Safety and Practice for Organic Food 9780128120606, 0128120606

Table of contents :
Content: Organic Food Products, Diverse Production Practices, and Policies 1. The Growing Market of Organic Foods: Impact on the US and Global Economy 2. Organic Farming Practices: Integrated Culture Versus Monoculture 3. Governmental Policies and Regulations including FSMA on Organic Farming in the United States and Around the Globe 4. Major Issues and Limitations in Organic Farming in the US Quality and Safety Concerns of Organic Food 5. A Nutritional Perspective: Importance of Organic Foods Over Conventional Counterparts 6. Listed Foodborne Disease Outbreaks Associated with Organic Foods: Animal and Plant Products 7. Food Safety Risks and Issues Associated with Farming and Handling Practices for Organic Certified Fresh Produce 8. Proper Farm Management Strategies for Safer Organic Animal farming practice 9. Effective farm management strategies for organic produce and plant food production 10. Alternatives to pest and disease control in pre-harvest, and washing and processing in post-harvest levels for organic produce Recommendations and intervention for Improving Safety and Sustainable Organic Food 11. The Plant Microbiome: Diversity, Dynamics and Role in Food Safety 12. Control strategies for post-harvest microbiological safety of produce during processing, marketing and quality measures 13. Control strategy for post-harvest microbiological safety of animal products during processing, marketing and quality measures 14. Future of organic farming: bringing technological marvels to the field 15. Pectin as an alternative feed additive and effects on microbiota 16. The impact of grower training on food safety outcomes 17. Acceptable alternatives growth promoters for organic farm animal production 18. Application of bacteriophages in organic farm animal production 19. Bio-control for foodborne zoonotic pathogens in animal reservoirs and food products

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SAFETY AND PRACTICE FOR ORGANIC FOOD

SAFETY AND PRACTICE FOR ORGANIC FOOD Edited By

DEBABRATA BISWAS SHIRLEY A. MICALLEF

Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1650, San Diego, CA 92101, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, United Kingdom © 2019 Elsevier Inc. All rights reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher. Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions. This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein). Notices Knowledge and best practice in this field are constantly changing. As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary. Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library ISBN 978-0-12-812060-6 For information on all Academic Press publications visit our website at https://www.elsevier.com/books-and-journals

Publisher: Susan Dennis Acquisition Editor: Anita A Koch Editorial Project Manager: Emily Thomson Production Project Manager: Vignesh Tamil Cover Designer: Christian Bilbow Typeset by SPi Global, India

Contributors Juhee Ahn College of Biomedical Science, Department of Medical Biomaterials Engineering, Kangwon National University, Chuncheon, Republic of Korea

Maheswaran Easwaran College of Biomedical Science, Department of Medical Biomaterials Engineering, Kangwon National University, Chuncheon, Republic of Korea

Solmaz Alborzi Department of Nutrition and Food Science, University of Maryland, College Park, MD, United States

Angela M.C. Ferelli Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, United States

Sarah M. Allard Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, United States

Sarah Frail Department of Cell Biology & Genetics, College of Computer, Mathematical, & Natural Sciences, University of Maryland, College Park, MD, United States

Md. Latiful Bari Center for Advanced Research in Sciences, University of Dhaka, Dhaka, Bangladesh

Seon-Woo Kim University of Maryland, College Park, MD, United States

Luis J. Bastarrachea Department of Nutrition, Dietetics and Food Sciences, Utah State University, Logan, UT, United States

Sun Ae Kim Department of Food Science, University of Arkansas, Fayetteville, AR, United States

Elizabeth A. Bihn Department of Food Science, Cornell University, Geneva, NY, United States

Sang In Lee Department of Food Science and Technology, Oregon State University, Corvallis, OR, United States

Debabrata Biswas Department of Animal and Avian Sciences; Center for Food Safety and Security Systems; Department of Molecular and Cellular Biology, University of Maryland, College Park, MD, United States

Sun-Ok Lee Department of Food Science, University of Arkansas, Fayetteville, AR, United States Shirley A. Micallef Department of Plant Science and Landscape Architecture; Centre for Food Safety and Security Systems, University of Maryland, College Park, MD, United States

