Neglected Tropical Diseases - Europe and Central Asia [1st ed. 2021] 9783030842222, 9783030842246, 3030842223

Table of contents :
Contents
Introduction
1 Background
2 NTDs in Europe and Central Asia
3 Focus and Content of this Volume
References
Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on the Epidemiology and Control Efforts
1 Introduction
2 Lifecycles
2.1 A. lumbricoides
2.2 T. trichiura
2.3 Hookworm
2.4 S. stercoralis
3 Clinical Presentation
4 Diagnosis
5 Treatment
6 Control and Prevention
7 Epidemiology of Soil-transmitted Helminths in Europe and Central Asia
7.1 Tajikistan
7.2 Kyrgyzstan
7.3 Uzbekistan
7.4 Georgia
7.5 Slovakia
7.6 Moldova
7.7 Romania
7.8 Albania
8 Strongyloidiasis in Central Asia and Europe
9 Discussion
References
Food-Borne Trematodes: A Focus on Russia
1 General Description of Trematodes
2 FBTs of the Human Hepatobiliary System
2.1 Opisthorchiasis
2.2 Clonorchiasis
2.3 Fascioliasis
3 FBT of the Human Gastrointestinal Tract
3.1 Metagonimiasis
3.2 Nanophyetiasis
3.3 Heterophyiasis
4 FBT in the Lung: Paragonimiasis
5 Prevention and Control Activities
References
Taenia solium Cysticercosis/Taeniosis in Europe and Central Asia
1 Introduction
2 Taenia solium in Western Europe
3 Taenia solium in Eastern Europe
4 Taenia solium in Central Asia
5 Discussion and Conclusion
References
Leishmaniasis in Europe and Central Asia: Epidemiology, Impact of Habitat and Lifestyle Changes, HIV Coinfection
1 Biology
2 Epidemiology
3 Leishmaniasis: HIV Coinfection
4 Impact of Habitat and Lifestyle Changes
5 Impact of Climate Change
6 Immigration from Endemic Countries
7 Future Challenges and Outlook
References
Chagas Disease in Europe
1 Introduction
2 T. cruzi Infection
3 Epidemiology of Chagas Disease in Europe
4 Transmission Routes and Preventive Measures
5 Clinical Features
6 Clinical staging
7 Diagnosis
8 Treatment
9 Socioeconomic Determinants
10 Challenges and the Way Forward
References
Neglected Tropical Diseases in Travelers
1 Introduction
2 Neglected Tropical Diseases in Travelers and Immigrants
3 Dengue
3.1 Epidemiology and Clinical Features in Travelers
3.2 Diagnosis of Dengue in Travelers
3.3 Management of Dengue
4 Schistosomiasis
4.1 Epidemiology and Clinical Features in Travelers
4.2 Diagnosis of Schistosomiasis in Travelers
4.3 Treatment and Prevention of Schistosomiasis in the Non-endemic Setting
5 Strongyloidiasis
5.1 Diagnosis of Strongyloidiasis
5.2 Treatment of Strongyloidiasis
6 Leishmaniasis
6.1 Clinical Aspects of Leishmaniasis in Travelers
6.2 Management of Leishmaniasis in the Non-endemic Setting
7 Other Relevant NTDs in Travelers
References
Diagnosis and Treatment of Neglected Tropical Diseases in Europe: Laboratory Infrastructure, Diagnostic Techniques, Disease No...
1 Introduction
2 Laboratory Infrastructure for the Diagnosis of NTDs
3 Diagnostic Techniques for Specific NTDs
3.1 Schistosomiasis
3.2 Soil-transmitted Helminthiasis (Ascaris lumbricoides, hookworm, Trichuris trichiura)
3.3 Strongyloidiasis
3.4 Chagas Disease
3.5 Intestinal Protozoa Infections
4 Quality Control
5 Disease Notification in Europe and Surveillance-Response Systems
6 Treatment of Specific NTDs in Europe
References

Citation preview

Neglected Tropical Diseases

Peter Steinmann Jürg Utzinger   Editors

Neglected Tropical Diseases - Europe and Central Asia

Neglected Tropical Diseases Series Editor Peter J. Hotez, National School of Tropical Medicine, Baylor College of Medicine and Texas Children’s Hospital, Houston, USA

This book series publishes contributions from individuals engaged in any of the fields related to neglected tropical diseases clearly connected with their exceptional status as neglected. Specific focus of each title lies on the discussion of relevant issues in particular geographic areas of the world. Each volume of the series deals with the unique situation of one region and is built up by a team of authors lead by an expert for the geographic area discussed. This series provides a forum for wealthy discussion on the topic of neglected infectious diseases with a clear focus on basic scientific topics, clinically relevant issues as well as policy issues associated with the area. Topics to be covered: detection, diagnosis, monitoring, vaccine and drug development, new treatments, translational research (link basic research and health system research), clinical aspects, epidemiology, development of new surveillance and control strategies, public health/health policy issues.

More information about this series at http://www.springer.com/series/11165

Peter Steinmann • Jürg Utzinger Editors

Neglected Tropical Diseases Europe and Central Asia

Editors Peter Steinmann Swiss Tropical and Public Health Institute University of Basel Basel, Switzerland

Jürg Utzinger Swiss Tropical and Public Health Institute University of Basel Basel, Switzerland

ISSN 2194-8275 ISSN 2194-8283 (electronic) Neglected Tropical Diseases ISBN 978-3-030-84222-2 ISBN 978-3-030-84224-6 (eBook) https://doi.org/10.1007/978-3-030-84224-6 © Springer Nature Switzerland AG 2021 This work is subject to copyright. All rights are reserved 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 Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Contents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Peter Steinmann and Jürg Utzinger Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on the Epidemiology and Control Efforts . . . . . . . . . . . . . . . Johanna M. Kurscheid

1

11

Food-Borne Trematodes: A Focus on Russia . . . . . . . . . . . . . . . . . . . . . Evgeniya Chernikova

37

Taenia solium Cysticercosis/Taeniosis in Europe and Central Asia . . . . . Chiara Trevisan, Sarah Gabriël, Pierre Dorny, and Brecht Devleesschauwer

69

Leishmaniasis in Europe and Central Asia: Epidemiology, Impact of Habitat and Lifestyle Changes, HIV Coinfection . . . . . . . . . . Tanja Barth-Jaeggi and Pascal Mäser

83

Chagas Disease in Europe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 101 Yves Jackson, Luca Basile, and François Chappuis Neglected Tropical Diseases in Travelers . . . . . . . . . . . . . . . . . . . . . . . . 123 Emmanuel Bottieau Diagnosis and Treatment of Neglected Tropical Diseases in Europe: Laboratory Infrastructure, Diagnostic Techniques, Disease Notification, and Surveillance Systems . . . . . . . . . . . . . . . . . . . . . . . . . . 157 Sören L. Becker

v

Introduction Peter Steinmann and Jürg Utzinger

Abstract The geographical focus of this book pertains to Europe and Central Asia, while thematically, the seven chapters concentrate on a group of diseases, collectively termed neglected tropical diseases (NTDs). Geographically, Europe and Central Asia are a contiguous area. Yet, this vast territory is characterized by considerable heterogeneity and enormous cultural, ecological, economic, political, and social diversity, which, in turn, govern people’s health and well-being. For the purpose of this book, Europe and Central Asia are defined as the continent of Europe plus the Asian part of the former Soviet Union, namely Siberia, the Caucasus region, Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, and Uzbekistan. Essentially, this overlaps with the World Health Organization (WHO) European Region (EURO). The bio-eco-geographical diversity of this region is reflected in widely varying biomes, including arctic tundra, extensive forests, steppes, deserts, mountains, and Mediterranean areas. Of note, this region does not include tropical areas in a strict geographical or climatological sense. Keywords Central Asia · Control · Elimination · Europe · Migration · Neglected tropical diseases · Travel

1 Background Millennia of human presence have profoundly shaped many of the main biomes (Dawson et al. 2020). This process hastened with industrialization and mechanized agriculture, which started in the early nineteenth century in Western Europe and, along with the rise of the Soviet Union, reached all areas considered in this book. The economic, political, and social processes associated with industrialization are

P. Steinmann (*) · J. Utzinger Swiss Tropical and Public Health Institute, Basel, Switzerland University of Basel, Basel, Switzerland e-mail: [email protected] © Springer Nature Switzerland AG 2021 P. Steinmann, J. Utzinger (eds.), Neglected Tropical Diseases - Europe and Central Asia, Neglected Tropical Diseases, https://doi.org/10.1007/978-3-030-84224-6_1

