahara Desert in the northern African region, which, to some extent, is parallelable to that of the Thar Desert. Therefore, the constantly changing desert physiography (e.g. recently Sahara Desert experienced snowfall after nearly four decades), with mushrooming urban centres with populations there exerting unprecedented pressure on drinking groundwater resources and to sustain cultivating the inseparable water-storing habits, has clearly brought about a change that is commensurate to the breeding of the stubbornly insular breeder, An. stephensi.

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Anopheles stephensi: The First Vector to Show an. . .

Thus, when for the first time, Faulde et al. (2014) reported An. stephensi from Djibouti, in the Horn of Africa, where this species’ occurrence was linked to an unusual streak of urban malaria outbreaks dominated by P. falciparum, first in 2013 and subsequently in 2013, the factor mostly behind invasion by An. stephensi was understood to be the initiation of new structures all over with abundance of container water all around. Positive tests for P. falciparum circumsporozoite antigen in two of six female An. stephensi trapped in homes of malaria patients in March 2013 are evidence that autochthonous urban malaria transmission by An. stephensi has occurred. Anopheles stephensi was confirmed both microscopically and molecularly, the latter by sequencing of the barcode cytochrome c-oxidase I (COI) gene and the rDNA second internal transcribed spacer (ITS2). Taking cognizance of the fact that P. falciparum is prodigiously transmissible by An. stephensi may pose a significant future health threat. Further, An. stephensi is well known for its tolerance of urban habitats which alludes towards increased malaria outbreaks in African cities in the future. Incidentally An. stephensi is not the first malaria vector to invade a new continent. For posterity it is noteworthy here that An. arabiensis, a member of the An. gambiae complex, has much earlier established in the city of Natal, north-eastern Brazil. Both An. stephensi and An. arabiensis, despite being distant geographically, share between them certain remarkable behavioural attributes.

Trans-Border Migration and Malaria in Desert Populations

21.1

21

Introduction

Human movement such as migration, displacement, refuge, military personnel in war or on leave in peace, tourists, etc. has on many times an irrevocable impact on malaria prevalence, the former actually serving as fuel for the pernicious malarial fevers (Pousibet-Puerto et al. 2021; Walz et al. 2019). When humans from non-endemic or less malarious regions such as deserts move to areas endemic for malaria, they are exposed to malaria infections, on one hand, and/or, if already infected in the past, create new antigenic combinations, on the other, that continuously confound the immune systems of the more sessile existing residents of endemic sites, and they complicate measures for the control of malaria (Prothero 2001; Rajagopalan et al. 1984, 1986). Additionally, labourer force at the irrigational development projects, many of which might have hailed from different malariaendemic states, stands a much greater chance to create fundamental malariapromoting environment besides physical, economic and social changes in the mismanaged irrigation development site (Rajagopalan et al. 1984, 1986). In context with deserts, Indira Gandhi Nehar Pariyojana (IGNP) in the Thar Desert in western India is a vibrant example of de novo entry into the arid ecosystem an array of exotic vectors, e.g. Anopheles fluviatilis, and the malaria parasite, Plasmodium falciparum. Transmission potential of malaria, often drug-resistant malaria, from across the international border or the hyperendemic malarious states within the country has been adequately emphasized from time to time (Wangdi et al. 2015; Pousibet-Puerto et al. 2021; Tyagi 2002). While the significance of population movements is recognized, they and other human factors (e.g. distribution and composition of population, social organization and economic activities) have not received attention comparable to that given to malaria parasites and vectors.

# The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_21

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Human Movement in Search of Fodder for Cattle

Changes in agricultural productivity due to changes in climate could provoke migration and might lead to increased urbanization, which results in lower transmission rates (Hay et al. 2005; Keiser et al. 2004). Western Rajasthan with almost entirely covered by the Thar Desert, being a rain-deficient area, can offer fodder for livestock only during monsoon season which is scanty, irregular and erratic. In the event of the failure of monsoon, particularly so during the drought, the situation worsens and the cattle breeders do not find enough pasture lands to graze their livestock. Under these adverse circumstances, the cattle and sheep breeders have developed a definite pattern of migration with their livestock to areas where sufficient grazing ground or pasture is available. These migratory routes are followed year after year by the livestock raisers. They take away their domestic animals from their native places to such distant areas as Madhya Pradesh, Uttar Pradesh, Gujarat, Punjab and Haryana where enough pasture is generally available. Incidentally, all these new areas with pasture are highly endemic to malaria with a high proportion of P. falciparum. Sometimes, the cattle and sheep breeders remain away from their native places for several months or even years and return to their homeland only when favourable conditions return to their homeland for their animals to graze, but more often than not heavily malariated from their sojourn in the malaria-endemic areas. The traditional migration routes for sheep and cattle, together with their owners, are as given below (Fig. 21.1).

21.3

Malaria Transmission across International Borders

Border malaria is a serious issue in many countries engaged in disease elimination. Bracing differentially endemic nations across it, the international border poses specific challenges to policy makers and disease controllers due to its high porosity in many cases. As a consequence, many peoples cross over these borders legally or illegally, in the latter case almost always without any malariological inspection. Since the ecology of areas across the border is contiguously similar, peoples on both sides of the border frequently mix on one account or another (e.g. marriage rituals, marts and or hunting) reinforcing transfer of parasites through the local vectors (Al Zahrani et al. 2018). Nomadic settlers often migrate under the devastating impact of droughts and are vulnerable to fresh malaria infection in the endemic country of their settlement. This pattern of human movement across international borders may complicate achieving malaria elimination in the neighbouring countries which are often at different stages of the control-to-elimination pathway. India is one of those counties at risk from human movement across the Thar Desert’s nearly 1500 km international border bracing with Pakistan, a country overladen with malaria burden. It is noteworthy that India is one of those 34 countries which have declared a time frame for a malaria-free state by 2027 (Wangdi et al. 2015). People living on the international border, sometimes an usually difficult terrain and hard-to-reach communities, are often comparatively impoverished with poor treatment-seeking

21.3

Malaria Transmission across International Borders

335

Fig. 21.1 (a) Human migration with cattle and sheep across the Thar Desert border to other (malaria hyperendemic) states in India and (b) human migration with camel across the desert border to neighbouring non-desert (malaria hyperendemic) districts in the state

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behaviour. Since the marginalized populations have only lower access to health services, they have higher malaria and remain untreated usually. For above reasons surveillance activities for rapid identification of any importation or reintroduction of malaria are also very poor, and there is an urgent need to deploy satellite-based spatial decision support systems and other advanced communication technologies such as mobile phone technology which can be used to capture the movement of people in the border areas and likely sources of malaria importation. Additionally, the governments in the neighbouring countries across the border may undertake joint collaboration to prevent and control malaria transportation by reinforcement of early diagnosis and prompt treatment.

21.3.1 The Saudi-Yemeni Border The malaria problem is serious at the Saudi-Yemeni border with higher rates of transmission intensity on the Yemeni side of the border compared to the Saudi side. For instance, between 2012 and 2014, when a total of 91,676 people were examined for malaria in their blood in the bordering Jazan region, only three infections (0.003%) could be found out which were all imported from Yemen. Yemen exhibited a prevalence rate of 4.6% during a survey in Hajjar Governorate bordering Saudi Arabia, in 2013. In Yemen, between 2008 and 2015, a period of rapid economic development in Jazan and Aseer regions and moderately low rainfall, the incidence kept lower than 2.5 per 100,000 population per year, but a year later in 2016, with a moderately high rainfall, the incidence escalated dramatically to 7.5. Earlier between 1956 and 1979 in Aseer and Jazan regions, three major malaria parasites, viz. P. falciparum (6.4%), P. vivax (1.5%) and P. malariae (0.2%), respectively, were reported. In contrast, in a survey made in two bordering Governorates of Yemen, i.e. Hajjar and Sa’dah, between 1962 and 1977, a higher prevalence of the parasites, i.e. P. falciparum (13.8%) and P. malariae (1.2%), was diagnosed, save for P. vivax (0.8%) which was relatively lower. The scenario by 2020 had entirely changed since of all the cases detected indigenously in Yemen nearly 99% were pure P. falciparum. It is noteworthy that Plasmodium ovale was always wanting in any survey in either country.

21.3.2 The Jordan-Iraq Border Malaria in the northern borders between Jordan and Iraq was mainly transmitted by Anopheles superpictus. By the 1970s the vector mosquito was eliminated and active transmission was interrupted in that region. However, malaria continued to ravish the Red Sea facing areas infested by the deadly An. arabiensis and An. sergentii which sustained transmission. Generally malaria erupted during the Hajj time along the routes followed by pilgrims. Therefore, the health personnel, as early as the 1970s, targeted these households for indoor residual spraying (IRS) using dichlorodiphenyltrichloroethane (DDT) and larviciding all the positive breeding sites. Simultaneously all malaria cases were searched through active surveillance and treated with chloroquine.

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Malaria Transmission across International Borders

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21.3.3 Malaria Status of Countries Bordering India India shares land border with Afghanistan, Bangladesh, Bhutan, China, Myanmar and Pakistan. Currently, Pakistan and Afghanistan are the most populous countries affected by P. vivax malaria (WHO 2016). By 2016, P. vivax was the most prevalent species in the area especially alongside regions bordering the neighbouring Afghanistan, exhibiting same genetic background (Karim et al. 2016). The prevalence of P. vivax in Afghanistan is the highest (95%) among all the bordering countries of India. The WHO (2016) revealed that the prevalence of P. vivax in the other bordering countries of India was highest in Pakistan (81%), China (79%), Nepal (78%), and Bhutan (60%), while its prevalence in Myanmar and Bangladesh was 34 and 7%, respectively. However, P. falciparum was predominant in Bangladesh (93%) followed by Myanmar (66%), Bhutan (40%), Nepal (22%), Pakistan (19%), China (11%) and Afghanistan (5%). These results suggested that the high prevalence of P. falciparum in Bangladesh and Myanmar was likely to contribute to its prevalence (67%) in the northeast region of India. In addition, the high prevalence of P. vivax in Afghanistan, Pakistan, China, Nepal and Bhutan was also likely to contribute to its incidence in the west and north regions of India. Therefore, the cross-country collaboration to control malaria is urgently needed (Park et al. 2018).

21.3.4 Ethiopia and Sudan Both countries suffer from malaria attacks on regular basis along the border. Death and illness from diseases like malaria, leishmaniasis and tuberculosis are excessive, and the areas are remote and hard to access by the health-care delivery facilities in the countries. The spread of malaria disease is exacerbated by frequent population movement. Ethiopia and Sudan joined forces to beat border health hazards (Anon. 2000).

21.3.5 Border Malaria in the Thar Desert In case of the Thar Desert, besides some well-documented man-made means, natural calamities like floods and droughts also play a significant role in enforcing inter-state human migration. In not far distant time, in second half of the twentieth century, the Thar Desert had two major droughts, the first in 1976–1977 and the second in 1987, while two severe floods hailed one each in 1990 and 1994, respectively. Four desert districts, namely Sri Ganganagar, Bikaner, Jaisalmer and Barmer, brace for about 1048 km with the international border along Pakistan, in Sindh and Punjab provinces, on north-western flank of Rajasthan state, while the other nine desert districts touch the boundaries with Gujarat, Haryana and Punjab, besides the non-desert districts in the state. Very little information exists on the issue of border malaria, although the fact remains that border malaria, be it inter-state or

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international, definitely plays an important role in defining the endemicity level of the disease of the Thar Desert (Anonymous 1976). Some of the most vulnerable desert districts are discussed below: 1. Sri Ganganagar District This northernmost desert district borders with Punjab and Haryana states for 190 km of length. During the mid-1970s work of construction of the main Indira Gandhi canal had greatly increased, with the plans to launch the Indira Gandhi Nahar Pariyojana (IGNP) soon. The mega project obviously attracted a vast labour force from near and far states. Malaria prevailed in the settled work force during all years but more in 1974 and 1975 than in 1976. It is comprehensible that P. vivax alone was present in the border population of the two states, while P. falciparum was already represented in Sri Ganganagar unit population for period 1974–1976. The year 1975 experienced an epidemic since slide positivity rate (SPR) shot up to 10.56% from 6.86% in the preceding year, besides nearly four-times increase in the P. falciparum cases. The API for Haryana was significantly high during 1974–1976, being 28.0, 29.1 and 28.0, respectively, which was on an average nearly double to that of the Ganganagar unit (15.0) during the epidemic year of 1975. There had been a greater degree of importation of malaria cases (48) against 23 exported cases in 1975, and three against two exported cases in 1976. The contribution of different states in importing positive cases to Sri Ganganagar during 1975 ranged from 2.08% to 35.41% (Table 21.1; Fig. 21.2). The intensity of transmission within the 16 km border belt area was very high since a total of 340 positive cases, all of P. vivax malarial parasite, were detected from as many as 18 sections of Punjab (31.17%) as against 13 sections of Haryana (68.83%). Reasons accounted for rise in malaria cases, compounded by the migration of infected patients across the border (Table 21.2), included irregular spraying with only DDT 50% wdp, but sometimes also 75% wdp, insufficient supplies of the insecticide, shortage of spray pumps, and lack of fully and long-time operative vehicles. 2. Churu District This north-eastern desert district borders with Haryana state for 72 km of length. Save for the year 1975, when ABER was about 8.2%, ABER was very poor in each 1974 and 1976 being less than 4. The API was appreciably high in 1975, but only 2.3 in 1976 and 1.0 in 1974. Plasmodium falciparum was present in the belt area only in 1975. This clearly indicated that there was an epidemic in 1975, which is further corroborated by the fact that in 1975 the positive cases which were far high by about six- and threefolds from that of 1974 and 1976 in both the belt and Churu unit area (Table 21.2). There appeared to have been a good movement of the malaria positive cases across the border to or from Haryana, Gujarat, Punjab, Uttar Pradesh and Madhya Pradesh since about 80% of the cases had travelled to Haryana in 1975 and 1976. In