Chitrine Biswas Department of Molecular and Cellular Biology, University of Maryland, College Park, MD, United States Amber Brauer University College Maastricht (UCM), Maastricht University, Maastricht, the Netherlands

Byungjick Min Department of Food Science, University of Arkansas, Fayetteville, AR, United States

Gerald E. Brust University of Maryland, Upper Marlboro, MD, United States

Abhinav Mishra Department of Nutrition and Food Science, University of Maryland, College Park, MD, United States

Donna P. Clements Department of Food Science, Cornell University, Geneva, NY, United States

Tagelsir Mohamed Raleigh District Office, Food Safety and Inspection Services, United States Department of Agriculture, Trenton, NJ, United States

P.G. Crandall Department of Food Science, University of Arkansas, Fayetteville, AR, United States

ix

x

CONTRIBUTORS

Joy Mun Howard High School, Ellicott City, MD, United States

Natural Sciences, University of Maryland, College Park, MD, United States

Vinod Nagarajan Department of Animal and Avian Sciences, University of Maryland, College Park, MD, United States

Sultana Solaiman Department of Plant and Landscape Architecture, University of Maryland, College Park, MD, United States

Hao Pang Department of Nutrition and Food Science, University of Maryland, College Park, MD, United States

Zajeba Tabashsum Department of Animal and Avian Sciences, University of Maryland, College Park, MD, United States

Si Hong Park Department of Food Science and Technology, Oregon State University, Corvallis, OR, United States

Rohan V. Tikekar Department of Nutrition and Food Science, University of Maryland, College Park, MD, United States

Mengfei Peng Department of Animal and Avian Sciences; Biological Sciences Program— Molecular and Cellular Biology Concentration, University of Maryland, College Park, MD, United States

Thomas Tran Department of Biology, College of Computer, Mathematical, and Natural Sciences, University of Maryland, College Park, MD, United States

Abani K. Pradhan Department of Nutrition and Food Science; Center for Food Safety and Security Systems, University of Maryland, College Park, MD, United States Aishwarya Pradeep Rao School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ, United States Sadhana Ravishankar School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ, United States S.C. Ricke Department of Food Science, University of Arkansas, Fayetteville, AR, United States Serajus Salaheen Department of Animal and Avian Sciences, University of Maryland, College Park, MD, United States Patrick Shan Department of Mathematics, College of Computer, mathematical and

M. Nazim Uddin Bangladesh Agriculture Research Institute (BARI), Gazipur, Bangladesh Shifei Wang Changzhou Qihui Management & Consulting Co., Ltd, Changzhou, PR China Hongshun Yang Food Science and Technology Programme, c/o Department of Chemistry, National University of Singapore, Singapore, Singapore; National University of Singapore (Suzhou) Research Institute, Suzhou, PR China Xi Yu Food Science and Technology Programme, c/o Department of Chemistry, National University of Singapore, Singapore, Singapore; National University of Singapore (Suzhou) Research Institute, Suzhou, PR China Yuyan Zheng Food Science and Technology Programme, c/o Department of Chemistry, National University of Singapore, Singapore, Singapore; Food Science College, Shenyang Agricultural University, Shenyang, PR China

C H A P T E R

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The Growing Market of Organic Foods: Impact on the US and Global Economy Mengfei Peng Department of Animal and Avian Sciences, University of Maryland, College Park, MD, United States Biological Sciences Program—Molecular and Cellular Biology Concentration, University of Maryland, College Park, MD, United States

O U T L I N E 1 Introduction 2 The Growing Consumption Demand on Organic Foods 2.1 Role of Knowledge on Transition of Consumers’ Altitudes Toward Organic Foods 2.2 The Fact of a Growing Trend in Organic Purchasing 3 Production and Market Expansion of Global Organic Food Industry 3.1 The United States 3.2 Europe 3.3 Asia

Safety and Practice for Organic Food https://doi.org/10.1016/B978-0-12-812060-6.00001-5

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3.4 Oceania 3.5 Other Developing Regions

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4 Significant Organic Impact on Local and Global Economy 4.1 Organic Food Industry in Creation of US Job Market 4.2 Higher Cost and Price of Organic Products 4.3 The US Organic Trade on Economy

5 8 9 11 12 13

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14 14 15 15 15 16

5 Challenges and Future Directions

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6 Conclusion

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References

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# 2019 Elsevier Inc. All rights reserved.