1

2

P. Steinmann and J. Utzinger

closely intertwined with the rise of modern medicine, which, in turn, had profound impacts on public health. Today, Europe and Central Asia include some of the richest and most stable societies with advanced health systems; yet, there are also middle- and low-income countries struggling to provide essential curative and preventive health services to their people. Combined, secular developments and targeted interventions have fundamentally changed the distribution, epidemiology, public health measures, and health impact of the group of neglected tropical diseases (NTDs) that are at the heart of this book (Hotez et al. 2006; Molyneux et al. 2021). Indeed, while for many people NTDs are fading from their memory or are only relevant when travelling to tropical and subtropical countries, they continue to be a part of the everyday life for many others (Utzinger et al. 2012). The epidemiology and drivers of NTD endemicity warrant special attention. Historical trends and the recognition of key factors associated with the elimination of NTDs from certain regions of the world or disappearance in specific population groups might facilitate the identification of sustainable control and elimination strategies in areas where they are currently endemic (Monnier et al. 2020; Rollinson et al. 2013). Water, sanitation, and hygiene (WASH) have a profound impact on the transmission of many viral, bacterial, and parasitic disease agents for which stool or urine feature in their transmission cycle (Speich et al. 2016; Strunz et al. 2014; Wolf et al. 2018). Interestingly, in a survey conducted among more than 11,000 readers of the BMJ, the introduction of clean water and sewage disposal—the so-called sanitary revolution—was chosen as the most important medical milestone since 1840 (Ferriman 2007). Hence, one of the fundamental infrastructures of cities and key determinants of public health are water supply and sewage systems. However, the provision of safe water as well as the responsible management of sewage are costly and technically demanding. Universal safe water supply and sanitation can only be provided with central and long-term planning, supported by appropriate technical, financial, and human resources for implementing and maintaining the required infrastructure. Individual hygiene behavior is equally important for infection prevention, and hence, the health status of a population (Fewtrell et al. 2005; Wolf et al. 2018). Since hygiene awareness and daily behavior are to an important degree influenced by family traditions and acquired knowledge, a common focus of hygiene education efforts is on primary schoolchildren and their parents. According to WHO, in 2017, an estimated 16 million people lacked access to safe drinking water and over 31 million people had no access to basic sanitation services across the focus region of this book (Fig. 1). Nutrition is a prerequisite for health and well-being. Undernutrition can be a source of diseases, including parasitic NTDs (Hall et al. 2012; Nweze et al. 2020; Yap et al. 2014). While undernutrition has essentially disappeared from Europe and Central Asia and malnutrition rates have decreased, agricultural production systems and common food items have changed beyond recognition in many areas. Moreover, food safety regulations now routinely prevent many infection risks. However, culinary traditions, including associated behaviors such as the consumption of wild berries and raw fish and meat, traditional animal husbandry systems, and

Introduction

3 Household data - WHO regions - Europe - 2017 - Service Levels

100

Drinking Water Surface water Unimproved Limited Basic Safely managed Sanitation Open defecation Unimproved Limited Basic Safely managed

Coverage (%)

80 60 40 20 0

Drinking Water

Sanitation

Fig. 1 Quality of drinking water supply and sanitation infrastructure at household level in the WHO EURO region. Source: WHO UNICEF Joint Monitoring Programme (JMP) https://washdata. org/data/household#!/ (accessed: 18 April 2021)

hunting of wild animals are cherished traditions in many societies. Coupled with insufficient hygiene standards, such activities are at the root of the persisting transmission of food-related NTDs such as taeniasis, cysticercosis, and food-borne trematode (FBT) infections (Fedorova et al. 2020). Livestock production systems have evolved from traditional subsistence and small-scale farms to modern agricultural enterprises focusing on intensive production through mechanization and specialization. A particular aspect includes the dramatically reduced physical contact between humans and livestock and the separation of livestock from natural environments. Veterinary management of domestic animals, livestock, and wild animals has resulted in the elimination of zoonotic NTDs from a large part of their previous range and niches (Devleesschauwer et al. 2017). Indeed, animal vaccination and deworming are routinely implemented in many countries against several diseases, including NTDs. Cases in point are dog-mediated and wild animal rabies, taeniasis/cysticercosis, and echinococcosis linked to domestic animals (Robardet et al. 2019).

2 NTDs in Europe and Central Asia Out of the 20 NTDs currently recognized by WHO, at least eight are endemic in Europe and Central Asia and are of local public health relevance: echinococcosis, FBT infection, leishmaniasis, leprosy, rabies, soil-transmitted helminth (STH) infection, snakebite envenoming, and taeniasis/cysticercosis. Additionally, local transmission of schistosomiasis has recently been observed on Corsica, France (Boissier et al. 2015). The status of some of the other NTDs in Europe and Central Asia is unknown, e.g. scabies and other ectoparasites. While some of these diseases have historically been widespread and common, such as leprosy, rabies, STH infection, and taeniasis/cysticercosis, others have always been focal and relatively rare—or unrecognized—such as FBT infection and snakebite envenoming. Echinococcosis

4

P. Steinmann and J. Utzinger

and leishmaniasis have historically been confined to certain regions. However, recently they have expanded their endemic area, most likely as a result of habitat transformation and climate change (Chalghaf et al. 2018; Semenza and Suk 2018). Of note, the decline of certain diseases is closely linked to biomedical interventions, such as dog and wild animal vaccinations against rabies, while others retreated in the wake of improved living and sanitation standards, as is the case with STH infection and taeniasis/cysticercosis. The slow disappearance of leprosy from Western Europe started several hundred years ago and is probably linked to the gradually improving nutritional status and living conditions (Irgens 1981; Meima et al. 2002), a process that is not yet completed in marginalized communities in some of the countries considered here (Anonymous 2020). While the burden of NTDs (GBD Demographics Collaborators 2020) in Europe decreased mainly due to profound social and economic development, coupled with lifestyle changes, European research institutions, pharmaceutical companies, and donors were instrumental in the scientific study of NTDs, the development of new diagnostics, drugs, and vaccines, as well as funding the global fight against NTDs. Historical key drivers besides scientific interest were the colonialization of tropical areas, which prompted important investments in tropical medicine to protect European settlers, merchants and military personnel, while maintaining the labor potential of local populations and extending western medicine to indigenous populations through missionary hospitals. To name but a few: in 1855 the German Rudolf Virchow discovered the parasite causing echinococcosis; the Norwegian Gerhard Armauer Hansen discovered in 1873 the causative agent of leprosy (i.e. Mycobacterium leprae) and, in 1885, the French Louis Pasteur developed the first effective rabies vaccine for post-exposure prophylaxis of animal bite victims. Meanwhile, institutes pursuing research, education, and services with an emphasis on tropical medicine were established, e.g. in Belgium, Germany, Great Britain, Portugal, Spain, and Switzerland, with some flourishing to this day and contributing to a deeper understanding of NTDs and, more broadly, global health. This point is underscored in Fig. 2. In brief, we systematically searched the Web of Science Core Collection (https://apps.webofknowledge.com). Our search covered the timespan 2015–2020 and included the following document types: articles, book chapters, editorials, letters, and reviews. We searched for the 20 NTDs currently listed by WHO, namely (i) rabies; (ii) dengue and chikungunya; (iii) trachoma; (iv) yaws (endemic treponematoses); (v) Buruli ulcer; (vi) leprosy; (vii) Chagas disease; (viii) human African trypanosomiasis (sleeping sickness); (ix) leishmaniasis; (x) dracunculiasis (Guinea-worm disease); (xi) soil-transmitted helminthiases; (xii) lymphatic filariasis; (xiii) onchocerciasis (river blindness); (xiv) schistosomiasis (bilharzia); (xv) taeniasis/cysticercosis; (xvi) echinococcosis (hydatidosis); (xvii) food-borne trematodiases; (xviii) mycetoma, chromoblastomycosis, and other deep mycoses; (xix) scabies and other ectoparasites; and (xx) snakebite envenoming. We searched for these NTDs in the “Title” (TI), “Author Keywords” (AK), and “KeyWords Plus” (KP). We then counted the number of publications that are linked to one of seven selected tropical (medicine) institutes/schools based in Europe (i.e. Bernhard Nocht Institute for Tropical Medicine [Hamburg, Germany], Institute

Fig. 2 Number of publications in 2015–2020 produced by seven tropical (medicine) institutes/schools based in Europe that are cross-referenced in the Web of Science Core Collection, stratified by the 20 NTDs considered by WHO. Note that the following types of publications were considered: articles, book chapters, editorials, letters, and reviews (accessed: 30 April 2021)

Introduction 5

6

P. Steinmann and J. Utzinger

of Hygiene and Tropical Medicine [Lisbon, Portugal], Institute of Tropical Medicine [Antwerp, Belgium], ISGlobal [Barcelona, Spain], Liverpool School of Tropical Medicine [Liverpool, UK], London School of Hygiene and Tropical Medicine [London, UK], and Swiss Tropical and Public Health Institute [Basel, Switzerland]). Overall, there were 3597 publications, with the London School of Hygiene and Tropical Medicine and Swiss Tropical and Public Health Institute together contributing 56% of the research output. Worldwide, there were 47,310 NTD publications between 2015 and 2020; hence, the seven selected European institutes contributed 7.6% of the global share. Europe, in particular Great Britain and Germany, is among the leading funders of global NTD research, control, and elimination efforts. Six out of the 11 companies currently donating drugs to WHO for the control and elimination of NTDs are based in Europe. In addition to endemic NTDs, the population living in the target area of this book is potentially exposed to virtually all other NTDs due to the unprecedented rise in both business and leisure travel, long-distance migration, and global trade networks. Indeed, health services have to be alert to conditions that have previously not been encountered since they are only endemic in other parts of the world but are now regularly diagnosed in immigrants and travelers, and sometimes even in individuals who never visited endemic areas. Thus, after years of waning interest, NTDs have become relevant again for health systems even in countries that successfully eliminated most or all of them (Utzinger et al. 2012).