1976

1975

Year 1974

Belt/Area/ (State)/ Unit Belt(P) Belt(H) Unit Belt(P) Belt(H) Unit Belt(P) Belt(H) Unit Total 25,927 5275 187,875 33,537 5865 213,450 14,580 2334 73,547

Active 917 632 5653 1306 612 10,805 109 61 2318

Mass 732 429 3863 399 193 5667 2072 – 4253

Active 15,873 3818 148,865 19,626 4346 156,975 7532 1836 53,071

Passive 9322 1028 35,176 13,518 1326 50,807 4976 498 16,223

Positives

Blood slide examined Passive 955 446 7271 928 490 11,672 125 45 3173

Mass 3 – 31 – 1 77 – – 33

Total 1875 1078 12,955 2234 1103 22,554 234 106 5424

Pv 1875 1078 12,866 2234 1103 22,189 234 106 5244

Species Pf – – 88 – – 361 – – 175

M – – 1 – – 4 – – 5

Total 1875 178 12,955 2234 1103 22,554 234 106 5424

ABER 13.7 12.7 12.3 18.1 14.9 13.9 6.8 6.2 4.6

API 10.2 28.0 8.6 12.2 29.1 15.0 1.2 2.8 3.6

Table 21.1 Malariometric data for Sri Ganganagar district along the border during 1974–1976 (P = Punjab, H = Haryana; Unit = refer to the part of the district)

21.3 Malaria Transmission across International Borders 339

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Fig. 21.2 Relative movement of positive cases across the border of Sri Ganganagar district to and from Punjab and Haryana as well as other distant states (Source: Tyagi 2022)

the 16 km border belt along Haryana, a total of 84 cases of P. vivax were detected during 1976 which pointed out towards a high borderline prevalence of malaria. Reasons for rise in malaria cases in the border area were the same as for Sri Ganganagar district. (i). Sikar Districts This district borders with Haryana along its 52 km-long north-eastern boundary. The year 1975 can be singled out as an epidemic year with an appreciably high API (7.9) in the belt area comparable to 9.0 in the Sikar unit area. The main attraction to the labour force was the Khetri copper plant in Sikar from across the border where malaria epidemic broke out in 1975 with a total of 1222 positive cases in 1975. In Sikar, the epidemic had affected 953 villages (population 12,72,574), while in the 16 km belt along the border, 29 villages (population 44,599) were affected. In this border belt a total of 282 positive cases (P. vivax) were detected from as many as ten sections (Table 21.3). It may be highlighted here that about 10,000 people were estimated to have moved across the border between Haryana and Sikar every year. Reasons attributable to rise in cases between 1973 and 1975 included infrequent and irregular rounds of indoor residual insecticide spraying, besides the fact that the Sikar unit was under maintenance phase since 1967. (ii). Barmer and Jaisalmer Districts Of the two desert districts, only Barmer has common border with Gujarat for about 50 km. Together they had a population of 737,775. Of this population Jaisalmer constituted only 6.3%. There was no exportation or importation of positive cases across the border, even though approximately 7684 people had migrated in and out of the desert districts to the Gujarat state. A focal outbreak of malaria was nevertheless identifiable. Predominated by P. vivax, an epidemic in Barmer and Jaisalmer districts was definitely there in 1975 when the positive cases were three to six times more than those in 1974 or even 1976. Interestingly P. falciparum was almost invariably present in the district unit area, but it was present in a very insignificant number in the Gujarat state belt (Table 21.4).

1976

1975

Year 1974

Belt area (State)/ Unit Belt Unit Belt Unit Beit Unit

Active 1315 102,420 2869 123,696 1213 40,819

Passive 37 24,037 32 37,665 4 13,558

Blood slide examined

Mass 134 3977 226 5618 – 546

Total 2386 130,414 3127 167,179 1217 54,923

Active 37 2162 207 12,372 84 3108

Positives Passive – 1625 2 10,574 – 3070

Mass – – – 38 – 4

Total 37 3787 209 22,984 84 6182

Pv 37 2162 206 22,687 84 6165

Species

Table 21.2 Malariometric data on the belt area population in Haryana belt and the Churu unit population

Pf – 1625 3 284 – 14

M – – – 13 – 3

Total 37 3787 209 22,984 84 6162

ABER 3.8 8.6 8.2 11.0 3.4 3.7

API 1.0 2.5 6.3 15.7 2.3 4.2

21.3 Malaria Transmission across International Borders 341

1976

1975

Year 1974

Active 10,672 150,778 14,305 190,100 4757 63,688

Passive 43 12,263 366 30,872 112 11,874

Blood slide examined Mass – 8006 – 11,546 – 1310

Total 10,715 171,047 14,677 232,518 4869 76,872

Active 131 2229 931 1268 255 3158

Positives Passive – 1246 67 7496 27 3422

Mass – 35 2 17 – 5

Total 131 3510 980 8781 282 6585

Pv 130 3462 971 19,843 282 6551

Species PF 1 45 7 329 – 33

M – 3 2 23 – 1

Total 131 3510 980 20,195 282 6585

ABER 8.8 7.6 12.0 9.9 4.0 3.3

API 1.0 1.6 7.9 9.0 2.3 2.9

21

Belt area (State)/ Unit Belt Unit Belt Unit Belt Unit

Table 21.3 Malariometric data on the belt area population in Haryana belt and the Sikar unit population

342 Trans-Border Migration and Malaria in Desert Populations

1976

1975

Year 1974

Belt area (State)/ Unit Belt Unit Belt Unit Belt Unit

Active 19 60,886 332 113,293 48 31,647

Passive – 7357 – 24,549 – 4770

Blood slide examined

1187

Mass – 1568 – 4155

Total 179 84,230 332 141,992 48 37,604

Active – 2035 36 10,017 – 3107

Positives

Passive – 616 – 4409 – 966

Mass – 36 – 26 – 27

Total – 2687 36 14,596 – 4100

Pv – 2570 33 12,755 – 3812

Species

PF – 105 3 1780 – 255

M – 12 TV 61 – 33

Table 21.4 Malariometric data on the belt area population in Gujarat and the desert districts, Barmer and Jaisalmer, in Rajasthan

Total – 2687 36 14,596 – 4100

ABER 4.03 9.2 7.47 18.7 1.1 4.8

API – 3.6 0.8 19.8 – 5.6

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Total lack of spraying in 1973 and partial spraying of DDT in 1974 and 1975, besides difficult desertic terrain and the piecemeal budget, were identified as main reasons for rise in cases.

Malaria Management Including Vector Control in Major Deserts

22.1

22

Introduction

Malaria is a life-threatening disease of public health importance globally. Save for Plasmodium knowlesi, all other four have been reported from the malaria-endemic deserts worldwide, although P. vivax and P. falciparum predominate the scenario (Tyagi 2002). There are about four to five dozens of anopheline species (including complexes of species) occurring in the arid environments, but only half a dozen of them are serious vectors of malaria in the desert ecosystems (e.g. Anopheles arabiensis, An. sergentii, An. Stephensi, etc.). Regarding invasive potential of An. stephensi, the original desert species, the Asian mosquito has emerged in recent decades as the most threatening vector both in urban agglomerations and also, due to its increasing presence, in the rural environments (Ahmed et al. 2021). There are four major means to prevent and/or control infection from malaria, namely: 1. Vaccination in malaria-endemic countries to protect communities from infection. The World Health Organization (WHO) has in late 2021 recommended widespread use of the RTS,S/AS01 (RTS,S) malaria vaccine among children in sub-Saharan Africa and in other regions with moderate to high P. falciparum malaria transmission. The recommendation is based on results from an ongoing pilot programme in Ghana, Kenya and Malawi that has reached more than 800,000 children since 2019. Malaria remains a primary cause of childhood illness and death in sub-Saharan Africa. More than 260,000 African children under the age of 5 die from malaria annually. It is hoped that using this vaccine on top of existing tools will help to prevent malaria from affecting tens of thousands of young lives each year. This vaccine will at some point of time in the future will also be deployed in the malaria-sensitive countries in the Sahara Desert. 2. Early case detection and treatment with antimalarial drugs are life-saving and very effective (Gupta 1961). However, the adaptation of parasites to most of conventional antimalarials has so far limited the effect of these interventions. The # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_22

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emergence of resistance against drugs requires in response a steady stream of new interventions and strategies. Up to the beginning of this millennium, most sub-Saharan African countries have been using chloroquine (CQ) as the first-line antimalarial drug, which had to be replaced with sulphadoxine-pyrimethamine (SP) after resistant parasites had rendered CQ ineffective. Currently the first-line treatment of malaria consists of combination therapy which includes an artemisinin derivative. The current approach appears robust, but history has taught us to be alert and to expect resistance to emerge. There is a pressing need to develop and deploy complimentary strategies. Adding a protective vaccine to the existing control tools for malaria holds great promise in the future. 3. Indoor residual spray (IRS) and long-lasting impregnated bed nets (LLIN) are well-defined vector control tools across the malaria-endemic countries. Unfortunately, many vectors of malaria have developed strategies such as shifting behaviour to exophily and exophagy, to evade their contact with the insecticide sprayed on walls or impregnated in bed nets. Consequently, the need for developing new and effective tools (e.g. genetically modified mosquitoes, Wolbachiaguided vector populations) is becoming increasingly inevitable (Tyagi 2021). Antilarval measures include use of larvicides such as temephos for An. stephensi (and also Aedes aegypti, the vector for Dengue, chikungunya and Zika virus, etc.) in urban ecosystems. This based on the susceptibility levels of vector population against a given larvicide (Bansal and Singh 2001). Although genetic control of malaria through vector control using transgenic or genetically modified mosquito and Wolbachia—the microbial manipulator of arthropod reproduction—is foreseeable in the near future, they are still to be approved for open public use (Stouthamer et al. 1999). Interestingly, in An. stephensi, Wolbachia strain wAlbB displays both perfect maternal transmission and the ability to induce high levels of cytoplasmic incompatibility. Seeding of naturally uninfected An. stephensi populations with infected females repeatedly resulted in Wolbachia invasion of laboratory mosquito populations. 4. Repellents of various different types and formulations (e.g. DEET, DMP, DEPA, etc.) provide safety from hematophagous mosquitoes, including vectors, up to 8 h (Tyagi 2015; Kandasamy 2021). However, development of partial tolerance of Aedes aegypti against DEET has warranted an urgent need to look for some repellent materials from natural resources (Rutledge et al. 1994). Plant-based repellents are particularly preferred due to their favourable cost, availability, storage, effectiveness and transportability.

22.2

22.2

Malaria Control in the Desert

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Malaria Control in the Desert

22.2.1 Sahara and Arab Peninsula Deserts Despite presence of vectors like An. arabiensis and An. sergenti, most countries in the United Arab Emirates (UAE) region as well as the Saharan region have either eliminated or are at the verge of eliminating malaria. Along with the sub-Saharan region, malaria continues to remain a huge public health issue with complex challenges in the Saharan region particularly fringe areas with potential of large epidemics and morbimortality. There is a rising need to investigate escalation of drug and insecticide resistance, in parasites and vectors, respectively. One of the major constraints, however, is low coverage of existing preventive strategies, scarcity of safe and effective vaccines and weakness of public health systems to the generally mobile and difficult to reach populations and communities, notwithstanding the fact that malaria prevalence surveillance, one of the key cornerstones for achieving malaria control and elimination, is the third pillar for moving closer to malaria elimination by assessing the effects of intervention measures and progress in reducing the malaria burden. In most of the malaria-free countries in both the Sahara and Arab Peninsula desert regions, elimination of malaria has been achieved through disciplined and strict antimalarial campaigns involving timely and systematic distribution of antimalarials to the affected persons, subsequent follow-up of the cases and surveillance of their movements, not to mention in the least the ample coverage of human dwellings and cattle sheds by both the indoor residual spraying of an effective insecticide without lapses and, wherever needed, distribution of long-lasting insecticide-impregnated bed nets (LLIN). In certain situations even mosquito repellents were also resorted to. In spite of all this, new tools for monitoring malaria control and elimination are urgently needed to eliminate malaria from a few countries in these two regions of desert.