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1. THE GROWING MARKET OF ORGANIC FOODS: IMPACT ON THE US AND GLOBAL ECONOMY

1 INTRODUCTION Organic agriculture has been systematically developed over the last 70 year since the 1940s when J.I. Rodale, the father of modern organic farming movement, founded the first research institute for organic farming and gardening. Apparently, the recent market expansion of organic food products has been fueled by research as well as consumer demand. The amount of organic research funding, the number of certified cost-share operations, and other organic expanding programs and services have dramatically increased since 2000. Simultaneously, the national organic program (NOP) and standards, the federal regulatory framework governing organic food products, were sealed and published in the Federal Register (2000). As a matter of fact, research and policy initiatives by government, for example, the United States Department of Agriculture (USDA), has served as a crucial factor in enabling the adoption and maturation of new farming technologies and systems. On the other hand, the enlargement of the organic market is also driven by a growing demand from consumers with concerns about conventional food safety, personal health, and environmental contamination issues (Kearney, 2010). Annual double-digit consumer climb in the certification of organic food products has provided US farmers opportunities in organic agricultural and marketing across a variety range of products, although organic products still have considerable price premiums over traditional food products in market sales (Baudry et al., 2017). Consequently, US organic sales reached a significant milestone in 2015 with total product sales hitting $43.3 billion, which amounts to an 11% increased compared to 2014 ( Jaenicke and Demko, 2017a). Organic product sales account for approximately 5% of all food sold in the United States, which had a 1% increase over the value in 2012. Specifically, certain much weightier shares were found in consumers’ lifestyle product categories. For instance, organic produce (especially fresh juices and drinks) and dairy products are the biggest organic food categories driving the market, and they together account for more than 50% of the total organic product sales (Greene and Dimitri, 2002). Moreover, as the fastest growing sector of the US food industry, organic agricultural hotspots in the northeastern, north central, and western United States also lowers the county’s poverty levels by at least 1.35%, notably improving the median household annual income by more than $2000, which is a much greater rate than traditional agricultural systems ( Jaenicke and Demko, 2017b). Apart from the United States, Germany, France, China, Switzerland, Luxembourg, etc. also contribute to global sales of organic food products. According to Willer (2017a), global organic sales climbed over $80 billion in 2015, and more than 90 countries worldwide now systematically develop organic regulations. More than 2.3 million farms and producers are becoming involved in organic production and marketing from 172 countries, among which India, Uganda, and Mexico stand out in numbers of producers, whereas Australia, Argentina, and the United States stand out in terms of agricultural area (Willer, 2017a), although worldwide certified organic farmland remains at less than 2% of the total farmland under production. Specifically, in Europe and Oceania, governments in most countries including Denmark, Italy, Switzerland, Ukraine, Australia, and New Zealand have promoted a quick switch from conventional food production systems to organic systems, further lowering organic products’ prices to support the development and expansion of the organic market. However, for Asian countries, the consumption of organic foods and drinks is rising rapidly, whereas organic

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mass production is still limited; its system as well as the market is not mature enough. Therefore the imbalance between demand and supply stimulated the expansion of organic imports such as dairy and meat products from Europe, Australia, and the United States ( Jaenicke and Demko, 2017c). In consideration of the increased health concerns about pesticides, antibiotics, and genetic modification applied in food products, as well as the burgeoning popularity of organic agricultural production based on scientific research, perceived health benefits, and government encouragement, consumers are keeping their minds open and demanding to purchase organic foods ( Jaenicke and Demko, 2017d). Correspondingly, demand, production, and the market act as a triangle that support each other and together improve the whole organic system. According to a report from FMCG and Retail (2013), the organic food market in the United States is predicted to grow at the Compound Annual Growth Rate of around 14% from 2014 to 2018. In this chapter, we will address the expanding research and certification of organic foods, the growing consumption demand accompanying extended organic production, and finally the impact of organic market expansion on the US and global economy.