3 Focus and Content of this Volume This book seeks to provide an overview of several important NTDs that are endemic in Europe and Central Asia. It also introduces selected NTDs that are regularly diagnosed among immigrants and have considerable public health relevance. The book concludes with an overview of the diagnosis and treatment standards. The chapter “Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on the Epidemiology and Control Efforts” focuses on STH infections that are the most common parasite infections of humans (Hotez et al. 2008) and were historically widely distributed throughout Europe and Central Asia, as is attested by archeological evidence and historical data (Marti 2019; Mitchell 2017). Of note, Ascaris lumbricoides and Trichuris trichiura are endemic across climate zones, while hookworms are limited to warmer areas that allow for the survival of larvae in the soil. More recently, the prevalence of all STHs decreased dramatically in the wake of improved sanitation conditions and hygiene behavior. However, pockets of endemicity remain, especially in marginalized communities in Eastern Europe and poverty-affected populations in Central Asia (Papajova et al. 2021). The chapter “Food-Borne Trematodes: A Focus on Russia” provides a detailed account of FBT infections from a Russian perspective. It introduces the biology, epidemiology and transmission of the most important FBT species considering

Introduction

7

parasites of the hepatobiliary system, the gastrointestinal tract, and the lung, it summarizes diagnostic approaches and treatment options, and it provides an outlook of prevention and control activities. A particular focus of this chapter is on comparative tables and figures illustrating life cycles and the eggs that are characteristic to each FBT species. The chapter “Taenia Solium Cysticercosis/Taeniosis in Europe and Central Asia” introduces the epidemiology and transmission of taeniasis and cysticercosis before systematically reviewing recent data and reporting trends in Western Europe, Eastern Europe, and Central Asia. Long thought to play a negligible role, cysticercosis seems to be endemic in many countries, particularly in Eastern Europe. The chapter concludes by exploring the possibility that the current understanding of the burden due to cysticercosis is still incomplete and suggests further scientific inquiry to improve this situation. The chapter “Leishmaniasis in Europe and Central Asia: Epidemiology, Impact of Habitat and Lifestyle Changes, HIV Co-infection” pertains to leishmaniasis. It starts by describing the relevant biological and epidemiological characteristics of both cutaneous and visceral leishmaniasis, including the vectors and environmental determinants. Next, it explores the link between leishmaniasis and the human immunodeficiency virus (HIV) infections, and summarizes the impact of habitat changes due to climate change and other anthropogenic changes on local disease outbreaks. The chapter concludes with a survey of leishmaniasis among immigrants and the identification of research needs to successfully respond to future challenges, i.e. the further expansion of the endemic areas. The chapter “Chagas Disease in Europe” presents the transmission cycle and general epidemiology of Chagas disease, an NTD endemic in Latin America that is now recognized as causing an important disease burden among immigrants from endemic countries (Basile et al. 2011). This chapter introduces the specific epidemiology of Chagas disease in Europe, including likely transmission routes and options to interrupt them. The second part of the chapter is dedicated to aspects related to the diagnosis and treatment of Chagas disease in Europe, socio-economic determinants and persistent challenges related to Chagas disease among immigrants in Europe. The chapter “Neglected Tropical Diseases in Travelers” provides an overview of the current knowledge pertaining to non-endemic NTDs in travelers and migrants presenting to travel medicine centers in Europe. The starting point are the GeoSentinel studies and other observations in specialized tropical disease centers. Emphasis is placed on the more common NTDs among travelers such as dengue, leishmaniasis, schistosomiasis, and strongyloidiasis, including short introductions of their epidemiology, transmission, clinical features, diagnosis, and management. Observations around less common NTDs are also made. The final chapter introduces current diagnostic and treatment options for NTDs. Starting with the diagnostic infrastructure available in Europe, including traditional parasitological and modern molecular tools, this chapter summarizes quality control and surveillance networks, and reviews the availability of essential drugs currently available to treat and control NTDs. We provide check-lists on NTD endemicity in

8

P. Steinmann and J. Utzinger

Western Europe, as well as sources for selected drugs. A comprehensive overview of data sources used for epidemiological surveillance reports facilitates a rapid identification of relevant information. Acknowledgements Many distinguished experts contributed to the realization of this book. Leading experts in their fields wrote the individual chapters, and we thank each of them for making the necessary time available in their busy schedules and for sharing their knowledge in concise and accessible chapters. The authors of each chapter agreed to, when necessary, review and update previous drafts to keep the chapter content up to date. We thank several colleagues at the Swiss Tropical and Public Health Institute for assistance in one way or another (Dr. Tanja Barth-Jaeggi, Dr. Martin Bratschi, Mr. Giovanni Casagrande, Dr. Johanna Kurscheid, and Dr. Peiling Yap). We are grateful to Springer for entrusting us with the development of the concept for the book, including the choice of focus diseases and topics, chapter authors, and sequence of the different parts. The team was exemplary in providing clear guidance and keeping us focused on the project through regular and friendly reminders. We are particularly indebted for the understanding we always met when reporting yet another delay due to other competing priorities, personal circumstances and the challenges associated with active public health work prior to and during the ongoing COVID-19 pandemic. Last but not least, we are grateful for the care that the production team lavished on the book, including careful editing and a beautiful layout. We are sure that you—dear students, health professionals, and other interested constituencies—will enjoy reading this book as much as we enjoyed conceiving it. April 2021, the editors.

References Anonymous (2020) Global leprosy (Hansen disease) update, 2019: time to step-up prevention initiatives. Wkly Epidemol Rec 95:417–440 Basile L, Jansa JM, Carlier Y, Salamanca DD, Angheben A, Bartoloni A et al (2011) Chagas disease in European countries: the challenge of a surveillance system. Euro Surveill 16:19968 Boissier J, Mone H, Mitta G, Bargues MD, Molyneux D, Mas-Coma S (2015) Schistosomiasis reaches Europe. Lancet Infect Dis 15:757–758 Chalghaf B, Chemkhi J, Mayala B, Harrabi M, Benie GB, Michael E et al (2018) Ecological niche modeling predicting the potential distribution of Leishmania vectors in the Mediterranean basin: impact of climate change. Parasit Vectors 11:461 Dawson T, Hambly J, Kelley A, Lees W, Miller S (2020) Coastal heritage, global climate change, public engagement, and citizen science. Proc Natl Acad Sci U S A 117:8280–8286 Devleesschauwer B, Allepuz A, Dermauw V, Johansen MV, Laranjo-Gonzalez M, Smit GS et al (2017) Taenia solium in Europe: still endemic? Acta Trop 165:96–99 Fedorova OS, Fedotova MM, Zvonareva OI, Mazeina SV, Kovshirina YV, Sokolova TS et al (2020) Opisthorchis felineus infection, risks, and morbidity in rural Western Siberia, Russian Federation. PLoS Negl Trop Dis 14:e0008421 Ferriman A (2007) BMJ readers choose the “sanitary revolution” as greatest medical advance since 1840. BMJ 334:111 Fewtrell L, Kaufmann RB, Kay D, Enanoria W, Haller L, Colford JM Jr (2005) Water, sanitation, and hygiene interventions to reduce diarrhoea in less developed countries: a systematic review and meta-analysis. Lancet Infect Dis 5:42–52 GBD Demographics Collaborators (2020) Global age-sex-specific fertility, mortality, healthy life expectancy (HALE), and population estimates in 204 countries and territories, 1950–2019: a comprehensive demographic analysis for the Global Burden of Disease Study 2019. Lancet 396:1160–1203

Introduction

9

Hall A, Zhang Y, MacArthur C, Baker S (2012) The role of nutrition in integrated programs to control neglected tropical diseases. BMC Med 10:41 Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Invest 118:1311–1321 Hotez PJ, Molyneux DH, Fenwick A, Ottesen E, Ehrlich Sachs S, Sachs JD (2006) Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria. PLoS Med 3:e102 Irgens LM (1981) Epidemiological aspects and implications of the disappearance of leprosy from Norway; some factors contributing to the decline. Lepr Rev 52(Suppl 1):147–165 Marti H (2019) The discovery of helminth life cycles. Adv Parasitol 103:1–10 Meima A, Irgens LM, van Oortmarssen GJ, Richardus JH, Habbema JD (2002) Disappearance of leprosy from Norway: an exploration of critical factors using an epidemiological modelling approach. Int J Epidemiol 31:991–1000 Mitchell PD (2017) Human parasites in the Roman world: health consequences of conquering an empire. Parasitology 144:48–58 Molyneux DH, Asamoa-Bah A, Fenwick A, Savioli L, Hotez P (2021) The history of the neglected tropical disease movement. Trans R Soc Trop Med Hyg 115:169–175 Monnier N, Barth-Jaeggi T, Knopp S, Steinmann P (2020) Core components, concepts and strategies for parasitic and vector-borne disease elimination with a focus on schistosomiasis: a landscape analysis. PLoS Negl Trop Dis 14:e0008837 Nweze JA, Nweze EI, Onoja US (2020) Nutrition, malnutrition, and leishmaniasis. Nutrition 73:110712 Papajova I, Bystrianska J, Giboda M, Becker SL, Utzinger J, Marti H (2021) Intestinal parasites in segregated minority communities of Slovakia: results from a cross-sectional survey in children. Acta Trop 214:105783 Robardet E, Bosnjak D, Englund L, Demetriou P, Martin PR, Cliquet F (2019) Zero endemic cases of wildlife rabies (classical rabies virus, RABV) in the European Union by 2020: an achievable goal. Trop Med Infect Dis 4:124 Rollinson D, Knopp S, Levitz S, Stothard JR, Tchuem Tchuenté LA, Garba A et al (2013) Time to set the agenda for schistosomiasis elimination. Acta Trop 128:423–440 Semenza JC, Suk JE (2018) Vector-borne diseases and climate change: a European perspective. FEMS Microbiol Lett 365:fnx244 Speich B, Croll D, Fürst T, Utzinger J, Keiser J (2016) Effect of sanitation and water treatment on intestinal protozoa infection: a systematic review and meta-analysis. Lancet Infect Dis 16:87–99 Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC (2014) Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med 11:e1001620 Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J et al (2012) Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 142:w13727 Wolf J, Hunter PR, Freeman MC, Cumming O, Clasen T, Bartram J et al (2018) Impact of drinking water, sanitation and handwashing with soap on childhood diarrhoeal disease: updated metaanalysis and meta-regression. Trop Med Int Health 23:508–525 Yap P, Utzinger J, Hattendorf J, Steinmann P (2014) Influence of nutrition on infection and re-infection with soil-transmitted helminths: a systematic review. Parasit Vectors 7:229