22.2.2 Malaria Control in the Desert 22.2.2.1 Malaria Control Policy The control policy for malaria in the Thar Desert, or for that matter in the whole of Rajasthan state, is that defined by the National Vector Borne Disease Control Programme (NVBDCP) of the National Anti-Malaria Programme (NAMP). Major modus followed including annihilation of vector mosquitoes through residual insecticide spraying (as in rural areas) or larviciding the breeding sites (as in the cities and towns) and by eliminating the malaria parasites from the community through antimalarials. Though quite many research publications exist on national level, there is absolutely no scientific study in sight on the subject from the Thar Desert, except probably the views and/or recommendations made by Sharma et al. (1995).

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22.2.2.2 Diagnosis and Treatment Surveillance embodying early diagnosis and prompt treatment of malaria patients in the community constitutes the mainstay activity of the Global Malaria Control Strategy (WHO 1993a, b). In India, under the NAMP, the disease surveillance is accomplished through: 1. Active case detection (ACD), i.e. to effect early detection and treatment, regular fever surveys assisted often with mobile malaria clinics are made by specific health and medical personnels to every door. 2. Passive case detection (PCD), i.e. from every patient attending a government health facility, a blood slide is, in principle, taken for subsequent confirmation through microscopy at the primary health centre and/or general hospital. Though blood slide collection through PCD has generally been less than that of the ACD, nonetheless the yield of passive slide collection was higher in terms of detection of positive cases of malaria (Table 22.1). Sharma et al. (1995), however, had cautioned that generally only those patients who had fever presented themselves to the hospital or the health centres, making these patients subjected to PCD a selective population which could not be a true representative of the malaria-related suffering in the community. On the contrary, the active case detection has the advantage of suggesting a magnitude of the problem in the community and thus directly helps to identify focus of infection. Owing to the highly inhospitable climate and difficult terrain of the Thar Desert, both the ACD and PCD have suffered on account of one or another reason but mainly the field staff, particularly the male health workers who were mainly responsible for blood slide collections (Sharma et al. 1995). Like the rest of the state, in the Thar Desert, too, the malaria control programme is assisted by the large network of family health workers such as the auxiliary nurse midwife (ANM) or the multi-purpose worker (MPW) who distribute antimalarial drug, chloroquine, as a presumptive treatment to all fever cases in the community (Brandson et al. 1994; Sharma et al. 1995). In spite of several impressive trials with modern diagnostics like polymerase chain reaction (PCR), indirect fluorescent antibody test (IFA) and the ParaSight™-F and other similar dipstick tests for diagnosis of P. falciparum carried out in different parts of the country, none of these diagnostic methods have ever been put into use in

Table 22.1 Quantum of blood slides collected through PCD and ACD (1995–1998) Passive case detection

Year 1995 1996 1997 1998

Blood slides collected 2,221,213 3,154,062 2,790,478 2,160,642

Active case detection Positive slides found 169,443 211,500 199,323 59,046

Blood slides collected 2,538,593 2,932,610 2,825,584 2,552,799

Positive slides found 67,080 71,207 64,860 14,956

22.2

Malaria Control in the Desert

349

Table 22.2 Basic state data on demography and malaria-related administrative staff Demographic/administrative features Population – Rural population – Urban population No. of regions No. of districts No. of villages No. of towns No. of blocks No. of deputy chief medical and health officers (malaria) No. of assistant malaria officers No. of malaria inspectors No. of sector supervisors No. of senior multi-purpose workers No. of multi-purpose workers No. of squads for spraying

Data/figures 3,41,08,292 2,69,67,871 71,40,421 5 27 35,795 199 237 27 30 214 926 695 3761 978

the Thar Desert mainly due to very high operational costs as well as infeasibility. Therefore, still the standard method to diagnose malaria is the microscopic examination of blood film for malaria parasites. The timely and appropriate treatment is an indispensable component of control activities in malaria. The standard treatment policy followed is that formulated by the NAMP (Sharma 1986a, b; Sharma et al. 1996a, b). So far only P. falciparum resistance to chloroquine has been detected in vivo in the Thar Desert (Khatri 1991; Sharma et al. 1995). The parasite is still susceptible in large areas of the Thar, although resistance up to Riii level has been found in some selective parts of the desert. Sharma et al. (1996a, b) have thrown adequate light on the prevalence of chloroquine-resistant P. falciparum infection during epidemics in Rajasthan state in the mid-1990s. Although personal chemoprophylaxis is discouraged, nevertheless free sale of nearly all types of antimalarial drugs in the local pharmacies and those prescribed by private practitioners is considered important factors in accentuating the risk of development of drug resistance in the malaria parasite. Although the Government of India had set up an Anti-Malaria Organization in Ajmer in Rajasthan state in 1948, a well-planned and organized initiative to control malaria in the Thar Desert could be started only in 1954–1955 with the establishment of one of the two units under the National Malaria Control Programme. The National Malaria Eradication Programme (NMEP), which was launched in 1958, actually got off in Rajasthan in 1959 with the establishment of 17 units, which were later increased first to 26 units under the aegis of Modified Plan of Operation in 1977 and, subsequently, with the addition of Dholpur, to 27 units in 1983. At the 1981 level the administrative/demographic composition of the state staff responsible for control of malaria is given in Table 22.2, with a view to comprehend logistics associated with the control programme at present when, according to Jain

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(1994), Sharma et al. (1995), and, more recently, Anonymous (2002d), several important positions/posts have continued to remain unfilled, though the population of Rajasthan state has since been risen one- and-half times more and as many people are at risk of malaria infection.

22.2.2.3 Vector Control through Insecticides Indoor spraying with residual insecticides has been the main methodology to control adult vector population in the rural areas in the Thar Desert, whereas in the urban setups larviciding the vector breeding sites stayed as the major means of mosquito control. Insecticide spraying in the whole of Rajasthan was initiated on a regular basis in 1989. As an insecticide of choice, DDT had been applied indoors at the rate of 1–2 g (active ingredient) /m2 twice a year, although HCH and deltamethrin have also been employed occasionally for emergent spraying in the border villages of Sri Ganganagar and Jaisalmer districts. In the Thar Desert, insecticide spraying with DDT has been very irregular and far from satisfactory on account of various reasons (Sharma et al. 1995). Recently, Tyagi (1994d) has stressed the need for training of the spray squads and discouraging ad hoc employment of unskilled labourers. As observed by Sharma et al. (1995), untenable and ad hoc policies about spray operations, as come about following promulgation of the Malariogenic Stratification policy, clearly hampered the control programme in the whole of Rajasthan state. They had noted that while, on one hand, only 10.6 of the targeted population was covered in the first round in some districts in the state during the state-wide epidemic year of 1994, the second round scheduled for first August–15th October could not be started in time and, subsequently, the spray operations were undertaken by the district collector and his staff through teachers, revenue staff, school boys and members of the community, in October 1994. Lack of adequate vehicles for transporting insecticides, spray squads and drugs as well as for supervision and monitoring of malaria control activity was considered a major constraint. Application of low doses of insecticides for a long time, coupled with faulty and inadequate coverage of sprayed areas, often leads to development of resistance in the target vector species (Tyagi 1992a). Singh and Bansal (2001) have tested susceptibility of most of conventional insecticides being deployed in various parts of Rajasthan state, including the Thar Desert districts. As an alternative control approach, Tyagi (1994g) and Tyagi et al. (2001a, b), while investigating a focal outbreak of malaria in about a dozen villages in close vicinity of the main Indira Gandhi canal in Jaisalmer district during the mid-1999, used deltamethrin-impregnated bed nets to suppress the vector population in one village, Sadhna. After employment of the impregnated bed nets, the vector population in the village was substantially decreased with the cooperation of the village community which adopted the technology with a high degree of certitude. Similar results were obtained in a ‘dhani’ (hamlet) near Madassar village in Jaisalmer under similar physiographic situations where the per pan-hour density of An. culicifacies was reduced by 50% immediately after employment of the deltamethrinimpregnated bed nets. it was observed that after 90 days of employment of the bed

22.2

Malaria Control in the Desert

351

Table 22.3 Laboratory bioassay with deltamethrin-impregnated bed nets against An. stephensi and An. culicifacies

Species Anopheles stephensi Anopheles culicifacies

No. of females tested every time pooled) 120 120

Mortality (%) in consecutive months following exposure to deltamethrin-impregnated bed nets Month 1st 2nd 3rd 4th 5th 75 72 67 60 60 (62.5) (60.0) (55.8) (50.0) (50.0) 78 64 60 58 54 (65.0) (53.3) (50.0) (48.3) (45.0)

6th 55 (45.8) 56 (46.6)

nets the vector had disappeared from the sampling. Based on the laboratory bioassays and field observations, they also emphasized that the impregnated bed nets stayed effective for 6–7 months at least (Table 22.3). In an attempt to interrupt disease transmission by vector mosquitoes, Tyagi et al. (1997, 1998) and Tyagi (2000) studied repellent properties of Tagetes minuta and several grass species belonging to genus Cymbopogon, of which two species, viz. C. schoenanthus and C. jwarancusa, occur in the Thar Desert region and made attempts to develop certain formulations to repel vector mosquitoes transmitting malaria in the Thar (e.g. An. stephensi). Tyagi and Shahi (2001) discovered that both these species, particularly C. schoenanthus, offered an appreciable amount of repellence against An. stephensi, when their essential oils were developed into certain formulations. In urban areas, malaria control activities are carried out under the Urban Malaria Scheme in six major cities, two of which, Jodhpur and Bikaner, hail from the Thar Desert region while consideration is being given to also include Sri Ganganagar district. Scheme is implemented in the municipal areas of these cities. The vector control is carried out by larviciding the breeding sites with temephos, fenthion malaria oil (M.L.O.), kerosene and Paris green, etc. Save for Jodhpur city, and possibly also Bikaner city, urban malaria is still not a major contributor to the disease burden in the Thar Desert region, although more studies need to be made to understand this phenomenon (Shahi et al. 1996; Tyagi et al. 1999).

22.2.2.4 Biological Control of Mosquitoes The health department has often resorted to using mosquito fish (Gambusia affinis), as well as other varieties, to control vector mosquitoes in large-sized ponds such as those created in quarry mine areas. Unfortunately no scientific records are available to document frequency and quantum of application of the biological agents in vector control in the Thar Desert, although Tyagi (1991c, 1992c, 1994g), following examples by Corbet (1962), has drawn attention towards an effective use of certain odonate species (e.g. Bradinopyga geminata, Crocothemis servilia) for controlling An. stephensi in some breeding sites at least. Verma and Tyagi (1991) found An. stephensi infested with water mites and argued if the ectoparasites could be used as

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Fig. 22.1 Water mites’ infestation of Anopheles subpictus Table 22.4 Suppression of larval population of An. culicifacies by Bacillus thuringiensis var. israelensis (Bti) at the rate of 1 g (in sachets) /m2 in the quarry mine pits on the outskirts of Jodhpur township

Larval instar I II III IV

Pre-Bti release larval density 189 144 88 78

Post-Bti release weekly estimation of larval density (expressed as no. of larvae per ten dips) 1st 2nd 3rd 4th 5th 6th 7th 8th week week week week week week week week 160 50 0 0 0 0 11 47 110 66 2 0 0 0 1 12 33 23 5 0 0 0 0 4 45 11 2 0 0 0 5 13

control agents. Such water mites may parasitize a large number of mosquito vectors of different diseases (Fig. 22.1). Tyagi and Yadav (pers. comm.) have successfully employed Bacillus thuringiensis var. israelensis (Bti) at the rate of 1 g (in sachets) /m2 in both quarry mine pits and the weeded pools near Indira Gandhi canal breeding An. culicifacies. They found that the Bti was particularly effective against larval population in the quarry mine areas and totally wiped off the breeding for nearly 6 weeks, although the formulation became fully active slowly and only after nearly two weeks of application (Table 22.4).

22.3

Research on Phytochemicals as Repellents against Anopheles stephensi from the Thar Desert

Thar Desert though deficient in quantum and diversity of plant species, yet several of these carry enormous biomedicinal and insecticidal properties (Bhandari 1978; Tyagi 2016). Essential oil of Cymbopogon schoenanthus (L.) Spreng. (Family

22.3

Research on Phytochemicals as Repellents against Anopheles. . .