2 THE GROWING CONSUMPTION DEMAND ON ORGANIC FOODS During recent years, studies and investigations have been focused on purchasing demand and buying habits of organic foods. Although detailed results and outcomes from this research vary, the key conclusion is definite: there is an accelerated growing trend in organic demand and purchasing. Consumers nowadays take societal issues such as health concerns, environmental protection, and food safety into their buying considerations, which has induced the quick development of green and organic markets regardless of the established higher price premiums of organic products in the marketplace (Bhattacharya and Sen, 2004; Moisander, 2007; Groening et al., 2009; Pagiaslis and Krystallis-Krontalis, 2014; Nielsen, 2015). Moreover, organic food products have shifted from serving as an exotic and decadent dining option for a small percentage of people to becoming a more commonplace option for a majority of US households.

2.1 Role of Knowledge on Transition of Consumers’ Altitudes Toward Organic Foods On behalf of the rapid development of organic food culture, and with concerns about traditional farming system on human health, environmental sustainability, and animal welfare, there is a pervasive public belief that organic food products are more nutritious, safe, and tasty (White and Duram, 2013). Stimulated by the organic food industry, the organic labels in the market nowadays are symbols of foods that are healthful and nutrient-dense (Magkos et al., 2006). The higher prices and smaller scale of organic production have led to consumers considering organic foods as superior products, although there is little scientific and direct evidence proving their superiority in nutrition, taste, or any other healthpromoting benefits (Dangour et al., 2009; Schuldt and Schwarz, 2010; Blair, 2012).

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Negative factors including soaring prices, consumer’s lack of confidence, and ineffective marketing also influence the attitudes of consumers toward purchasing organic products (Tsakiridou et al., 2008; Aertsens et al., 2009; Ngobo, 2011; Akehurst et al., 2012; Bickart and Ruth, 2012; Tucker et al., 2012; Gleim et al., 2013; Atkinson and Rosenthal, 2014). However, healthy eating remains the top priority among current consumers and plays a significant role in overshadowing the previously described negative connotations associated with organic foods (Akehurst et al., 2012; Nielsen, 2015; Van Doorn and Verhoef, 2015; HidalgoBaz et al., 2017). In general, potential influence of environmental protection, health benefits, better taste, and satiety orientations, combined with common knowledge about organic products, determined consumers’ decisions in selecting organic foods and their willingness to pay higher prices (Barnes et al., 2009). 2.1.1 Biodiversity and Wildlife Welfare As the core principle of organic production, natural resources and biodiversity conservation could highlight the organic ideal (USDA, 2016). Despite concerns about food safety, consumers also care about environmental issues. Organic production, by utilizing sympathetic management of noncropped habitats, restricting synthetic pesticides/fertilizers, and applying a mixed farming system, offers multiple benefits to the environment and wildlife (Hole et al., 2005; Fließbach et al., 2006). Such advantages include the conservation of biodiversity, improving soil quality, attracting beneficial insects by weed species, stimulating pollination, and providing habitats for birds and small mammals (Van Elsen, 2000; Perrings et al., 2006). Apart from birds and small mammals, organic farms have approximately 30% higher species diversity such as spiders, earthworms, beetles, butterflies, and soil microbes than conventional farms (Bengtsston et al., 2005; Gabriel et al., 2006). Specifically, the rich soil microbiome of organic farms has been suggested to assist in the higher yields of organic plots by breaking down soil chemicals, plant matter, and animal wastes into beneficial nutrients (Fließbach et al., 2006; Horne and Page, 2008). 2.1.2 Consumer Safety The most substantial differences between conventional food products and organic food products lie in the diversified substances utilized in traditional food production systems, which are prohibited in organic systems. In general, organic standards by NOP only allow the use of naturally occurring substances, and synthetic items such as pesticides, antibiotics, hormones, synthetic fertilizers, growth regulators, and genetically modified organisms are strictly restricted (Paull, 2011a; USDA, 2012). Therefore in theory, organic food products are supposed to contain fewer artificial ingredients, such as pesticide and antibiotic residues and food preservatives, than their conventional food counterparts, and this is where the most positive perception comes from among organic purchasers (Peng et al., 2014; Salaheen et al., 2014). Organic food products properly relieve the concerns of artificial residues of consumers as well as farmers. For instance, farmers do not have to worry about the serious adverse health effects induced by massive exposure to pesticides; consumers could entirely avoid the acute toxicity caused by food contamination with pesticides. However, little scientific evidence can sufficiently support that organic foods are safer because the variable nature of food production systems and handling processes complicate the study and data generation