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on the Epidemiology and Control Efforts Johanna M. Kurscheid

Abstract Soil-transmitted helminth infections are among the most prevalent neglected tropical diseases. Infections are caused by a group of parasitic worms transmitted via soil contaminated with feces from infected individuals. Highest Ascaris lumbricoides and Trichuris trichiura prevalences are usually found among children while hookworm prevalence increases with age. Clinical presentations range from mild to severe, and while most infected individuals do not realize their status, infections can be fatal. Soil-transmitted helminth endemicity is strongly associated with poverty, limited access to safe water, and poor hygiene and sanitation practices. Once common throughout Europe and Central Asia, improvements in living conditions, treatment availability, and targeted control and health education programs led to their near elimination in Western Europe. Today soil-transmitted helminths are found primarily among marginalized populations and in poorer countries of Central Asia and Eastern Europe and among marginalized populations in central Europe, where environmental and socioeconomic conditions facilitate transmission. This chapter provides an overview of the current status of soil-transmitted helminth infections in Europe and Central Asia with a focus on countries where transmission is ongoing and these parasites remains a public health problem. Keywords Soil-transmitted helminths · Ascaris lumbricoides · Trichuris trichiura · Hookworms · Ancylostoma duodenale · Necator americanus · Strongyloides stercoralis · Epidemiology · Europe · Central Asia

J. M. Kurscheid (*) Swiss Tropical and Public Health Institute, Basel, Switzerland e-mail: [email protected] © Springer Nature Switzerland AG 2021 P. Steinmann, J. Utzinger (eds.), Neglected Tropical Diseases - Europe and Central Asia, Neglected Tropical Diseases, https://doi.org/10.1007/978-3-030-84224-6_2

11

12

J. M. Kurscheid

1 Introduction With nearly a quarter of the world’s population believed to be harboring at least one soil-transmitted helminth (STH) species (WHO 2020b), these intestinal helminths are among the most prevalent parasitic infections worldwide and the most common neglected tropical diseases (NTDs). The term STH refers to a group of parasitic nematodes, most notably the human roundworm, Ascaris lumbricoides, the human whipworm, Trichuris trichiura and the human hookworm species Ancylostoma duodenale and Necator americanus (Jourdan et al. 2018). Strongyloides stercoralis is another STH species of public health importance that can cause disease in humans but is often considered separately due to its unique characteristics, which requires different diagnostic and treatment approaches (Sato et al. 1995; Siddiqui and Berk 2001; Steinmann et al. 2007). There is also a group of Ascaris, hookworm, and Trichuris species which are zoonotic but generally do not develop further after infection nor cause serious disease in humans. These include A. suis, A. ceylanicum, A. braziliense, A. caninum and Uncinaria stenocephala, T. vulpis, and T. suis (Cutillas et al. 2009; Del Giudice et al. 2019; Mahdy et al. 2012; Traversa 2011). If ingested, A. caninum larvae can migrate to the intestine causing eosinophilic enteritis (Prociv and Croese 1990). Skin penetration of the larvae of these zoonotic hookworms may result in cutaneous larva migrans (Brenner and Patel 2003; Del Giudice et al. 2019; Kwon et al. 2003; Mahdy et al. 2012). A. ceylanicum can establish long-term infections and is considered to be an important emerging human parasite in some regions (Traub 2013). Toxocariasis (caused by Toxocara spp.) is another zoonotic helminthiasis transmitted primarily from dogs and cats. It is ubiquitous, including in Europe (Rostami et al. 2019; Rostami et al. 2020) and recognition of its importance as a neglected disease of humans is increasing (Chen et al. 2018; Paller and de Chavez 2014; Rostami et al. 2019). Human infections, although rare, may result in severe clinical syndromes caused by larvae migrating through tissues or organs such as the eyes, heart, lungs, and brain (Ahn et al. 2014; Hotez 2014; Kuenzli et al. 2016; Walsh 2011). Children are disproportionately affected and infection with Toxocara can lead to stunted growth and poor physical and mental development (Walsh and Haseeb 2012). This chapter focuses on the most common STH species infecting humans: A. lumbricoides, T. trichiura, the hookworm species A. duodenale and N. americanus, and S. stercoralis. Soil-transmitted helminthiasis, like most NTDs, is inextricably linked to poverty, inadequate sanitation, and poor hygiene conditions and behavior, and limited access to clean water. Warm, moist environments of tropical and sub-tropical regions facilitate the persistence and transmission of STH (Pullan et al. 2014) but the parasites also occur in temperate climate zones. In recent decades, the burden of STH has been significantly reduced, largely due to mass drug administration in the frame of preventative chemotherapy campaigns. However, STH remain endemic in many high income countries, with a focus on neglected populations where poverty rates are high and living standards remain low (Hotez et al. 2014).

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

13

Transmission of STH occurs through contact with the infective stages present in soil contaminated with human feces from infected individuals while person-toperson transmission does not exist. For A. lumbricoides and T. trichiura, infection is through ingestion of the infective eggs from either contaminated food, soil, or water, and raw or unwashed vegetables (Strunz et al. 2014). Hookworm and S. stercoralis infections are through skin penetration with infective larvae, most often in the frame of barefoot walking (CDC 2019a, b, c, d; Jourdan et al. 2018). Infection with S. stercoralis can also occur through autoinfection when the filariform larvae penetrate the intestinal wall or skin of the perianal region (Ganesh and Cruz Jr. 2011). A. duodenalis can also be acquired by ingestion of larvae or via the transmammary route (Brooker et al. 2004). Typical manifestations of poverty, poor sanitation, inadequate hygiene practices, and unsafe water supply, as well as low education levels, overcrowding, shared sanitation facilities, having to travel far to fetch water and the use of wastewater or sewage sludge in agriculture are associated with STH infections (Amoah et al. 2018; Jourdan et al. 2018; Strunz et al. 2014; Traub et al. 2004). Environmental factors such as soil type (Amoah et al. 2017) and land surface temperature (Brooker et al. 2002) also influence the transmission potential for STH as under the right conditions, STH eggs remain viable for many months or years (CDC 2019a). A. lumbricoides and T. trichiura infection have been found to be more common in peri-urban areas compared to urban and rural areas, whilst the prevalence of hookworm and S. stercoralis are higher in rural areas (Pullan and Brooker 2012). Ascariasis is also associated with frequent contact with pigs, which often harbor the related A. suum species but can also be infected with A. lumbricoides (Monteiro et al. 2019; Traub et al. 2004). The main risk factors for hookworm and S. stercoralis include agriculture and mine work and walking barefoot (Matthys 2007; Schär et al. 2013). Genetic factors may also play a role in individual susceptibility to STH (Wright et al. 2018). In general, children are most at risk of ascariasis and trichuriasis, with prevalence and intensity of infection highest in preschool- and school-age children, whereas for hookworm peak prevalence and intensity is most often seen in adolescence or early adulthood, after which it begins to stabilize (Weatherhead and Hotez 2015).

2 Lifecycles 2.1

A. lumbricoides

After infective A. lumbricoides eggs have been ingested, the larvae hatch, penetrate the intestinal mucosa, and are transported by the blood stream to the liver and then to the lungs where they mature before penetrating the alveolar walls. Once inside the alveolar space, the larvae ascend the bronchial tree to reach the throat and are swallowed. Upon reaching the small intestine the larvae develop into adult worms which sexually reproduce and can survive for 1–2 years (CDC 2019a; Jourdan et al. 2018). Egg production occurs 2–3 months after infection (Jourdan et al. 2018).

14

J. M. Kurscheid

A female worm may produce approximately 200,000 eggs per day, which reach the environment in the feces and remain viable for years in the right conditions. In order to become infective, A. lumbricoides eggs must incubate at 5 to 38
C for 8 to 37 days (Brooker et al. 2006). The infective larvae develop within fertile eggs, which, when ingested by a human host, can again result in an infection (CDC 2019a; Claus et al. 2018).

2.2

T. trichiura

After a human host ingests the infective T. trichiura eggs, they hatch in the small intestine. The larvae then mature into adult worms in the colon and establish themselves in the cecum and ascending colon where they mate and the female produces eggs (between 3000 and 20,000 per day). Adult worms may survive and produce eggs for several years. The unembryonated eggs are excreted with the feces. In the soil, the eggs develop into the 2-cell stage followed by an advanced cleavage stage and then embryonate (infective stage) (CDC 2019d). In order to become infective, T. trichiura eggs must incubate at 5 to 38
C for 20 to 100 days (Brooker et al. 2006).

2.3

Hookworm

When the human host comes into contact with contaminated soil, the infective filariform larvae penetrate the skin (e.g. on bare feet) and are transported via the circulatory system to the heart followed by the lungs. Here they penetrate the pulmonary alveoli, ascend the bronchial tree to the pharynx, and are swallowed. A. duodenale infection can also result from ingestion of the infective filariform larvae. Once the larvae reach the small intestine, they mature into adult worms and reside in the lumen where they attach to the intestinal wall and feed on blood. This attachment results in blood loss, which can lead to anemia in the host. The adult worms reproduce sexually and eggs are excreted with feces. Female adult A. duodenale hookworms produce 10,000 to 20,000 eggs per day, whereas N. americanus produce 5000 to 10,000. Under favorable conditions, the rhabditiform larvae hatch within a day or two and become free-living in soil. After two molts (which take approximately 5–10 days and temperatures below 40
C), they develop into the infective filariform larvae, ready to infect a new host. Typically, adult hookworms survive in the host for several years. In some cases, after skin penetration, the A. duodenale larvae can become dormant usually in the intestine or muscle, which are then capable of re-activating and establishing patent, intestinal infections (CDC 2019b; Jourdan et al. 2018).