353

Table 22.5 Repellent effect of Tagetes minuta on the landing of three major vector species (1. An. stephensi, 2. Cx. quinquefasciatus and 3. Ae. aegypti)

Time period (in h) 1h 2h 6h 8h

% L A N D I N G

Test group Vector species 1 2 3 1 4 4 4 2 12 11 15 9 25 32 25

Average landing ( ± SD) 3.0 ± 1.73 6.0 ± 5.29 11.7 ± 3.06 27.3 ± 4.04

Control group Vector species 1 2 3 67 87 60 71 97 36 81 95 36 82 73 37

Average landing ( ± SD) 71.3 ± 14.01 68.0 ± 30.61 70.7 ± 30.83 64.0 ± 23.81

80 70 60 50 40 30 20 10 0 2 hr

4 hr An. stephensi

6 hr Ae. aegyp

8 hr Cx. quinquefasciatus

Time (in hours) Fig. 22.2 Percent landing of An. stephensi, Aedes aegypti and Cx. quinquefasciatus on volunteer (B.K. Tyagi) when tested for repellence efficacy of T. minuta (Source: Tyagi et al. 1998)

Poaceae), growing wildly in Jaisalmer, was studied for its chemical properties (Tyagi 2000; Shahi et al. 2000). The essential oil is rich in terpenoids up to 0.8% (v/w; fr. Wt. basis), with major chemical constituents belonging to volatile semiochemicals such as sesquiterpene oxygenated compounds (50%), sesquiterpene hydrocarbons (17%) and limonene (20%). Most of the compounds are abundantly used as odourants in perfumeries. A common plant like Tagetes minuta (Family Compositae), growing abundantly in the Thar Desert, too, was evaluated for its efficacy as a repellent against An. stephensi, besides Culex quinquefasciatus and Ae. aegypti, in the Thar Desert (Tyagi et al. 1997). Among the three vector mosquito species evaluated, the malaria vector, An stephensi, was repelled maximally by the phytochemicals of the plant (Table 22.5; Fig. 22.2). Tagetes minuta essential oil was highly effective (94.4%) on An. stephensi for 4 hours but lost 50% effect by the tenth hour of exposure. When essential oils of four species and two hybrid varieties of Cymbopogon grasses were evaluated for their repellent properties against the major vector mosquitoes, namely, Anopheles stephensi, Culex quinquefasciatus and Aedes aegypti, sampled from Jodhpur in the Thar Desert, both in laboratory and field

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% Landing

commutatus

(

mar nii

) An. stephensi

pendulus

nardus

CKP-25

Cymbopogon spp. ( ) Cx. quinquefasciatus (

Jamrosa

) Ae. aegyp

Fig. 22.3 Percentage landings of the three major vector mosquitoes against the six Cymbopogon essential oils in the laboratory evaluation (Source: Tyagi et al. 1998)

observations exhibited promising results against the malaria vector, in particular. The magnitude of repellency in the Cymbopogon essential oils was found to be of moderate to high order. All grass species protected completely from mosquito bites for 4 hrs, whereas C. nardus provided protection for as much as 8–10 hrs overnight. When the landing in the test alone was considered, maximum protection was recorded against the group of CKP25 (40.4%), C. martinii (41.9%) and C. nardus (43.9%), followed by another group of Jamrosa (45.5%), C. commutatus (45.9%) and C. pendulus (47%) (Table 22.2). This was amply substantiated in another evaluation when landings of vector species were compared with those in the control (Fig. 22.3). By and large An. stephensi was easily repelled, particularly by C. nardus, CKP25 and C. commutatus.

22.4

Role of Community and Future Scenario of Malaria Control in the Thar Desert

Community-based antimalaria interventions depend on the ability of the operating agency to overcome cultural barriers and to institutionalize new practices within the village environment. Obstacles deriving from politics and a sense of personal ownership and control may prove insuperable.

Inventions, Innovations and Discoveries in Malaria in Desert Environments

23.1

23

Introduction

It is an irony that, for a vector-borne disease like malaria which is inseparably associated with water, the cradle for the malaria parasite’s discovery had to be but a desert country, Algeria, then a French territory, in the Sahara Desert. Thus, the first ever human malaria parasite, Plasmodium malariae (which was later confirmed to be P. falciparum, though certain stages of P. malariae also coexisted), was shown to the world by a French physician, Dr. Charles Louis Alphonse Laveran, in 1880. Yet again, more than a century later, the same African nation was to be declared free from the clutches of malaria; in 2019 the World Health Organization certified Algeria as one of the 38 malaria-free countries. The danger, however, has not completely waded away, and the risk of malaria contraction continues to loom large on many African countries largely due to the fact that both the major desert vectors, viz. An. arabiensis and An. Sergentii, still exist, besides the deadliest An. gambiae in desert-fringe areas. This threat has been further escalated by an unsolicited and unwelcome entry in to some of the north-eastern African nations in recent years. Under such stressful scenarios of malaria prevalence in the deserts of Arabian Peninsula, Middle East/Central Asia/ West Asia and the Great Indian Thar Desert, a streak of fascinating discoveries, inventions or innovations sprang up naturally, some of which are elicited below.

23.2

Discovery of the First Human Malaria Parasite

Dr. Charles Louis Alphonse Laveran was a French military physician and an expert in anatomic pathology as well as a prolific scientist writer, having authored a famous ‘Treatise on Military Diseases and Epidemics’ and 62 other scientific communications. Upon his transfer to Algeria, then a French territory, he found most of the military soldiers suffering by the lethal malarial fevers which also affected army installations. A thorough, well-read and systematic in approach, he # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_23

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excellently dealt with histologic description of cerebral malaria in his regular and copious admission of patients—prompting him to focus on striking at the root cause of the causal agent of the deadening disease. Laveran had no information either about the protozoan (protozoa are microorganisms that are single-celled, with a well-defined nucleus, and without cell walls), parasite or the mosquito vector (which was later pinned down in 1897 by Dr. Ronald Ross, a British army doctor working in India and for the first time demonstrated the role of mosquito, an Anopheles, in transmitting the malaria parasite to man) behind the malarial infection, and the more common hypothesis about the malaria pathology then in vogue was the presence of a bacterium due largely to the influence by several discoveries of Louis Pasteur which alluded that most infectious diseases are caused by microbial germs (his ‘germ theory’). Laveran was also influenced by the Italian hypothesis that malaria emerged from the marshes (Laveran 1884). Since malaria was rampant among soldiers, his mind was always occupied by the thought of the disease. As a careful pathologist he developed a keen eye even for the mildest change in his slides prepared from patients’ blood for examination in routine. With a phlebotomist’s precision, he collected all information on lesions in organs and in blood wherein he found a constant presence of granules of black pigment in the blood, albeit at very different frequencies. Laveran conclusively associated these pigmented granules, having origin in the blood, with malaria. Subsequently, he soon discovered ‘crescents’—a very specific stage in biology of the parasite pointing towards the male and female gametes of P. falciparum. On 6 November 1880, however, while examining the blood of a patient who had been febrile for 15 days, he saw for the first time in the world the phenomenon of ‘exflagellation’ in a male gametocyte, wherein on the edges of a pigmented spherical body filiform elements move with great vivacity, displacing the neighbouring red blood cells. The enchanting phenomenon of motility of these elements immediately convinced Laveran that he had discovered the agent causing malaria and that it was a protozoan parasite and not a bacterium that was all along doctrine behind disease. Laveran quickly dispatched two manuscripts to the Academy of Medicine, in November and December 1880, respectively, on this ‘New Parasite Found in the Blood of Several Patients Suffering from Marsh Fever’ (Laveran 1880). To his utter dismay and disappointment there were hardly any established scientists who came forward and appreciated his truly path-breaking and epochal research. In fact he was squarely repudiated for his premature publication. The history of science is witness that after a long gap of 27 years Dr. Laveran was to be awarded with the most lucrative Nobel Prize 1907, in the field of Medicine and Physiology. Ironically Laveran’s name was nominated by none other than Dr. Ronald Ross (winner of the Nobel Prize 1902, for his discovery of malaria-mosquito relationship) who had himself grown learning malaria under the shadow of Laveran’s discovery!

23.4

23.3

Discovery of ‘Tanka’ and ‘Beri’ as the Main Breeding Habitats. . .

357

Discovery of Entry of Anopheles stephensi in Africa’s Sahara Desert

Anopheles stephensi Liston 1901 is a major malaria vector in South Asia and the Middle East, including the Arabian Peninsula (Sinka et al. 2011), and is known to transmit both the major malaria parasite species Plasmodium falciparum and P. vivax (Korgaonkara et al. 2012; Thomas et al. 2017). Originated probably in the Great Indian Thar Desert, the South Asian vector Anopheles stephensi was for the first time discovered in Djibouti in the Horn of Africa in 2013 (Faulde et al. 2014). Later, in 2016, it was found in Kebri Dehar (Somali region), Ethiopia, and raised concerns about the impact on malaria transmission in the country and the rest of the Horn of Africa. Seyfarth et al. (2019) confirmed the persistence of the invasive alien species (IAS) in several parts of the Horn of Africa. Since in field An. stephensi may confuse with An. arabiensis, the validity of taxonomic status of the species was checked by molecular markers which settled the issue that it was An. stephensi in Djibouti.

23.4

Discovery of ‘Tanka’ and ‘Beri’ as the Main Breeding Habitats for Anopheles stephensi in the Thar Desert

‘Tanka’ and ‘Beri’ originated in India’s Thar Desert several hundred years ago as the two main man-made engineering feats, to store and conserve water for long periods of time ranging from months to years for meeting essential and vital livelihood needs, on one hand, and tide over water-deficient non-rainy periods, on the other (Anon. 2003; Mishra 2003). Both these water-storing facilities are built underground. The beris are well-like semi-natural structures built in multitude in the concavity of a seasonal pond at the periphery of the village. Underneath sometimes some beris may merge together to form a bigger tank. Beris are always charged naturally with the once-in several years rainwater. All the rainwater in the catchment area of the dried pond gushes towards the pond with a natural gradient and fills the beris. Contrary to it, tankas are entirely man-designed underground reservoir either in solitary (when built with stone and cement inside dwelling area) or multitude (when built, with partial assistance with stone and cement, in series outside the village). Tankas are charged up both naturally through rainwater and man-fetched water on camelback or camel cart from far off areas. Both ‘Beri’ and ‘Tanka’ are essential parts of desert life in the Thar Desert. Although Beris are specific to the Thar Desert so far, Tankas, notwithstanding abundance in the Thar Desert region of Rajasthan, India, certainly exist in.

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Invention of a ‘Tanka Lid’

During early 1998, inspired by his extensive malariological explorations of the ‘tanka’, the major source of breeding of malaria vector Anopheles stephensi, in Sri Ganganagar district, north-western Thar Desert, between 1988 and 1990 (Tyagi and Verma 1991), Dr. B.K. Tyagi, while heading as the Scientist ‘F’ and Officer-inCharge of Desert Medicine Research Centre (Indian Council of Medical Research), designed and fabricated as well as assembled an ‘Anopheles stephensi breeding preventer’ (Fig. 23.1). It was also limitedly tested in field to ascertain its foolproof modus operandi to prevent the vector from entry or those inside from exit. In 2000 when a malaria outbreak struck in desert districts, he had suddenly received a telephone call from the Jaisalmer district health authorities to help control mosquito breeding in Tanka (cf. Tyagi 1995a, b). Dr. Tyagi immediately informed Mr. Rajat Mishra, District Collector, Jaisalmer, of his invention and sent them a copy of the drawings of the prototype so that they could replicate the same and get it deployed en masse in desert villages. Much later, first in 2014, during the Scientific Advisory Committee meeting of the ICMR-National Institute of Malaria Research, Delhi, and second time, during the 12th Joint Annual Conference of Indian Society for Malaria and Other Communicable Diseases and Indian Association of Epidemiologists, held on 1–3 September 2017 in Armed Forces Medical College, Pune, Dr. A.C. Dhariwal, the then Director of National Vector Borne Diseases Control, conversed with Dr. Tyagi about the unfailing utility of the ‘Tanka Lid’ in preventing vector, Anopheles stephensi, breeding in the thousands of Tanka in the Thar Desert villages, and praised the invention with much aplomb. He asserted that the invention has certainly resulted in the overall reduction of malaria cases in Jaisalmer district. This most appropriate compliment—a summa cum laude—apparently delighted Dr. B.K. Tyagi more than any award for having done something useful to the Society! Singh and Puri (1951) have emphasized on control of vector mosquitoes by making modifications in certain breeding sites with the aid of engineering. Recently, Singh et al. (2021a, b) have studied the utility of a ‘Tanka Lid’ in two villages, namely, Ajasar (intervention) and Tota (control), with similar ecological features, for the control of An. stephensi in ‘Tanka’ (97.8%).

23.6

Invention of a Mechanical Mosquito Sampler (Tyagi Sampler)

Anopheles stephensi, the original and major malaria vector mosquito in the Thar Desert, specializes to breed in ‘Tanka’ and ‘Beri’, the underground deep water reservoirs in the arid environments of the Thar, on one hand, and relatively high anthropophily and anthropophagy, i.e. resting and feeding indoors in human dwellings, on the other. Keeping these behavioural attributes of the vector in mind, Tyagi (1993) indigenously developed a mechanical mosquito sampler and

23.6

Invention of a Mechanical Mosquito Sampler (Tyagi Sampler)

359

Fig. 23.1 A prototype design of the ‘Tanka Lid’ (B.K. Tyagi 2020): various components of the ‘Tanka Lid’ (Source: Dr. B.K. Tyagi, personal archive)

tested in various different habitats for sampling resting adults of An. stephensi and other mosquitoes (Fig. 23.2). This mechanical mosquito sampler was specifically developed to sample mosquitoes in the arid environments where it was >2.5 times superior to the conventional mouth-operated aspirator. This is portable, non-hazardous, economical

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Fig. 23.2 A mechanical mosquito sampler developed by B.K. Tyagi in the Thar Desert (Source: Dr. B.K. Tyagi archive)

(Rs. 625.00 or US$ 31.25, at 1992 exchange level, per unit) and highly feasible in conducting field sampling. It is also efficient, durable and reliable for data mining and samples’ physiological fitness. This invention of mechanical mosquito sampler was awarded an Indian Patent (No. 191635) in 2005.