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

2.4

15

S. stercoralis

The S. stercoralis life cycle is complex and involves a free-living and a parasitic cycle, while autoinfection is also possible. The free-living cycle is established when rhabditiform larvae in the intestine are excreted in feces of an infected individual and develop into free-living adult males and females that sexually reproduce, resulting in the production of eggs. In contrast to other STH species, female adult S. stercoralis worms produce very low egg numbers, up to 40 per day. Rhabditiform larvae hatch from these eggs and develop into a new generation of adults. Alternatively, infective filariform larvae may develop, which then goes on to infect new hosts through skin penetration, initiating the parasitic cycle. In this parasitic cycle, the filariform larvae present in contaminated soil penetrate the host’s skin and migrate to the small intestine where they undergo two moltings to become adult female worms. The females live embedded in the submucosa of the small intestine and produce eggs via parthenogenesis (parasitic males do not exist) from which rhabditiform larvae hatch whilst still in the intestine and are either excreted in feces or further develop into filariform larvae that cause autoinfection (CDC 2019c). This autoinfective cycle of S. stercoralis is unique among helminth parasites and can result in long-lasting infection (Schär et al. 2013).

3 Clinical Presentation Soil-transmitted helminthiasis is rarely fatal and light infections are often asymptomatic or can present in non-specific symptoms that are not readily noticed by the patients (Claus et al. 2018). Chronic or high intensity infections can, however, lead to morbidity, with an estimated global burden of 3.3 million disability-adjusted life years (DALYs) in 2016 (Hay et al. 2017), mainly driven by the high number of infected individuals. In children and women of reproductive age, moderate- and high-intensity chronic STH infections can lead to anemia, stunting (through malnutrition), neurological or cognitive deficits (affecting a child’s ability to learn), and cause damage to affected organs (e.g. brain, liver, and urinary tract) (Weatherhead and Hotez 2015). High worm burden and co-infections exacerbate morbidity (Weatherhead and Hotez 2015). The most common of the four main STH species is A. lumbricoides, which in 2010 was estimated to account for more than 60% of global STH infections, and also accounts for most deaths attributable to STH (Pullan et al. 2014). Ascariasis can cause abdominal pain and intestinal obstruction and, in severe cases, perforation of the intestine (Gupta et al. 2012; Mbanga et al. 2019; Villamizar et al. 1996). Clinical manifestations differ as larvae develop and migrate into various tissues (Kennedy and Qureshi 1986). Reactions to the larval migration can result in acute lung inflammation, difficulty breathing, or eosinophilic pneumonia (e.g. Loeffler syndrome) (Aleksandra et al. 2016; Ozdemir 2020). Anemia might result from mucosal

16

J. M. Kurscheid

bleeding in the upper gastrointestinal tract or through generalized inflammation (Claus et al. 2018; Jourdan et al. 2018). Ascariasis has also been reported to cause vitamin A malabsorption (Weatherhead and Hotez 2015). The clinical manifestations of trichuriasis also depend on the parasite burden. Symptoms may include loss of appetite, weight loss, and abdominal pain. In high intensity infections, T. trichiura may cause frequent and painful bloody diarrhea, potentially with rectal prolapse (Bansal et al. 2018; Else et al. 2020; Fishman and Perrone 1984). Chronic infections in children may lead to malnutrition, anemia, and chronic inflammation (Weatherhead and Hotez 2015). Among the four main human STH species, hookworm is responsible for the greatest morbidity in terms of years lived with disability (YLDs) (estimated at 65% of a total of 4.98 million in 2010) (Pullan et al. 2014). One of the most common pathophysiological presentations of hookworm infection is iron deficiency anemia, particularly from A. duodenale infection (Brooker et al. 2004). Hookworm can also lead to protein malnutrition, especially in children (Weatherhead and Hotez 2015). Other clinical manifestations include abdominal pain, diarrhea, weight loss, fatigue, and rash (resulting from larval entry into the skin) (Brooker et al. 2004). Strongyloidiasis, whilst usually resulting in asymptomatic chronic disease of the gut, can also lead to severe health implications due to hyperinfection and dissemination (Gordon et al. 2017; Siddiqui and Berk 2001). Less severe symptoms commonly associated with S. stercoralis infection include abdominal pain, diarrhea and, most frequently, urticaria (Tamarozzi et al. 2019). Disseminated skin rash and eosinophilia are other possible clinical manifestations (Pielok et al. 2019). Left untreated, S stercoralis infection can persist for decades (Siddiqui and Berk 2001). Long-term corticosteroid therapy can lead to hyperinfection, resulting in high mortality rates (up to 87%) (Siddiqui and Berk 2001). Infection in immunocompromised individuals e.g., due to HTLV-1 infection is particularly serious, and can be fatal (Schär et al. 2013). People suffering from chronic alcoholism, renal failure, and diabetes or those who are of advanced age or receive immunosuppressive drugs for organ transplantation are also at increased risk of the severe clinical presentations (Schär et al. 2013). Early diagnosis and effective therapy are therefore essential in order to eradicate the infection (Buonfrate et al. 2015).

4 Diagnosis Stool-based microscopy, either by direct fecal smear or Kato-Katz (K-K), remains the gold standard diagnostic method for STH (Jourdan et al. 2018). Microscopybased diagnostic approaches are relatively cheap and easy to set up requiring fairly basic equipment and training, making it ideal for low-resource and field settings. Sensitivity is an issue and largely depends upon the quality of the slide preparation and skills of the microscopist (Else et al. 2020). Molecular diagnostics are superior in terms of sensitivity but due to the high cost and additional training required, they are

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

17

generally restricted to research settings and high-income countries and are rarely used in endemic field settings (Else et al. 2020). The standard diagnostic methods used for STH are less appropriate to diagnose S. stercoralis (Siddiqui and Berk 2001; Steinmann et al. 2007). This has been attributed to low and irregular shedding of parasite larvae (Schär et al. 2013) but may also be due to the fact that S. stercoralis secretes larvae in feces as opposed to eggs (Ganesh and Cruz Jr. 2011). Nonetheless, stool microscopy and K-K are still often used, especially in prevalence studies (Buonfrate et al. 2015). Coprological examination using the Koga agar plate culture or the Baermann have a higher sensitivity (Knopp et al. 2014; Siddiqui and Berk 2001; Steinmann et al. 2007), although still insufficient (Buonfrate et al. 2015). Serological examination using various ELISA tests have been shown to produce good results and are widely used, however, they have a tendency to produce false-positive results (Salvador et al. 2014). Luciferase immunoprecipitation system technique combined with a recombinant antigen (NIE) and ELISA coproantigen detection have been shown to be an improvement compared to other serological tests (Buonfrate et al. 2015). Molecular diagnostic methods are also used but there remain issues with sensitivity.

5 Treatment Treatment is available in the form of anthelmintic drugs albendazole and mebendazole, and to a lesser extent levamisole and pyrantel pamoate. The first two drugs are administered through mass drug administration campaigns as preventative chemotherapy to schoolchildren in countries where STH is endemic and prevalence exceeds 20% (Pullan et al. 2014). Although these drugs are generally safe and well tolerated, their efficacy varies between the STH species. Whilst most of the drugs are effective against A. lumbricoides, albendazole appears to be more effective against hookworm, while for T. trichiura, a single dose of all drugs achieves good intensity reductions but cure rates are lower (Hotez et al. 2014). The recommended treatment for S. stercoralis infection is ivermectin, which, in cases of disseminated disease, may be combined with albendazole (Ganesh and Cruz Jr. 2011). Important to note is that treatment of STH, including S. stercoralis, does not confer protection against future infections.

6 Control and Prevention The current mainstay of STH control programs is the periodic administration of preventative chemotherapy (PC) in endemic areas. The choice of whom to treat and the frequency of treatment depend on the local epidemiologic situation and available resources. In an area where the whole community is at risk of STH and resources are available, the whole at-risk population may be treated. Often, the true

18

J. M. Kurscheid

epidemiologic picture is not known, especially in low-resource settings. For this reason, a targeted approach is often used, whereby those at greatest risk of infection and morbidity are treated. In the case of STH, this is predominantly children, adolescent girls, and women of reproductive age. Currently, WHO recommends the periodic administration of anthelmintic drugs (typically albendazole or mebendazole) as a public health intervention to all children from the age of 24 months to 12 years, non-pregnant adolescent girls (10–19 years of age) and non-pregnant women of reproductive age (15–49 years of age) once a year in areas where the baseline prevalence is between 20 and 50%. The dose is 400 mg of albendazole or 500 mg of mebendazole. For children aged 12–24 months, a single 200 mg dose of albendazole or 500 mg mebendazole is recommended. In areas where the prevalence exceeds 50%, the frequency of PC should be twice per year, at the same dosage (WHO 2017b). When prevalence starts to fall below 10%, the frequency of PC can be reduced to every two years (WHO 2019), and as prevalence drops below 2%, the treatment strategy moves to selective treatment, whereby only infected subjects are treated through primary health care institutions (WHO 2019). In the short term, the objective of periodic chemotherapy is to reduce worm burden and the morbidity associated with infection, and in the longer term, to reduce transmission (WHO 2017a). The benefits of PC are that drugs are safe and donated at sufficient quantity, while the intervention is easily scalable and cost effective (Vaz Nery et al. 2019). Preventative chemotherapy has had a significant impact globally on reducing the prevalence and morbidity associated with soil-transmitted helminthiasis (Hotez et al. 2018). However, in many endemic areas, budget constraints and the complex logistics impact the frequency and coverage of chemotherapy, meaning it does not always meet set targets and may only be administered sporadically, and not in all at-risk areas. Furthermore, as prevalence levels start to fall to low levels, it becomes more difficult for PC to have the desired impact (Freeman et al. 2019). If elimination is ever to be achieved, an integrated approach is thus needed. This includes incorporating health education and promotion, and improving water, sanitation, and hygiene (WASH) alongside a locally appropriate PC strategy (Freeman et al. 2019). In general, the provision of safe water, adequate sanitation, and good hygiene helps prevent disease and improve health and well-being. Consequently, clean water and sanitation represent one of the United Nations Sustainable Development Goals (SDG 6). Improvements in access to safe water have made great strides in the last two decades but it is estimated that more than 2 billion people still lack access to safe water, affecting primarily people living in rural areas or in temporary settlements (UNICEF and WHO 2019). The nature of STH transmission dynamics means that exposure to contaminated soil, either directly or indirectly, is necessary for infection to occur. Preventing environmental contamination with feces is therefore one of the key factors in interrupting STH transmission. Considering the widespread lack of basic sanitation and the number of STH eggs an infected individual can excrete every day, it is not difficult to imagine the scale of the issue nor to understand the challenge of preventing or even reducing environmental contamination in areas of high STH prevalence.

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

19

Improved sanitation can be defined as the mechanic prevention of contact with untreated human fecal matter, e.g., through flush or pour-flush toilets linked to sewers (JMP 2008). The positive impact of sanitation on reducing the STH burden has been demonstrated through several systematic reviews (Freeman et al. 2017; Strunz et al. 2014; Ziegelbauer et al. 2012). Based on the evidence gained from these reviews, sanitation seems to be most effective at reducing A. lumbricoides and T. trichiura infections but less effective for hookworm and S. stercoralis. Critical to the success of any sanitation intervention is adequate community coverage, uptake and behavior change as well as being appropriate for the setting (Vaz Nery et al. 2019). WASH programs have been proven to be highly effective, but initial investments and maintenance are expensive and can be challenging to successfully implement even in wealthy, industrialized countries (Claus et al. 2018). Increasing knowledge and understanding of how STHs are transmitted and their effects on health are important for modifying people’s behavior to reduce environmental contamination and disease incidence. This can be achieved through welldesigned health education and promotion activities. A prime example is the ‘Magic Glasses’ intervention conducted in 38 schools in Hunan province in China between 2010 and 2011 (Bieri et al. 2013). Bieri and colleagues demonstrated that their cartoon video health education intervention was highly effective at increasing student’s knowledge of STH (nearly double the knowledge score in intervention vs. control group) and the percentage of children washing their hands after using the toilet (98.9% in intervention vs. 54.2% in the control group), as well as decreasing the incidence of STH infection (4.1% vs. 8.4%, P < 0.001 in the intervention and control group, respectively). To ensure health education and promotion interventions are well received and effective at reinforcing educational messages and promoting positive behavior change, it is crucial to make the content engaging and appropriate for the target audience, including adapting content to the local context.

7 Epidemiology of Soil-transmitted Helminths in Europe and Central Asia Historically, STHs were endemic in most of Europe and Central Asia (Bouchet 1997; Bouchet et al. 1995; Dufour et al. 2016; Fernandes et al. 2005; Flammer et al. 2018, 2020; WHO 1964) but improved living conditions and the availability of universal health care, and control and health education programs led to their near elimination (Flammer et al. 2020; Hotez and Gurwith 2011). However, several events in the last two to three decades such as the war in the Balkans, the fall of communism, and the break-up of the former Soviet Union, have resulted in economic collapse and instability resulting in increasing poverty rates. This has led to a regression in many of the improvements that had been made and has driven the

20

J. M. Kurscheid

re-emergence of many diseases including STH across Eastern Europe and Central Asia (Hotez and Alibek 2011; Hotez and Gurwith 2011). Today, STH infections are found primarily in the less developed and poorer countries of Central Asia and Eastern Europe and among marginalized populations in central Europe (Hotez and Gurwith 2011) where environmental and socioeconomic conditions facilitate transmission (Steinmann and Samwel-Mantingh 2013a). The Roma are among the most vulnerable populations for STH infection in Europe (Hotez and Alibek 2011). Among the STH species, A. lumbricoides appears to be the most prevalent with relatively few reports of T. trichiura and hookworm. Strongyloidiasis is increasingly more prominent as more sensitive diagnostic methods are becoming available. Cases have been reported all over Europe. A number of country case studies are offered to illustrate the range of conditions encountered across poorer countries in the Europe and Central Asia region. Although exact numbers of infections are not known, WHO estimates that in the European Region alone, there are four million children suffering from soiltransmitted helminthiasis (WHO EURO 2016). Sporadic cases of STH in returned travelers or immigrants also occur throughout Europe and are largely detected through specialist travel or tropical medicine clinics. The three key priorities listed in the framework for control and prevention of soil-transmitted helminthiases in the WHO European Region 2016–2020 include: strengthening surveillance and diagnosis capacity, mass deworming, and raising public awareness (WHO EURO 2016). Information on soil-transmitted helminthiasis in Central Asia is limited. Most of the earlier data are from the Soviet era when considerable progress had been made in their control. Soil-transmitted helminthiasis was reportedly occurring in humid areas and among miners in Central Asia in the 1950s (Matthys 2007). After the independence of today’s Central Asian countries, public infrastructure and healthcare services deteriorated and STH prevalence rebounded (Hotez and Alibek 2011). It is only relatively recently, with the support of WHO and international development agencies that improvements in access to safe water, sanitation, and healthcare have been made, reducing again the STH prevalence (Steinmann et al. 2010).

7.1

Tajikistan

Among the Central Asian countries, Tajikistan is the poorest and more than a quarter of the population still live in poverty (The World Bank 2020a). Public water and sanitation infrastructure is weak and water scarcity is a growing issue (Matthys et al. 2011). In rural areas, where more than 70% of the population still live (WHO 2020a), only 36% of the population have access to safe drinking water (The World Bank 2020a). A study of 594 school children aged 7–11 years, conducted in the lowlands of the western region in 2009, found that nearly half of the study families relied on drinking water from unimproved sources (e.g. canals, rivers, and unprotected wells) and sanitary facilities that primarily consisted of pit latrines (Matthys et al. 2011). In this cohort, the overall prevalence of STH (assessed by K-K thick

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

21

smear) was 8.6%, with A. lumbricoides the most common (4.4%), followed by hookworm (3.5%) and T. trichiura (1.4%). Although the prevalence of each species was relatively low, nine of the 10 schools surveyed were positive for infection, suggesting STH was widespread across the study region, particularly A. lumbricoides (prevalence ranging from 1.7–16.0%) and hookworm (2.0–10.0%), which were each identified in seven schools. In contrast, T. trichiura was found in only two schools with prevalences in the range of 6.0–8.5%. All STH infections among this cohort were of light intensity based on WHO cut-offs (Matthys et al. 2011; WHO 1998). The most recent data on STH prevalence in Tajikistan come from a national intestinal helminth survey conducted in 2011–2012, also among 7–11 year old children, from 33 schools randomly selected across the country (Sherkhonov et al. 2013). Among the 1642 children surveyed, an STH prevalence of 19.4% (also by K-K thick smear) was reported, mostly due to A. lumbricoides (16.9%). The T. trichiura prevalence was 2.7% but no hookworm was observed. The national survey also revealed that prevalences varied significantly across oblasts (administrative districts). The Gorno-Badakhshan Autonomous Region (GBAO) had the highest A. lumbricoides prevalence (42.1%), followed by the Republican with 22.0%. T. trichiura prevalence was lowest in GBAO (0.4%) but highest highest in the Republican (4.3%) and Sugd (3.5%) oblasts (Sherkhonov et al. 2013). Knowledge and perception of helminth infections also differed across oblasts, and appeared to align with observed prevalences. Khatlon oblast, for example, had the lowest prevalences of A. lumbricoides and T. trichiura (5.4% and 2.4%, respectively) and more than 90% of children were aware of the harmful nature of helminth infections and associated risk factors. In comparison, only one third of surveyed children in GBAO were aware of the potential harm and risk factors of helminths infections (Sherkhonov et al. 2013). In the study by Sherkhonov and co-authors, STH infection status was not found to be associated with knowledge or sanitation and hygiene practices. Rather, the authors speculated that geographic and socioeconomic conditions may have accounted for differences observed in their study (Sherkhonov et al. 2013). Another study published in 2012 (in Russian), found a prevalence of 54.2% among 2629 participants of different ages in the districts of Vanch, Faizobod, and Murgab (Karimov et al. 2012). Higher prevalences were observed in the foothill and mountain zones of Vanch and Faizobod compared to the high-altitude areas in Murgab district. Low levels of personal hygiene and sanitation, and the use of water from unprotected sources were mentioned as explanatory factors for the persistence of STH in these areas. With regard to prevention and control activities, there is no current national program targeting STH but mass deworming campaigns are implemented among children aged 2–14 years.