23.7

Coining a New Classification System of the Thar Desert Based on the Distribution of Malaria Vectors (Anopheles stephensi and An. culicifacies)

Thar Desert’s malariological history is documented since 1975, although Najera et al. (1998) have postulated of a far older records due to a nationwide epidemic in 1908. Epidemics in those times occurred in areas falling under the Luni river basin, i.e. Barmer, Pali, Jalor and a part of Jodhpur, which being low-lying were floodprone during erratic heavy monsoon and were not yet accessible by the network of distributaries under Indira Gandhi Nehar Pariyojana (IGNP). Following the operation of IGNP in the 1950s, the whole physiography, along with human settlement, groundwater level, agriculture practices and surface water availability, has changed a great deal favouring breeding of not only the desert mosquito, An. stephensi, but also the new entrants like An. culicifacies and even An. fluviatilis, all of which have a propensity for transmitting P. falciparum. The IGNP command area became the epicentre for all epidemics, save for the 1990 epidemic which had an epicentre in Barmer district (Tyagi 2002). On record at least 13 outbreaks are countable till 2002. Many of these outbreaks were generally focal in nature covering often parts of a district or two, save for those which occurred in 1990, 1992 and 1994. Inter alia some of the epidemics particularly those of 1983–1985, 1990, 1992–1995, 1996 and 1999–2002, all of which were characterized with a high proportion of P. falciparum (40–80%), appeared to have a strong correlation with the progression of the IGNP irrigation activities. It is to be noted here that proportion

23.8

Hypothesis on the Cradle of Anopheles stephensi in the Thar Desert

361

of P. falciparum significantly grew after 1977, even though there was an appreciable decline in overall malaria cases. Ironically, rise in annual parasite incidence and percentage of P. falciparum in Jaisalmer, and to some extent in Jodhpur, since the early 1990s, clearly coincided with the period of increase in volume of canalized irrigation, implying that a likely outbreak could be professed in the near future. Interestingly P. falciparum-dominated malaria outbreaks had struck Jaisalmer annually since 1992, especially two periods of 1994–1996 and 1999–2002. If all the above referred chronological features of progression of epidemics and distribution of two major vector species, An. stephensi and An. Culicifacies, since 1983 are taken into consideration then it becomes more than clear that P. falciparum-dominated malaria epidemics have spread from the northernmost Sri Ganganagar district to the western and southern districts in the interior of the Thar Desert, more or less along the course of the Indira Gandhi canal (Tyagi et al. 1995; Tyagi 2002). A malariabased classification of the Thar region based on distributional patterns of the malaria vector species, An. stephensi and An. culicifacies, as well as the corresponding distribution of malaria parasites, P. falciparum and P. vivax, is explained as follows: 1. The mixed An. Culicifacies–An. stephensi area: Being under the IGNP command area, this is a canalized irrigation-rich area, covering only 11% of the entire Thar Desert in Rajasthan that spans over Jaisalmer northwards including also the Sri Ganganagar and Hanumangarh districts as well as parts of Jodhpur and Bikaner constituting upper reaches of the ‘marusthali’ desert. Anopheles culicifacies and An. stephensi jointly dominate the area, the former being in abundance. The area has been experiencing annual epidemics with a high proportion of P. falciparum cases. 2. The An. stephensi area: Falling under IGNP non-command area, this area comprises arid environment in a true sense and occupies 78% of the Thar Desert covering largely the districts of Churu, Jhunjunu, Nagaur, parts of Bikaner, Jaisalmer and Jodhpur and Sikar. The desert specialist An. stephensi dominates this area where P. vivax-dominated malaria occurs at a low intensity. 3. The An. culicifacies area: This area (including Barmer, Pali and Jalor districts) is presently referred to as a non-IGNP area due to non-extension of canal water, occupies 11% of the Thar Desert and largely falls within the flood-prone Luni river basin. Being flood-prone area, it is An. culicifacies which is circumstantially numero uno in the region. It is responsible for high malaria transmission following heavy monsoonal rains in the Aravalli mountain catchment of the Luni river.

23.8

Hypothesis on the Cradle of Anopheles stephensi in the Thar Desert

Hypothesis of Tyagi (this work) alluding to the cradle of Anopheles stephensi and its chorogeography is propounded in this book, albeit certain limitations, with a view to comprehend their implications in future malaria elimination at a global front.

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Discovery of the Phenomenon of ‘Self-Immobilization’ in Anopheles stephensi

The phenomenon of ‘self-immobilization’ or thanatosis as a defence mechanism has been observed in many different kinds of animals (Edmunds 1974; Humphreys and Ruxton 2018), but it was Tyagi (1994) who for the first time discovered this phenomenon in a mosquito, Anopheles stephensi. Thanatosis or self-immobilization (death feigning) is a state that in some respects resembles shock and is characterized by cessation of all voluntary activity and usually by assumption of a posture suggestive of death and occurs in various insects when disturbed (tonic immobility, TI). A fascinating anti-predator strategy adopted by larvae of An. stephensi, the phenomenon has great evolutionary implications. Anti-predatory defences are crucial to many aspects of behavioural ecology and, thus, are truly path-breaking in mosquito science.

23.10 Hypothesis on Anopheles stephensi: A Sibling Species Complex For nearly a century the mosquito, Anopheles stephensi, has been regarded to comprise three subspecies or races: the ‘Type’ form, the ‘Intermediate’ form, and the ‘mysorensis’ form. Tyagi et al. (1991) hypothesized a possible sibling species complex within the mosquito. More recently, Firooziyan et al. (2018) speculated with a better evidence based on odourant binding protein 1 intron 1 sequence about the possibility for a species complex under Anopheles stephensi.

23.11 Discovery of Cerebral Malaria Caused by Plasmodium vivax in Adults Organ dysfunction characteristic of Plasmodium falciparum malaria is unusual in P. vivax infections. Cerebral malaria is a diffuse encephalopathy associated with seizures and status epilepticus which can occur in up to one-third of patients with severe malaria, particularly that caused by P. falciparum. Cerebral malaria is usually secondary to P. falciparum infection. However, there are infrequent reports of cerebral malaria associated with P. vivax infection. As regards an arid environment, Kochar et al. (1998a, b, c, 2005, 2009, 2012) discovered and demonstrated the phenomenon in a desert population for the first time that P. vivax infection can also present as cerebral malaria. Clinical data provided by them indicated that P. vivax could cause both sequestration-related and nonsequestration-related complications of severe malaria, all of which are commonly associated with P. falciparum infections (Sarkar and Bhattacharya 2008).

23.12

New Theory on Epidemics in the Thar Desert

363

23.12 New Theory on Epidemics in the Thar Desert Tyagi (1995a, b, 1997a, b, 2002, 2020) interpreted a new ‘Vector’ theory on malaria epidemics in the Great Indian Thar Desert and questioned the validity of the Boumavan der Kaay’s El Nino Southern Oscillation (ENSO) theory as an early warning system for future epidemics.

Future Implications of Desert Malaria in Global Elimination Campaign

24.1

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Introduction

Deserts, covering nearly 33% of the earth’s land area (approximately 33.7 million square kilometres) and inhabited by over 500 million people, are found in every continent and are, therefore, truly global in representation. These are located on both sides of the equator in the northern and the southern hemisphere (Goudie and Wilkinson 1977). Deserts such as Saharan and Chilean-Peruvian deserts have hyperaridity, followed by the Arabian, East African, Gobi, Australian and South African Deserts, whereas Thar and North American deserts have lower aridity. Both cold and hot deserts have arid environments with varying degrees of aridity index. A desert is a barren area of landscape where little precipitation occurs and, consequently, living conditions are hostile for plant and animal life which though less diverse are, nevertheless, unique and rich in rare and endemic species despite being often subject to vulnerability to extinction and environmental degradation (Thornthwaite 1948; Louw and Seely, 1982; UNEP 2002; FAO 2019; Sher et al. 2004; Ezcurra et al. 2006). The scanty, erratic and variable precipitation/rainfall is the basis of chronic shortage of available moisture/water for plants/animals resulting from an imbalance between precipitation and evapotranspiration. This situation is exacerbated by considerable variability in the timing of rainfall, influenced often by the El Nino and La Nina phenomena in the Pacific Ocean, low atmospheric humidity, high daytime temperatures and winds such as that in case of the Thar Desert (Bouma and van der Kaay 1994, 1995). The Thar Desert environment is so dry that it supports only extremely sparse vegetation; trees are usually absent, and, under normal climatic conditions, shrubs or herbaceous plants provide only very incomplete ground cover such as the ‘Khejri’ tree (Prosopis cineraria) in the vast expanse of the desert. A hot desert and its boundaries are varyingly defined either climatologically in context with arid and hyperarid areas or biologically as the ecoregions wherein plants and animals are adapted to optimally survive in arid environments or physiologically where exist humongous extensions of bare and contiguous soil with

# The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_24

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Fig. 24.1 The desert biome defined by combined criteria, i.e. climatological, biological and physiological (the intensity of the red colour on the map indicates congruence in the three criteria: areas in intense red correspond to regions where the three criteria coincide, areas in intermediate red highlight regions where two criteria coincide and areas in pale red show regions where only one criterion operates) (Source: Ezcurra et al. 2006)

scarcely vegetated cover. Overlaying the areas defined by each of the three criteria yields a composite definition of global deserts (Fig. 24.1). A desert is, as a rule, thinly populated in its voluminous sandy and arid environments. In contrast, margins of the desert, some of which include several of the most endangered terrestrial ecoregions of the world, are faced with higher pressures from human activities such as housing, tourism, transportation and agriculture. Apparently, barren-looking deserts are, in fact, complex arrangements of diverse and fragile assemblages of species of flora and fauna. Malaria is mostly local and focal in the desert, save for the desert margins at times. Mosquito vectors are fewer in number and low in abundance. They breed in intra- or extradomiciliary available ‘Tanka’ and ‘Beri’, the typical breeding sites of Anopheles stephensi in the Thar Desert, or a variety of containers, puddles and other surface, fresh or even turbid, water sources such as those of An. arabiensis in the African Sahara desert— both in rural and urban environments.

24.2

Anthropization and Climate Change: The Major Triggers for Malaria Exacerbation in the Desert

In as far as the world’s malariated deserts are concerned, it is singularly the human intervention or anthropization tipped by changes in the climate and environment which is regarded as the main reason behind malaria exacerbation in the otherwise placid deserts. The Thar Desert in northwestern India has established itself as a model to understand how canalized irrigation water drawn from outside into the deserts, if not properly managed, could transform the nonmalarial arid environments

24.2

Anthropization and Climate Change: The Major Triggers for. . .

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Fig. 24.2 Diagrammatic representation of locations of the three ecotypes of malaria related to desert and the intensity of affecting malaria scenario at the periphery or in neighbourhood of the desert (Note: Fringe malaria tend to affect the approximating areas in non-desert region more intensely, quickly and widespread; the total impact could be escalated if joined by other ecotypes of malaria)

in the highly fulminant, often P. falciparum-dominated, malariated ecosystem (Tyagi 1994a, b, 1995a, b, 1996a, b, c, d, e, f, g, 2002, 2003a, b, 2020; Tyagi et al. 1995; Tyagi and Chaudhary 1997). This shift was attributable, more than anything, to the drastic changes in the environment of the Thar Desert (Sikka and Kulshrestha 2001). By nature of environment, as defined above, deserts are not the places where either the mosquitoes or malaria parasites should generally find it conducive to either sustain or breed. Yet, in the deserts like Sahara, Arabian Peninsula, the Middle East/Central and West Asia and the Thar, both malaria and their vectors thrive unabatedly, posing at the same time a discernible threat to the neighbouring areas where the antimalaria campaign was being successfully implemented (Tyagi 1995a, b) (Fig. 24.2). The inter-relationship between climate, weather and human health under the impact of malaria is quite intricate to comprehend (Bouma et al. 1994a, b). It is now realized the world over that climatic changes across timescales influence ecological systems through direct and indirect events, in turn affecting disease conditions. Temperature and relative humidity, which are influenced by rainfall pattern, are important determinants to the biology of malaria vectors. Therefore, to understand the effect of variability in temperature on the development of diseasetransmitting mosquitoes, vector transmission potential and development of parasite extrinsically in the intermediate host body of mosquito, Fig. 24.3 is referable. Economically and politically unstable populations are most vulnerable under extremes of climatic variabilities due to their inability to adapt or respond adequately and rapidly to counteract the devastating outcomes during malaria epidemics. Drastic ecological changes in non-immune or less-immune population-inhabited ecosystems may often prove to be a certain major determinant of malaria epidemics in a vulnerable area like the Sahara and the Thar Desert. In other words, whenever a disturbance takes place in previously existing equilibrium of the ecological system comprising human, parasite and vector populations in a particular environment niche, an epidemic is imminent. After the epidemic had occurred, the ecological equilibrium may or may not revert or even may give way to a new equilibrium with

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Fig. 24.3 Effect of variability in temperature on the development of a mosquito and the development of malaria parasites in its body

or without passing through a period of vicissitude, depending on resilience of the ecosystem. The stability of equilibrium can be gauged simply by a combined comprehension of the epidemiological background and results of a current study on the situation of the epidemic-hit areas. As far as the Thar Desert is concerned, the possible factors and pathways for evolution of epidemics have already been explained in the foregoing pages, and presently there is an urgent need to comprehend the wide spectrum of climatic oscillations triggering off onset of the epidemics and the tools to contain these before they result into heavy morbimortality.

24.3

Excessive Rainfall and Malaria Epidemics in the Thar Desert

The spread of malaria may be influenced by a large number of factors of which increased rainfall in unaccustomed areas as the Thar Desert region could also increase malaria incidence (Gupta 1996). According to Akhtar and McMichael (1996), there have been 5 flood years in the Thar Desert during 1908, 1917, 1944, 1990 and 1994, when the summer monsoon exceeded 500 mm. The last two of these flood years coincided with the epidemics of malaria in the region. The rainfall in western Rajasthan in the year after El Nino event was reported to be about 40% higher than in El Nino year and 50% higher in the La Nina years (the opposite phase of ENSO phenomenon). On examination of time series data for 1982–1994, the relation between total rainfall, number of rainy days and annual malaria rate as well as the percentage of total cases due to P. falciparum for the partly irrigated Jodhpur

24.4

Climate Variability: Impact of El Nino Southern Oscillation on. . .

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district, they discovered a strong correlation (r = +0.72) between rainfall and malaria incidence, particularly between number of rainy days and malaria incidence (r = +0.68). In western Rajasthan during 1973–1984, the correlation between annual rainfall and the annual malaria incidence was approximated 0.8. It was suggested that variations in the annual rainfall cast a strong influence on malaria outbreaks in the Thar Desert, which no longer remains a low-risk zone for malaria epidemics. Contemporarily, Gupta (1996) had arrived at a similar conclusion after examining various parameters like annual incidence of malaria particularly falciparum malaria, annual and monthly rainfall and agriculture in Rajasthan, between 1980 and 1994. The overall malaria incidence showed a moderate correlation (r = 0.48) with annual rainfall, while the incidence of P. falciparum showed a strong correlation (r = 0.61). It was stressed that higher and prolonged rainfall posed a greater risk in initiating malaria epidemics, particularly dominated by falciparum malaria.

24.4

Climate Variability: Impact of El Nino Southern Oscillation on Malaria Conflagration

Climatic changes in timescales are of different kinds and intensities, and the vectorborne diseases particularly malaria are influenced in their occurrence and frequencies (Tyagi 2001a, b). The El Nino seasonal variations occupy a special place in the global weather formation, even though the ENSO (El Nino Southern Oscillation) represents one of several natural variabilities. The ENSO, known for over 50 years, is an unstable atmospheric system in the Pacific occurring roughly at an interval of 5 years. Its influence on global climate is second only to that of seasons, and it is predictable. The impact of El Nino on the conflagration of certain vector-borne diseases like malaria, in particular, in the Thar desert needs special attention to comprehend climate-disease relationship (Nicholls 1993; Bouma and van der Kaay 1994). An El Nino event is a major change in the global climate system associated with epidemic warming of the upper ocean layer in the eastern tropical Pacific Ocean, lasting for 3 or 4 months. The El Nino events are linked with rainfall and temperature extremes and are a major cause of inter-annual climate variability. During 1990 El Nino event, a postulation was cast for heavy rains in northwestern India, on one hand, while in case of the 1997 El Nino event an increased risk of serious drought was forecast in India, on the other. It is noteworthy that the Thar Desert had unprecedented heavy rains (>1000 mm in some areas) during 1990, but also experienced a string of serious droughts for 3 consecutive years during 1998–2000! Climatically, the transmission of malaria is affected by rainfall patterns, triggered in turn by the El Nino patterns (Bouma et al. 1994a, b). Studies have already proved a strong correlation between outbreaks of malaria in certain parts of the Indian Subcontinent and Sri Lanka and the ENSO (Bouma and van der Kaay 1996), although it remains debatable whether all epidemic episodes in the Thar Desert were actually consequent to the ENSO (Bouma and van der Kaay 1994; Bouma et al. 1994b; 1997a, b).

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The Phenomenon of ‘Inundative Vectorism’

It is a well-acknowledged fact that in the arid areas the vector mosquitoes cannot breed easily and their lifespan is restricted, reducing the chances for the mosquito to become infective after completion of the sexual cycle of the malaria parasite. Working on the causes for the widespread malaria epidemic of 1994 in the Thar Desert, Bouma and van der Kaay (1994) refuted the basic hypothesis emphasizing that the epidemic, which seemed to be a repeat of the epidemic in 1990, was likewise caused by heavy monsoon rains and cuts in India’s budget for malaria control. The monsoon rainfall in India is affected by the ENSO, and years with a low and high precipitation—and thus low and high risk years, respectively, for malaria epidemics—can be forecast. The relation between the ENSO and the rainfall was found more stronger in the Thar Desert region where 22 of the 25 ENSO events between 1875 and 1980 had below average rainfall. The two massive epidemics in the Thar Desert during 1990 and 1994 emerged 3 and 2 years after the ENSO events during 1987 and 1992, respectively. Tyagi (1997a, b), on the other hand, propounding a new theory of ‘inundative vectorism’, agreed but partially with the above ENSO-malaria theory as being applicable to only a small part of the Thar Desert region in the lower reaches of the Luni river basin, particularly the Barmer district. According to Tyagi et al. (1995), repeated malaria epidemics in the IGNPirrigated areas in the Thar Desert during 1990s were due to the phenomenon of inundative vectorism, defined as the sudden ushering of one or more vector species in prodigious densities in new virgin areas, like the Thar Desert, when highly conducive conditions were formed through extensive irrigation plans, like the IGNP, for their effective survival and preponderance. In support of this theory, it was advocated that malaria epidemics in the IGNP-irrigated areas could not have occurred until: 1. either the existing desert species, An. stephensi, had modified its behaviour so as to be able to breed in rain-filled water bodies after the monsoon and the seepage water from the canals, or 2. the new entrant, An. culicifacies, highly adaptive to all kinds of open ground freshwater sources, including rainwater, increased its density and biting rate during and after the monsoon rains. During the first half of this century, malaria epidemics did not occur in the Thar Desert presently covered under the IGNP because (1) malaria parasites, including the dangerous P. falciparum, naturally existed in a very low frequency; (2) mostly An. stephensi occurred throughout the Thar Desert, as a dominant vector species which bred characteristically in the intra-domestic earthen pits (‘tanka’ and ‘beri’) and maintained a low adult density; and (3) the ecological conditions dominated by extremes of temperature (about 0 °C in winter and 50 °C in summer) and low relative humidity for most part of the year precluded possibilities of survival of both the vector and the parasite. In areas under the IGNP in the Thar Desert, both, chronologically the older vector, An. stephensi, and the new entrant in the desert along with

24.6

Malaria Control in Deserts

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canalization, An. culicifacies, thrive abundantly for most part of the year. It implies that these two proven vectors transmit malaria in the areas under the IGNP perpetually irrespective of unduly high rainfall. On the contrary, An. culicifacies in the flood-prone Barmer area is largely dependent on monsoon rains and, therefore, is only able to increase density and biting following unprecedented heavy rains in the Luni river catchment areas of the Aravalli mountains. This argument stands good to demonstrate that in the Thar Desert there are two well-demarcated situations in which malaria epidemics could occur; first, an epidemic may essentially occur irrespective of any rainfall such as in the irrigated areas under the IGNP (e.g. Jaisalmer, Jodhpur and Bikanar districts with epidemics of 1994–1996, 1999–2001), and, secondly, an epidemic may occur in the flood-prone areas such as the lower reaches of the Luni river basin (e.g. Barmer and Pali districts with the epidemic of 1990).

24.6

Malaria Control in Deserts

While in Africa, particularly in the sub-Saharan region, following a long history of antimalarials, larvicide and adulticide usage, along with the long-lasting insecticideimpregnated bed nets (LLIN) in recent past, more than one million children in Ghana, Kenya and Malawi have now received one or more doses of the world’s first malaria vaccine, RTS,S/AS01 (RTS,S), most of the other countries with deserts have been nearly completely relying on their strength of medical services embodying Drug Distribution Centres (DDC), Fever Treatment Depots (FTD), Active Surveillance, unique system of Integrated Disease Surveillance Project (IDSP), larviciding in urban centres for An. stephensi control, residual spray (RS) in human dwellings and cattle sheds with adult insecticides, long-lasting insecticide-impregnated bed nets (LLIN) and, of course, a range of repellents, e.g. DEET, DEPA, etc. Malaria control in the Thar Desert, a vast region with hostile climate and topography. is beset with several challenges unseen anywhere else in the country, just like in other arid environments. One of the major constraints, of course, is rather very little knowledge of specific behaviour of the vector species, particularly its breeding in ‘Tanka’ and ‘Beri’ in the Thar Desert (Tyagi 1992a, 1995a, b, 1996a, b, c, d, e, f, g, 2002, 2020; Tyagi and Verma 1991; Tyagi and Yadav 1996a, 2001a, b), and suspected attribute of overwintering. At the same time, determination of immunity level of the desert population is important to realize the counter potential of the local population against the malarial parasites. The human populations in the Thar Desert, just like in other deserts, are mobile due to their evergrowing need for food and fodder for the cattle and pet animals and hard to reach to deliver medication on time. In case of most of malariated deserts of the world, including the Thar Desert, highly fragmentary efforts have so far been made to find out alternate vector control methods in view of insecticide resistance development in the vectors, and virtually no research has been made to understand the health facility seeking behaviour of the desert population, mainly the women-folk and more particularly the pregnant women. Although residual insecticide operations have

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been in vogue for several years, no major studies have been undertaken to quantify its impact on reduction of the year-by-year incidence of malaria. In the Thar Desert, since now the combined role of An. culicifacies and An. stephensi in malaria transmission has been confirmed in different physiographic situations of the Thar Desert, it would be interesting and highly useful to develop distributional maps of the sibling species under An. culicifacies and An. stephensi, but also other lessknown primary (An. fluviatilis) and/or secondary (An. subpictus, An. annularis) vectors. Global policy makers need to keep an eye on the malariated deserts which have at least one common feature; they have potential to exacerbate desert malaria and impact malaria situation in the neighbouring regions where successful elimination campaigns were continuing. India, for that matter, is facing a challenge from ‘Desert Malaria’ since the Rajasthan state where it is mostly present is bracing along its border with some highly endemic states such as Punjab, Haryana, Uttar Pradesh, Madhya Pradesh and Gujarat where full-throated malaria elimination campaigns have been progressing. It is noteworthy here to mention that India currently has a National Framework for Malaria Elimination (NFME) in India 2016–2030, and the country’s resolve to achieve this target can be realized only when efflux of malaria cases from a region like the Thar Desert could be seriously taken into consideration beforehand! Therefore, desert malaria is very important to the world policy makers, disease managers and programme implementers on malaria elimination. Long-term investigations are the need of the hour to comprehend the world’s deserts’ inherent prowess to conflagrate malaria in the xeric environments.

Conclusion: Will Deserts Transform into Malaria Hotspots Tomorrow?