22

7.2

J. M. Kurscheid

Kyrgyzstan

Kyrgyzstan is a lower-middle income democracy but continues to suffer from political instability which arose with independence from the Soviet Union in the 1990s (The World Bank 2021a; UNICEF 2021). With the assistance of UNICEF and other donors, improvements in WASH have been made in the last decade and according to UNICEF, 77.2% of the population were using appropriately treated water in 2014 compared to only 34.6% in 2006 (UNICEF 2021). Despite such improvements, access to safe water and sanitation remains a major issue, especially in marginalized and rural communities (UNICEF 2021). Previously, rural areas relied on public taps, rivers, and piped water as main water sources and traditional pit toilets (Matthys 2007). Even today, schools across the country have limited access to water with more than one-third reported to have no water supply at all (UNICEF 2021). Despite the recent introduction of hygiene promotion in schools on a large scale, school sanitation has reportedly not improved (UNICEF 2021). The current epidemiology of soil-transmitted helminthiasis in Kyrgyzstan is difficult to ascertain given the scarcity of studies. In 2007, Matthys (Matthys 2007) reported the findings of a school-based parasitologic survey conducted in 35 villages across six oblasts. Among 1998 children and adolescents aged 1–21 years surveyed across 24 villages, a mean prevalence of 26.4% for A. lumbricoides was reported with no difference between males and females but more infections were found in the Leilek district in the South (prevalences of 20–60%) compared to other areas. The prevalence appeared to rise from 3 year olds (approximately 35%) over 6 year olds (approximately 50%) to 12 year olds (approximately 45%). In 2010, a small survey among school children was conducted in a peri-urban municipality near the capital city of Bishkek. Among the 90 children from which multiple samples were collected and analyzed, 54.4% were positive for A. lumbricoides, the only STH species identified (using K-K and FLOTAC) (Jeandron et al. 2010). The same year, 1262 school children aged 6–15 years were surveyed in 51 schools across the southwestern Osh oblast, the largest and most populous oblast in Kyrgyzstan (Steinmann et al. 2010). STH was widely distributed across the oblast with 78.4% of schools positive for infection, although higher prevalences were seen in the north-eastern part of the oblast near the Fergana valley and in mountain areas. Infections were almost exclusively A. lumbricoides at a prevalence of 23.1%. Two cases of T. trichiura and no hookworms were observed (Steinmann et al. 2010). The prevalence of A. lumbricoides was similar to that reported by Matthys in 2007 (Matthys 2007). The absence of hookworm may be due to unfavorable climatic conditions—cold winters and dry hot summers (Steinmann et al. 2010). Despite the relatively high prevalence of A. lumbricoides seen in Bishkek and some schools in Osh oblast, infection intensities (mostly assessed from a subset of samples) were reported to be light. Factors that were either protective or borderline protective against A. lumbricoides infection in Osh oblast included reported washing of raw vegetables and the use of tap water, respectively. Night time defecation in the garden was

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

23

associated with higher prevalence compared to the use of a pot or standard toilet but socioeconomic class was not associated with STH prevalence (Matthys 2007). Kyrgyzstan currently does not have a national framework for STH prevention and control (WHO EURO 2016). However, PC for school-age children has been implemented since at least 2013 and a national coverage of over 75% has been achieved (Montresor et al. 2020). Several key priorities have been noted including: identification of high risk areas, conducting mass drug administration in all schools until prevalence falls below target levels, improving hygiene and infectious disease prevention knowledge through locally-adapted health education campaigns, and improving access to clean water and adequate sanitation (Steinmann et al. 2010; WHO EURO 2016).

7.3

Uzbekistan

Uzbekistan was the first among the Commonwealth of Independent States (CIS) countries to return to growth after independence in 1996 (The World Bank 2016). Poverty rates are low (approximately 9% in 2021) compared to its neighbors (The World Bank 2021b). According to a recent report by the WHO/UNICEF Joint Monitoring Programme, only 59% of the population of Uzbekistan have access to safe drinking water services (UNICEF and WHO 2019). Although this compares well with Tajikistan (48%), the rate lags behind Kyrgyzstan (68%), Kazakhstan (90%), and Turkmenistan (94%). Water services and sanitation infrastructure are reportedly outdated and desperately require updating (UNDP Eurasia 2018). Similar to most countries in Central Asia, rural populations are less likely to have access to safe WASH infrastructure (UNDP Eurasia 2018). The situation in schools appears to be better than in other Central Asian countries. It has been reported that 83% of schools had access to clean drinking water and 78% had access to basic sanitation facilities (UNICEF Uzbekistan 2020). Efforts are being made to improve access to safe water and infrastructure for sewerage collection and treatment across the country in collaboration with WHO, UNICEF, and other donors (The World Bank 2020b; SDC 2014; UNICEF and WHO 2019). Data on STH in Uzbekistan is limited. No national surveys on helminths have been conducted since independence from the Soviet Union in 1991 (Gungoren et al. 2007). A 2001 article (in Russian) mentioned that 200,000 cases of parasitic diseases, including helminths, were notified per year, suggesting that there is some sort of reporting system although no other details could be ascertained from the abstract (Abdiev and Shamgunova 2001). During the Soviet era, efforts were made to eliminate some parasitic diseases as a health problem, including hookworm (Hotez and Alibek 2011). Based on the available literature, ascariasis appear to be the predominant STH disease in Uzbekistan (Abdiev and Shamgunova 2001; Nurtaev et al. 2005). It has been linked to loss in economic productivity (Abdiev et al. 1990; Hotez and Alibek 2011).

24

J. M. Kurscheid

A prospective cohort study published in 2007 aimed to assess the effectiveness of a hygiene promotion for reducing the risk of reinfection by intestinal parasites in children in 276 rural Uzbek households over a 1-year period. It found that over 80% of the surveyed children were infected with at least one intestinal parasite species (Gungoren et al. 2007). The study, which was conducted in the provinces of Fergana and Andijan in the densely populated Fergana valley, found a considerable difference in the prevalence of A. lumbricoides between the two provinces. In Andijan province, 24% of the sampled children were infected compared to only 1% in Fergana province. Study sites were reportedly similar in terms of ethnicity, socioeconomic situation, size of village, geography, topography, access to water resources (none of the villages had access to safe water) and distance to major irrigation channels (main source of drinking water). Interestingly, the study by Gungoren and co-authors (Gungoren et al. 2007) also found that parents typically viewed parasitic diseases as inconsequential, often believing that children will outgrow them.

7.4

Georgia

Georgia is located in the South Caucasus and has historically been known to be endemic for STH. Georgia shares a number of characteristics with many Central Asian and east European countries, including high rates of poverty, a large rural population, insufficient access to safe water and sanitation, a weak healthcare system and no legislation or directives regulating the surveillance, diagnosis, treatment, and control of intestinal helminth infections (Steinmann and Samwel-Mantingh 2013a). In 2012, WHO conducted a mission to assess the current status of intestinal helminth infections in Georgia and its capacity to control infections (Steinmann and Samwel-Mantingh 2013a). The findings indicate that A. lumbricoides and hookworm were the most common STH in the past but as a result of control activities during Soviet times, which largely focused on hookworm, these species are now believed to be nearly eliminated from the country. There are no recent data on the prevalence of these species but a survey conducted in 2009 identified a prevalence of 21% of A. lumbricoides among 800 children in the Tserovani camp for internally displaced persons (Steinmann and Samwel-Mantingh 2013a). However, there are some doubts as to the accuracy of this figure due to concerns of misdiagnosis of A. lumbricoides eggs with other eggs or non-parasitic elements. S. stercoralis is also believed to be endemic but due to the absence of national surveys and unreliable passive surveillance, the prevalence remains unclear (Steinmann and SamwelMantingh 2013a). In addition to the lack of regular surveillance, the WASH situation is unsatisfactory. A 2013 survey by UNICEF of WASH conditions in public schools in Georgia found that WASH standards, whilst better in urban versus rural areas, were well below international standards (Educational and Scientific Infrastructure Development Agency 2013). Quality and access to water (including drinking water) were

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

25

inconsistent across schools and regions, with frequent interruptions to supply. In some areas such as Santskhe-Javakheti, large proportions of schools were without access to a nearby water source and others schools relied upon unimproved water sources. Also concerning, was the near total absence of regular water quality surveillance. Sanitation and hygiene conditions were also poor, with many schools using unimproved sanitation facilities that were often located away from the school buildings (sometimes up to 200 m), not adapted for children with physical disabilities and in insufficient quantities for the number of students (Educational and Scientific Infrastructure Development Agency 2013). It was also found that 10% of schools lacked functional handwashing facilities and the majority of schools failed to provide students with soap or towels for appropriate handwashing behavior. Nearly half of the students did not wash their hands after using the sanitation facilities. To help overcome many of these WASH related challenges, efforts have been made by several international aid organizations. In 2009, UNICEF and the International Rescue Committee (IRC) played a leading role in providing WASHrelated emergency response to schools and displaced people affected by the 2008 conflict in the area of South Ossetia (Degen 2009). More recently, the Swiss Agency for Development and Cooperation (SDC) and UNICEF Georgia have been working together to improve access to WASH facilities for children through the construction of toilet blocks and improving access to running water in schools (UNICEF 2020). Based on the limited information available, there is no legislation or directives regulating the surveillance, diagnosis, treatment, and control of intestinal helminth infections in Georgia and STH are not reportable (Steinmann and Samwel-Mantingh 2013a). A number of control efforts were recommended by Steinmann and SamwelMantingh, including (but not limited to) administering anthelmintic drugs to all school-age children followed by individual level treatment once the prevalence falls below the WHO set limit, implementing locally-adapted health education campaigns and making improvements to clean water and sanitation. Other key priorities include the need to conduct surveys among children and in high risk areas, and training on diagnosis (WHO EURO 2016).