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Malaria is a mosquito-borne global disease which exerts a whopping disease burden in terms of Disability Adjusted Life Years (DALYs = 56,200,201), mostly in communities of sub-Sahara Africa, South America and Asia (Hay et al. 2017). As far as the desert ecosystems worldwide are concerned, two vector mosquitoes can be singled out for their great prowess to adapt to the xeric conditions, namely, (1) Anopheles arabiensis, one of the eight-sibling species of the deadly Anopheles gambiae complex and a major vector throughout Africa and parts of Arabian Peninsula, and (2) An. stephensi, the enigmatic Asian vector mosquito about which the taxonomic riddle whether it is a species complex or merely comprising a few subspecies (forms or races) is yet to settle. The eco-biological behaviour of An. arabiensis is well known for deciding the modus of implementation of the current intervention tools. However, the recent invasion of An. stephensi in urban Africa with different habitats and breeding behaviour is an alert on the success of malaria vector control efforts achieved so far (Sinka et al. 2020; Kweka 2022). Through a unique amalgamation of environmental, geographic, ecological and biological data, Sinka et al. (2020) have predicted by constructing evidence-based maps, with particular reference to Africa, on a likely expansion of An. stephensi in the near future, if allowed to spread (Fig. 25.1). Results from the study by Sinka et al. (2020) have suggested over 126 million people in cities across Africa could be at risk of malaria infection mainly mediated by An. stephensi. Djibouti City on the Horn of Africa was the first site of intrusion by An. stephensi, detected during an unusual outbreak of malaria in 2012 and invariably followed cyclically by increasingly severe annual outbreaks thereafter. Investigations into these episodes of outbreaks in the fast growing urban environment of Djibouti City revealed the presence of An. stephensi, thriving in all kinds of potable waters. The gradual changes in land use, anthropogenic interventions and climate changes are regarded as the major factors to have led to species shift and re-distribution. From here the vector have travelled to Ethiopia, Sudan and Somalia (Kweka, 2022; Balkew et al. 2020). The intrusion of An. stephensi in various # The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3_25

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Fig. 25.1 Inclusive map: Environmental suitability map of An. stephensi using the updated occurrence database including all African sites. Red indicates a higher probability of environmental suitability, whereas the blue indicates environments with a lower probability, i.e. more likely to be unsuitable for the species to occur. The environmental variables selected by the model as relevant to An. stephensi habitat suitability, in descending order (based on correlation score): Ann. Mean Temp. = 0.461, Human Popn Dens. = 0.370, EVI = 0.174, Precip (season) = 0.161, TCW = 0.134, Irrigation = 0.130, Crop mosaic = 0.010. Turquoise circles indicate the location of cities with a population > one million. The thumbnail map shows the coefficient of variation calculated per pixel across the predicted range, indicating where the ensemble model provides the most reliable (higher confidence: dark green) and least reliable (lower confidence: red) predictions (Source: Sinka et al. 2012)

different places in Africa has been confirmed after the DNA molecular analysis (Balkew et al. 2021). Sinka et al. (2020) overlaid zoogeographic data for An. stephensi across its full range in Asia, Arabian Peninsula and Horn of Africa with spatial models that identify the species’ preferred habitat, and provided futuristic maps of the possible African locations where An. stephensi could establish. This supports the WHO’s call for targeted An. stephensi control and prioritized surveillance (WHO 2020, WHO 2021a, b). Besides Africa as its new home far west of India, An. stephensi has made intrusion in the Indian Ocean island country Sri Lanka in close approximation in the south (Fig. 25.2). Fresh invasions such as these and others projected in the future are being considered as a challenge for the management of An. stephensi in both urban Africa and Sri Lanka, in addition to new sites within India, to retain the achievement attained in malaria control. Within a short span of a decade only, the chronology of zoogeography attained by An. stephensi is both interesting and

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Fig. 25.2 Global prevalence of Anopheles stephensi (purple), recent invasion to new countries (green) and countries at risk (red) (Source: Surendran et al. 2019) Table 25.1 Global malaria incidence between 2017 and 2021

Year 2015 2016 2017 2018 2019 2020

No. of cases (in mill.) 224 229 231 228 227 241

Deaths 445,000 451,000 435,000 405,000 558,000 627,000

Source: extracted from WHO Annual Reports 2016–2021

threatening at the same time! Anopheles stephensi was, in brief, discovered to be established in 2012 or 2013 on the continent of Africa, in Djibouti on the Horn of Africa, in 2016 in Ethiopia, in 2017 in Sri Lanka and in 2019 in the Republic of the Sudan. Being the largest hot desert ecosystem in the world, and the third largest overall after the Antarctica and the Arctic, the Sahara Desert (9.2 million km2; approx. 8% of the earth’s land area) is also the centre of major risk of malaria epidemics and increased intensity of malaria transmission by the combination of two of the world’s dreaded vectors, viz. the original desert vector An. arabiensis and the now unwantedly inveigled An. stephensi. If the global data on malaria between 2017 and 2021 is any indication to remain ever alert and to not allow ephemeral success predate our mind (Table 25.1), then it is extremely to map zoogeography of the emerging and new vectors in the region, ‘especially in the light of the spread of the distribution of some anopheline vectors into new locations’ (Dr Marianne Sinka, pers. comm. 10.x.2022). There have been an array of interventions directed towards control of various vector species in Africa, including An. arabiensis in the Sahara Desert, and most of

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Fig. 25.3 Alert on Anopheles stephensi vector occurrence; last updated 5/10/2022 (Source: WHO 2022, auto permitted with due acknowledgement)

the counties in the arid environments of the desert were either retrieved free from malaria or were kept terra incognita for the disease in human memory. Timely and widespread distribution of long-lasting insecticidal nets (LLINs) and increased coverage by the indoor residual spray (IRS) and urban larval source techniques managed vectors well for the past two decades with significant progress in preventing malaria and related adverse outcomes. This progress is evidenced by the fact that malaria mortalities were stalled from 2018 to 2019, though there was a reversal through increase in 2020. Notwithstanding spectacular success achieved in many countries, both in the sub-Sahara region (SSA) and in the Sahara Desert region (SSD), the unprecedented streak of malaria outbreaks first in Djibouti (2012) and subsequently in Ethiopia (2016), Sudan (2019) and Somalia—all in the expanse of the Sahara Desert— relayed an alert signal not merely to the African continent nations but the whole world, in the recent invasion by An. stephensi, a highly competent vector of Plasmodium falciparum and P. vivax. The introduction of An. stephensi in African countries from Asia has alerted the national malaria control programmes in re-designing vector control strategies. The WHO (2022) has also considered the spread of An. stephensi to be a major potential threat to malaria control and elimination in Africa and southern Asia. This vector alert has been developed to urge WHO Member States and their implementing partners—especially those in and around the Horn of Africa, the Republic of Sudan and surrounding geographical areas and in Sri Lanka—to take immediate action (Fig. 25.3). In fact, An. stephensi s.s., essentially a vector of urban agglomerations in Asia (except the Thar Desert in western India), is entirely different from any of the vector species native to Africa. While An. stephensi typically breeds in containers or cisterns of variety with clean water and appears to quickly adapt itself to the local environment, it also survives extremely high temperatures during the dry season, when malaria transmission is at the low ebb. In the Thar Desert An. stephensi, possibly its cradle, occurs throughout the year, daring the summer (months of

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May–June) when the temperature is as high as 50 °C (aestivation) or in the winter (months of December–January) as low as 0 °C (overwintering), in certain districts thriving with the vector. There the vector species also exhibits certain quaint behaviours, for example, thanatosis or reflex immobilization as a defence mechanism, high reproductive plasticity to breed in both rural (Thar Desert) and urban settings with equal aplomb and alacrity (Tyagi 2002) and the genetic makeup or genome of An. stephensi with 29 previously hidden members of insecticide resistance genes, unreported for any mosquito so far. The genetic configuration of the vector species seems to also confer resistance to multiple insecticide classes, posing potential challenges to its control. For the above attributions of An. stephensi, it is absolutely inevitably essentially desired to inventorize the main factors which are expected to be challenges in the efforts to control the species in the countries where it was earlier not known. These are hinted as follows: 1. In Africa An. stephensi is both taxonomically and molecularly confirmed to be different from any of the native malaria vectors available. 2. Anopheles stephensi breeds mostly in habitats like containers, underground and overhead water-storage tanks, vases, water coolers, cement tanks for animal water drinking and wills. 3. In the Thar Desert, An. stephensi utilizes innovatively the underground water reservoirs, ‘Tanka and ‘Beri’, for breeding and even resting. These water reservoirs offer a unique situation for vector management since both these reservoirs hold water for months or even years for drinking by men and cattle, as well as for the agricultural purpose (Tyagi and Yadav 1996a, b, c). 4. Anopheles stephensi-owned ‘Tanka’ always has pure drinking water, but when, for reasons of tear and wear and/or mismanagement, the An. stephensi leaves the abode of ‘Tanka’, and Aedes aegypti, the well-known vector for dengue/ chikungunya/Zika/Yellow Fever virus, begins to breed there in the organically polluted habitat (Tyagi and Hiriyan 2004). Both ‘Tanka’ and ‘Beri’ are difficult to attend effectively for larviciding. In Sri Lanka the An. stephensi has been found colonizing large water bodies of breeding sites including wells which pose a likewise challenge to control vector (Dharmasiri et al. 2017; Surendran et al. 2019). 5. The rate at which An. stephensi has so far invaded new countries within a short span of 6 years, it can be safely assumed that many more countries in the neighbourhood could well be targeted in the near future, if allowed to disperse unabated. 6. The vector has already exhibited development of resistance against insecticides used in indoor residual spraying (IRS) and in long-lasting insecticide nets (LLINs) in both Sudan and Ethiopia (Ahmed et al. 2021; Enayati et al. 2020; Yared et al. 2020). Compared to An. stephensi, the local native vector, An. arabiensis, is continuing to be susceptible to the insecticides in vogue. For the deployment of preferred insecticide-related tools, it is important to know beforehand the resistance or susceptible status of the vector.

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7. In contrast with studies made on feeding and resting behaviour on An. stephensi in Asia, particularly in India, only fragmentary information is available to its range of feeding on human and bovine blood and resting indoors or outdoors in Africa. 8. Much of Africa, just like that in Djibouti, Ethiopia Sudan and/or Somalia, is under enormous change towards urbanization, that too most of it unplanned and unorganized with little or insufficient drainage system, high rural-urban migration between Saharan and sub-Saharan regions and emerging of urban agriculture at the peripheral regions. Thus, it becomes highly desirable to monitor the impact of these anthropogenic factors on the preponderance and distribution of the vectors like An. arabiensis and An. stephensi, particularly the latter which is well known to be urban and peri-urban malaria vector. Taking cognizance of the above irrefutable challenges associated with the intruding An. stephensi, it is probably most opportune to say here that the Indian model for controlling the vector An. stephensi in metropolises like Mumbai (old name Bombay), Delhi, Chennai and Bengaluru (old name Bangalore) is considered highly successful and must be adopted with modifications to justify present-day needs in both Africa and Sri Lanka (Covell 1928). As a first step towards mosquito control in a fast developing Bangalore metropolitan city in south India, Rajagopalan et al. (1987) prepared a ‘Master Plan for Mosquito Control’. Similar master plans were drafted for Chennai and Delhi later. Since urban malaria is very tricky, unassuming and beset with many operational bottlenecks, there is certainly no single panacea for the solution, and all available ecological, biological, chemical, physical and environmental methodologies should be integrated to target the vector elimination. A few suggestions are: 1. Foremost the entomological surveillance system, aided by modern tools, should be strengthened with the ability to capture the presence of the invasive An. stephensi mosquitoes. 2. Both African and Sri Lankan scientists have a great expertise in mosquito taxonomy. They should take initiative to coordinate capacity building for laboratory and field entomologists in identification of An. stephensi and An. arabiensis and any other anopheline mosquito involved in malaria transmission. Such an expertise at every level of worker will ensure sustenance of achieved success on the vector control. 3. Develop a master plan of the city based on breeding habitats, and thereby identify the potential breeding habitats for An. stephensi in urban and peri-urban for appropriate control design. 4. Since resistance development in An. stephensi is a serious constraint in the way of its management, it is highly desirable to know vector mosquito’s profile of the insecticide resistance in different places of its occurrence. This will help to avoid wastage of time, labour and money in using ineffective insecticide-based strategy in areas where resistant populations occur.

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5. Sentinel sites should be established for continuous data collection in all zones. These sentinels’ sites should operate on proposed standard operating procedures for species sampling, identification and insecticide resistance status. 6. Awareness should be generated among communities through Self-Help Groups (SHG) and ward-heads on the use of personal protection tools such as bed nets for protection indoors and outdoors and repellents for protection outdoors. ‘Desert Malaria’, however, has a complicated epidemiology as it occurs in different ecotypical situations, in different intensities and in different time periods. Moreover more than one vector species can be responsible for malaria exacerbation and outbreaks. Firstly, while ‘Desert Malaria’ per se in the penetralium of the desert is triggered by An. stephensi, it is usually P. vivax-dominated malaria; however, it could be dominated by P. falciparum if the primary malaria vector, An. culicifacies, joined An. stephensi in the disease transmission in a heavily canal-irrigated Thar Desert region; secondly, ‘Desert Oasis’ vectors may result in focal outbreaks in the congregated communities generally undertaking movements or even migration between sites of oases and those that are hyperendemic for malaria; and thirdly, ‘Desert Fringe’, being dependent on heavy rainfalls on the periphery of desert, can really vector heavy epidemics exacting multiple deaths and health devastation. These malaria ecotypes, especially, when conjoined or even solitary, may spill malaria cases to the neighbouring areas where these may multiply unabatedly or impair a successful control programme already in process. ‘The spread of the vectors, and subsequently malaria, into new areas is something we need to keep highlighting’ (Dr Marianne Sinka, pers. comm. 15.vi.2022). Hot deserts, particularly the Sahara and the Thar, do not remain malaria-free any longer. Contrarily these have become heavily malariated, due mostly to anthropization, climate change and vector dispersal to newer areas. It is, therefore, most important for the world countries, particularly those bracing the malarious desert ecosystems, to keep a constant watch on the movements of both humans and vectors, as well as the malariogenic factors in the deserts.