7.5

Slovakia

Slovakia is located in Central Europe and has a significant Roma population (Andjelic 2018). It is one of only few high-income European countries where STH remains endemic, particularly among Roma communities living in unsanitary conditions with limited access to clean water and health facilities (Andjelic 2018; Dudlová et al. 2016; Pipiková et al. 2017; Rudohradská et al. 2012). Recent studies also indicate that STHs are predominantly found among the Roma population. For example, a survey conducted across 32 segregated villages and settlements in Košice and Prešov self-governing regions of eastern Slovakia in 2020 found a prevalence of 27.4% and 2.3% for A. lumbricoides and T. trichiura, respectively, among 259 Roma children aged between 7 months and 18 years (Papajova et al. 2021).

26

J. M. Kurscheid

An earlier study among 426 children (Roma and non-Roma) aged 0–18 years, also in Košice and Prešov, found a prevalence of A. lumbricoides of 14.3% and 3.8% for T. trichiura (Pipiková et al. 2017). Among the Roma children, more than one-quarter (n ¼ 71/275) were positive for at least one helminth species (which also included Hymenolepis nana and H. diminuta). In comparison, only a single non-Roma child (n ¼ 1/151) was found to be infected with any helminth parasite (Pipiková et al. 2017). Further highlighting the contrast in STH prevalence between Roma and non-Roma populations is a study of 2760 people (no specific ethnic groups) from the eastern, western and central regions of Slovakia. This 2016 study was one of the largest epidemiologic surveys undertaken in Slovakia in the last decade (Dudlová et al. 2016). The findings revealed a prevalence of 0.8% for T. trichiura and 3.7% for A. lumbricoides. However it should be noted that this study population covered a wide range of ages (1 month to 88 years). Although the prevalence of A. lumbricoides was quite low, it was the most common parasitic infection from a spectrum that also included protozoa and various helminth species. In terms of geographic distribution, Eastern Slovakia recorded the highest prevalence of parasitic infections (Dudlová et al. 2016). In Slovakia, monitoring of the current epidemiologic situation of infectious diseases in the human population occurs through the ‘The Epidemiological Information System’ (EPIS) of the Public Health Authority. However, this system does not include information on the incidence of STH and in terms of parasites, only covers toxoplasmosis and taeniasis (Dudlová et al. 2016).

7.6

Moldova

Moldova is the poorest country in Europe (The World Bank 2021c). A survey of water and hygiene conditions in educational institutions (referred to as schools below) by UNICEF in 2009 revealed that access to tap water was very limited, both in the home and in schools (Steinmann 2013). Water quality was deemed to be very poor and daily supply interruptions were common. Sanitation and handwashing facilities were also determined to be unsatisfactory in many schools. More than half of all students did not have access to indoor toilets and nearly a quarter of all schools had toilets that were of unsatisfactory sanitary-technical condition. Approximately three quarters of the schools had no handwashing facilities close to toilets, and soap and toilet paper were often not available. Only about a quarter of students reported washing hands before eating. More recent data suggest improvements have been made with regard to access to water and sanitation. In 2018, it was reported that 97.3% of urban and 45.1% of rural populations and 85% of kindergartens and schools had access to safely managed water (Anonymous 2019). Access to improved sanitation has also increased due to the combined efforts of the national government and international donors (Anonymous 2019).

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

27

A nationwide intestinal helminth survey covering 534,506 people including 259,007 children aged 0–17 years that was conducted in 2011, found a low STH prevalence (Steinmann 2013). A. lumbricoides prevalence was 0.8% among the total cohort and 1.5% among children. An overall prevalence of 0.02% was identified for T. trichiura and among children the prevalence was 0.02% (Steinmann 2013). Subsequently, in 2012, Moldova (along with Romania and Turkey) was removed from the list of countries requiring preventive chemotherapy for STH control (Anonymous 2014). The low prevalence of STH in Moldova is likely a result of the clear legal framework for the diagnosis and control of intestinal helminths, comprehensive intestinal helminth surveillance, and control interventions including large-scale screening for infections, regular mass drug administration to selected population subgroups, wide availability of deworming drugs, and regular health education in schools (Steinmann 2013).

7.7

Romania

Romania is one of the poorest member states of the European Union and has a predominantly rural population. Access to safe water, adequate sanitation infrastructure, and health and social services are often limited in rural or remote areas (Steinmann and Samwel-Mantingh 2013b). Although Romania has the tools and capacity to control STH infections, there is no specific legislation comprehensively regulating the surveillance, diagnosis, treatment, and control of STH infections and in general helminth infections are not prioritized (Steinmann and Samwel-Mantingh 2013b). Hookworm, which is virtually eliminated, is the only notifiable intestinal helminth infection. There are almost no current data on the epidemiology of STH in Romania. A review of human parasitic diseases in Romania from 2011 reports that in the past, ascariasis was frequently detected at prevalences ranging from 1% to 69% (Neghina et al. 2011). The most recent estimates for A. lumbricoides are from 2011 and indicates a very low overall prevalence of only 0.24% (Steinmann and SamwelMantingh 2013b). Trichuris suis is believed to be widely endemic but also at a low prevalence. S. stercoralis is more common with prevalences up to 16%, particularly in the North and Western Transylvania (Steinmann and Samwel-Mantingh 2013b). The lack of large-scale surveys and routine screening means the true epidemiologic status of STH in Romania remains unknown.

7.8

Albania

Albania is a small country located in south-eastern Europe. Poverty, overcrowding in urban areas and peri-urban slums with no sanitation, improper waste management,

28

J. M. Kurscheid

and poor infrastructure have facilitated the transmission of STH in the past. Water supply was decentralized in the early 2000s and there were issues with wastewater treatment across the country (Anonymous 2009). Over the past decade there have been significant improvements in living standards, although poverty remains widespread (The World Bank 2019). Priority has also been placed on improving WASH conditions, often with the support of international donors. Data on STH prevalence in Albania are scarce and most recent data are from 2008 when a cross-sectional survey of 321 children from the counties of Tirana and Elbasan found an overall prevalence of 8.1% (Sejdini et al. 2011). Hookworm was the most common species detected at 5.6%. A. lumbricoides and T. trichiura were both detected at low prevalence (1.9% and 0.6%, respectively). These figures contrast findings from a study carried out just 3 years earlier among 277 healthy subjects, aged 1–72 years, from the city of Mamurras, which reported a prevalence of T. trichiura of 12.3%, whilst the prevalence of A. lumbricoides was 1.1% (Spinelli et al. 2006). This is one of the few studies from European region countries that has reported a higher prevalence of T. trichiura than A. lumbricoides in the last two decades. At the time of the study, it was reported that there were no water or wastewater treatment plants in rural areas of Albania, meaning sewage was discharged into the environment (including directly into rivers, lakes and seas) untreated (Spinelli et al. 2006).

8 Strongyloidiasis in Central Asia and Europe The reported prevalence of human strongyloidiasis has seen a steady increase in recent years, especially in southern, eastern, and central Europe (Puthiyakunnon et al. 2014). This is most likely due to improved diagnostic tests rather than changes in the true prevalence (Tamarozzi et al. 2019). A recent review of human strongyloidiasis in Europe identified a total of 20 countries all across Europe where S. stercoralis had been identified. The highest numbers were reported from Romania, Slovakia, Spain, Italy, and France, while most autochthonous cases have been reported from Spain (mostly in the Valencia region), Italy, and France (Ottino et al. 2020). The most comprehensive human S. stercoralis prevalence data are available from a recent study by Buonfrate and co-authors in 2020. The overall prevalence was 2.8% for the European region (including Central Asia). Country level prevalences ranged from 0–10%: relatively high prevalences were calculated for Albania (8.0%), Armenia (6.5%), Azerbaijan (5.8%), Belarus (6.5%), Bosnia and Herzegovina (9.4%), Bulgaria (6.3%), Croatia (8.6%), Cyprus (2.8%), Czech Republic (4.5%), Estonia (4.1%), Georgia (10.0%), Hungary (4.9%), Kazakhstan (3.3%), Kyrgyzstan (6.5%), Latvia (5.1%), Lithuania (5.0%), Macedonia (6.7%), Poland (5.0%), Moldova (6.2%), Romania (6.1%), Slovakia (6.0%), Slovenia (7.3%), Tajikistan (7.8%), Turkey (5.6%), Turkmenistan (3.9%), Ukraine (6.6%), and Uzbekistan (4.7%). Countries with 0–1% prevalence included Austria, Belgium, Denmark, Finland,

Soil-transmitted Helminthiasis in Europe and Central Asia: An Update on. . .

29

Germany, Greece, Iceland, Ireland, Italy, Luxemburg, Malta, Netherlands, Norway, Portugal, Spain, Sweden, Switzerland, and UK (Buonfrate et al. 2020).

9 Discussion The data presented in this chapter indicate that ascariasis is the predominant traditional STH species and persists across Central Asia, parts of Eastern and Central Europe, and in the Caucasus. Overall prevalence of A. lumbricoides was highest among central Asian countries, particularly in Tajikistan (16.9–54.2%) and Kyrgyzstan (26.4–54.4%) according to data collected 10 or more years ago. Among the European countries, Slovakia was found to have the highest prevalence of A. lumbricoides infections, with a focus on the Roma populations (25–27.4%). In the general population, prevalence was lower (3.7%). Also noteworthy, Slovakia and Moldova were the only countries where recent national prevalence data were available. A. lumbricoides prevalence was very low in Albania and Romania but higher in Georgia and Uzbekistan. Albania was unique among the countries in that it was the only one to report higher prevalence of T. trichiura (12.3%) and hookworm (5.6%) compared to A. lumbricoides (1.1–1.9%). In contrast to other STH species, S. stercoralis appears to be widespread across most of Europe as well as Central Asia and the Caucasus, albeit at relatively low prevalence generally