Glossary

ABER Annual blood examination rate. Slides examined as % of population over a year period. Abiotic factors The climatic characteristics (temperature, humidity, saturation deficit, rainfall, light, wind) and edaphic characteristics (type of soil, soil texture) of a region or habitat. ACD/PCD Active/passive case detection. Aedeagus A finger-like evagination of the ventral body wall of male mosquito enclosing the terminal section of the ejaculatory duct. Allergy A state of hypersensitivity to a given material (called an allergen), acquired through exposure; re-exposure to the Allergen shows altered reactivity. Al Nina A phenomenon opposite of El Nino. Antennae Paired appendage of head of insects and other arthropods. Usually with many segments. Antennae carry chemosensory organs. Anterior The front end. Anterodorsal The front of the upper surface. Anteroventral The front of the under surface. Anthropophilic Man-biting (literally: liking man). API Annual parasite incidence. The number of parasite-positive blood slides per thousand population. Apical At the tip or end of (APEX). Arthropod An animal belonging to the phylum Arthropoda in the animal kingdom, having a hard jointed exoskeleton and paired, jointed legs. The phylum includes, among other classes, the Arachnida and the Insecta, many of which are important medically as parasites or as vectors of organisms capable of causing disease in man. Attack phase (of a control programme) The phase in which all houses are treated, regardless of whether or not the house was infested. Biological control Control measures by means of living organisms. Biology The science that deals with the phenomena of life and with living organisms in general. Bionomics The (quantitative) relation of the development, reproduction, and survival of an organism or population of organisms to factors in the environment.

# The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2023 B. K. Tyagi, Desert Malaria, https://doi.org/10.1007/978-981-19-7693-3

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Biotic factors Factors connected directly with the organisms living in a given environment, e.g. nature and availability of hosts, water quality, plant environment, etc. Biotype A small topographic unit, including the biotic community. BSC/BSE Blood slides collected/examined. Bti Bacillus thuringiensis subsp. israelensis, a bacterium well known for its toxicity against vector/pest mosquito larvae. Chromosome A linear structure within the nucleus of a cell composed of proteins and DNA which holds the genetic material or genes of an organism, the arrangement of which is unique to each organism. Control Of insects (or other undesirable animals), the restriction of the population density of such insects to a level below that at which they can be harmful to the interests of man. Cytospecies Species which because of their morphological similarity have been identified primarily by cytological characters, such as the banding patterns of the chromosomes. Cytotaxonomy The description of species based on a study of the banding patterns of the chromosomes. DDC Drug distribution centre. Density (of flies) Number of flies per given area or other unit. Density-dependent A term used to describe factors that vary according to the population density, and provide a form of ‘negative feedback’ to stabilize population numbers. All living populations must be limited by density-dependent factors operating on either their birth rate or death rate (or both); otherwise their populations would increase forever. ln some cases, however, populations can be limited by density-independent factors, before density-dependent factors come into operation. Diptera An order of insects containing the two-winged flies which have only the anterior pair of wings well developed. Dispersion The movements of flies in and around a locality or area in which they emerged or are found at a given time. Diurnal Daytime—usually relating to a cycle of activity. The opposite of nocturnal. Dorsal Upper surface or back. Drug resistance in parasite The ability of a parasite strain to survive and/or multiply despite the administration and absorption of a drug in doses equal to higher than those usually recommended but within the limits of tolerance of the subject. Ecology The study of the inter-relationship between organisms and their environment (including other organisms). Ectoparasite A parasite that lives on the external surface of an animal, e.g. fleas, lice, mites, ticks. El Nino A term used to describe anomaly in the flow of ocean waters along the west coast of South America. This anomaly is the result of the nutrient-rich cold water

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of the coastal Humboldt Current being replaced by eastward flowing warm ocean water (which is nutrient poor) from the equatorial Pacific. EIR Entomological inoculation rate. The number of infectious mosquito bites a person is exposed to in a certain time, typically a year. The EIR is the product of the human biting rate (HBR) and sporozoite rate. Endemic disease A disease that is caused by factors that are constantly present within a given geographical area or population group. Endophilic insects Insects that regularly enter houses and spend at least part of their life indoors. ENSO The ‘El Nino’ Southern Oscillation is a large-scale atmospheric ‘seesaw’ centred over the equatorial Pacific Ocean. The variation in pressure is accompanied in surrounding areas by fluctuations in wind strengths, ocean currents, sea surface temperatures, and precipitation. The Southern Oscillation (SO) and the warm waters of the El Nino are part of the same climate phenomenon referred to as ENSO (El Nino/Southern Oscillation). The ENSO triggers several climatic vagaries: from heavy rainfall to flooding in arid areas (e.g., parts of Asia, Africa, Australia and southern America), weakening of Summer Monsoon ( e.g., India) and winters becoming milder in western Canada and parts of the northern USA. Overall, disasters triggered by drought are twice as frequent worldwide during El Nino years. Environment The sum total, at a given moment, of all external influences and conditions to which an organism or object is subjected, including all physical, chemical, and biological factors. Epidemic A period of increased prevalence of a given disease in a population (usually, but not necessarily, as a result of factors that are not constantly present in the populations). Epidemiology The study of the factors that determine the frequency and distribution of disease and of other health-related states in populations. Eradication Complete removal or destruction (e.g. of an infectious agent in a given geographical area). Exophilic insects Insects that normally do not enter buildings. Femur The third segment of an insect’s leg, distal to the trochanter. FF/HF Fully engorged/partially engorged female mosquitoes; abdomen of female mosquitoes showing state of engorgement due to blood fed on. FTD Fever treatment depot. Genetic A hereditary factor controlled by genes of the previous generation. Genitalia The external genital organs of the insect; the gonads and their ducts and all associated accessory organs. Genus (plural, genera) a taxonomic category within a family, consisting of one or more generally similar species. GIS Geographical information systems. Gonotrophic cycle The events between successive egg-laying, or the time interval between them. Gravid Swollen and full of mature or nearly mature eggs.

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G/SG Gravid/semi-gravid females. Females with fully or partially developed state of eggs in ovaries. Habitat The physical place (home) where an organism lives. Haematophagous The term applied to an insect that feeds exclusively on blood; in mosquitoes only females blood-feed. Head The anterior region of an insect, which bears the mouthparts, eyes, antennae and houses the brain. Host The animal parasitized by a parasite or disease organism. Humidity or relative humidity The content of water vapour in the air measured as a percentage of the content of saturated air (100% RH). Hyperendemic Heavily endemic. IIBN Insecticide impregnated bed nets. A bed net that is treated with a fast-acting and long-standing insecticide such as deltamethrin, permethrin, and lambdacyhalothrin which is also safe for humans. Immunity Resistance to parasites or other noxious agents or organisms in a given time, e.g. a year. Incidence Occurrence of new cases in a population over time. Infection The invasion of a host by pathogenic microorganisms (establishing a host-parasite relationship) and the subsequent multiplication of the latter within the body of the host. Infestation (1) The invasion of the surface of the body of the host by parasites, (2) The harbouring of parasites on the surface of the body. Insect development inhibitors (IDI) Chemicals which inhibit the development of larvae or pupae. Insecticide A chemical substance or a mixture of substances used to kill insects. It may be applied as a liquid, powder, fine spray, or as vapour. The term ‘larvicide’ is usually applied to an insecticide that kills immature stages of insects, and the term ‘adulticide’ to an insecticide that kills mature or adult forms. Insecticide resistance A characteristic that renders a given population of an insect species resistance to a given insecticide although the species is normally susceptible to that being no longer controlled by the insecticide in the area concerned. Insecticide resistance in vector Development of strength in a population of a given vector species to counteract the effect of the conventional or even higher dose of a given insecticide Instar The stage of an insect’s life between successive moults, for example the first instar is between hatching from the egg and the first moult. Integrated control Applied pest control that contains and integrates chemical, physical, and biological control measures (including the use of natural enemies of pests). Larva An immature form occurring in some animals after hatching, differing markedly from the adult form. Larvicides Chemicals which kill larvae directly or by preventing them from developing into adults.

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Life cycle Stages of development through which an organism passes between fertilization of the egg of one generation and the same stage in the subsequent generation. The term is sometimes used loosely to mean the number of days between egg deposition and the attainment of sexual maturity. Mesonotum The notum (tergum) of the mesothorax. Metamorphosis In insects, the series of changes through which the insect passes in its development from the larval through the pupal to the adult form. If the pupa is inactive and does not feed, metamorphosis is said to be ‘complete’; if there is no pupa, or if the pupa is active and feeds, it is said to be ‘incomplete’. Microorganism Any microscopic or ultramicroscopic animal or plant, especially any of the bacteria, protozoa, or viruses. Mortality The action of death on populations; more specifically, the number of deaths in a given population in a given period of time. NAMP National Anti-Malaria Programme. Natural host A host in which a given pathogenic microorganism (or parasite) is commonly found and in which the pathogen can complete its development. The term ‘natural host’ implies that the host is the usual one; it has the same meaning as ‘typical host’. NMEP National Malaria Eradication Programme. Nomenclature The scientific (Latin) names given to species, genera, families, etc. of animals and plants. NP Nulliparous female mosquitoes, which have as yet not got opportunity to oviposit eggs even once. Nulliparous The term applied to a female mosquito that has not yet laid the eggs. Oviposition The act of depositing eggs. Parasite An organism which derives its nutrition by competing with its host, often with deleterious results to the host, or by feeding upon its tissues. Pathogen An organism which causes disease. Pathogenic Causing or giving rise to disease. Pathogens Microorganisms (germs) such as viruses, bacteria, protozoa, and eggs and cysts of worms, which can cause disease if man is infected. PCR Polymerase chain reaction. A method for amplifying DNA in vitro, involving the use of oligonucleotide primers complementary to nucleotide sequences in a target gene and the copying of the target sequences by the action of DNA polymerase. Pest Any mosquito species that is harmful in any way, biting or otherwise, or present in sufficient numbers to be considered a nuisance by man. Pesticide An agent or a substance or a mixture of substances used to kill species regarded as pests by man. Pf Plasmodium falciparum. %Pf Slides with P. falciparum as % of all positive cases. PMH Per man-hour density. Average number of vectors collected in human or animal dwellings (or even outdoors shelters) by hand collection done by standard methods by searches over fixed periods of time.

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Glossary

Polytene chromosomes Chromosomes which have divided many times but have not separated, thereby forming thick bundles of up to a thousand parallel strands. After staining, their banding pattern can be seen under moderate magnification, and they are therefore convenient for examination. They are found in the nuclei of the cells of a few specialized tissues only. Population density The number of individuals of a given population per unit area or volume. Potential Existing and ready for action, but not yet active. Precipitin testing A serological technique whereby the source of a blood meal can be identified by testing it with antibodies to blood from known host species. Predator An animal which preys upon insects or other animals. Preparatory phase (of a control programme) The planning phase, when areas are mapped and surveyed for infestations, prior to the attack phase. Prevalence Existing cases in a population (Point prevalence: cases at a certain point of time; Period prevalence: cases during a period of time). The proportion of individuals in a population having malaria parasites in the blood. Proboscis The mouthparts of mosquito, which form a tube containing the stylets which penetrate the host tissues in order to suck up the host fluids. Pupa The free living, highly mobile but not feeding stage of development of a mosquito that occurs between the larval and adult forms. Pv Plasmodium vivax. Residual treatments Treatments with insecticide formulations having a long-term effect (weeks or months). RS Remote sensing. SFR Slide falciparum rate. The number of blood slides found with P. falciparum as a percentage of those examined. Sibling Very closely related. Literally means brothers or sisters. In taxonomy means the species which make up a single species complex and usually cannot be distinguished by morphological features. Sibling species Good species which do not interbreed but are difficult to separate purely on morphological basis. Species The smallest unit of classification commonly used, i.e. the group whose members have the greatest mutual resemblance are able to interbreed (if not separated in space or time), but not to breed with organisms of other groups (species). Species may be divided into subspecies which differ in certain genetic characters but are able to interbreed. Species complex A species complex consists of a number of species with almost identical morphological characteristics but with differences in certain aspects of their biology, behaviour, and distribution. In most cases, the distinction has to be made using modern diagnostics such as the cytological tools or the PCR techniques. SPR Slide positivity rate. The number of blood slides found with Plasmodium parasites as a percentage of those examined.

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Subspecies A geographical group of local populations, differing taxonomically from the other groups of the same type forming part of the species under consideration. Surveillance Observation of a thing, an animal, or a person. The term also implies supervision or inspection. Survey To examine for some specific purpose; to inspect or consider carefully; to review in detail. Taxon (plural taxa) The basic taxonomical units. Often refers to species, but can refer to an element of the classification at any level. Taxonomy Classification of animals and plants divided into species, genera, families, etc. Terrestrial Living on the ground. Thorax Flies and other insects are divided into three regions: head, thorax, and abdomen. The thorax carries the legs and wings. Tibia The fourth segment of an insect’s leg, distal to the femur. UF Unfed female mosquitoes, which have not got a chance to feed on blood, say, before sampling was done on them. ULV Ultra-low-volume concentrate. Vector An arthropod or other animal that carries a parasite from one host to another host. The vector may or may not be essential for the completion of the life cycle or the parasite. If it is not essential, it is referred to as a ‘mechanical vector’. Vectorial capacity The number of infective bites a person receives in a given period. A function of relative populations of mosquitoes and people, feeding frequency of the mosquito, duration of the latent period in the vector, and the survival of the vector. Ventral Pertaining to the front or lower surface. Wettable powder A water dispersible but insoluble, formulation of an insecticide, in which the active ingredient is bound to an inert insoluble carrier material such as talcum powder. Wettable powder formulations are mixed with water to be sprayed, and usually have greater residual activity than liquid formulations of the same insecticide. Zoonosis A disease of animals that may be transmitted under natural conditions to man. Zoophilic Feeding on animals other than man.

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