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(Blair, 2012; Smith-Spangler et al., 2012). As a matter of fact, in terms of organic food microbiological safety, multiple reports have claimed that organic food consumption is connected with an increased risk of bacterial contamination (Bourn and Prescott, 2002; Magkos et al., 2006). The increase in outbreaks of foodborne bacteria might not be particularly linked with organic food production, whereas the application of manure fertilizer and restricted use of antibiotics are among the biggest risk-inducing factors (Peng et al., 2016, 2018; Salaheen et al., 2016, 2017; Teramoto et al., 2016). 2.1.3 Nutritional Value Variations in cultural season/weather, crop fertilizer/pesticide treatments, soil composition, and transportation/storage conditions all have an influence on the chemical composition of organic foods, which causes a difference in nutrient values between organic and conventional food products (Bara
nski et al., 2014, 2017). As organic foods become more and more popular, people prefer to purchase these food products as a healthier option. However, it is still too early to draw a final conclusion, as scientists have found no consistent results in field research. Several negative or neutral results may refute the claim previously mentioned by some market drivers such as print media and social media, but it is uncertain if they will have an impact on the popularity of organic foods among current consumers who have already accepted that “organic” equals “nutritious.” The 2009 systematic review found only insignificant lower nitrogen and higher phosphorus content in organic produce, but no difference in content of vitamin C and major elements, including calcium, copper, iron, magnesium, potassium, and sodium, compared with traditionally grown produce (Smith-Spangler et al., 2012). The 2012 scientific survey failed to find notable differences in vitamins (such as ascorbic acid, betacarotene, alpha-tocopherol, and retinol), proteins, or fat content between organic and conventional animal products and produce (Hunter et al., 2011; Smith-Spangler et al., 2012). Finally, the 2016 metaanalysis found that, although organic meat and milk products had significantly higher levels of overall and n-3 polyunsaturated fatty acids, they contained only comparable or even slightly lower content of saturated and monounsaturated fat (SrednickaTober et al., 2016a,b). 2.1.4 Hedonic Orientations As indicated by some previous research (McEachern and McClean, 2002; Cervellon and Carey, 2014), a vast group of consumers perceive that organic food products could provide a better visual appearance, scent, and taste. To be specific, McEachern and McClean (2002) suggested that consumers were more willing to link a perception of better flavor with organic products, because this notion served as the primary factor in organic purchasing. Recently, Cervellon and Carey (2014) also pointed out that, in postpurchase assessments, most consumers evaluated the hedonic attributes such as visual appearance, scent, or texture more positively instead of the price, despite the fact that no convincing evidence shows organic foods taste better than traditional food counterparts. Blair (2012) presented one suggestion that some organic fruits are normally drier than conventionally grown fruits due to their difference in farming environments and irrigation systems. Therefore the slightly drier organic fruits might provide consumers with a more intensive flavor due to a higher concentration of their flavoring components (Blair, 2012).

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Furthermore, ripeness of picked fruits always has an influence on taste. For example, organic bananas are usually harvested unripe, and then they are rapidly induced to ripen once shipped into the market with propylene or ethylene exposure, which might alter the flavor as well as texture (Magkos et al., 2003; Hunter et al., 2011; Smith-Spangler et al., 2012).

2.2 The Fact of a Growing Trend in Organic Purchasing The Organic Trade Association (OTA) has revealed that more than 75 million US Millennials now prefer organic foods, accounting for approximately 52% of all US organic buyers. These buyers also encourage their families to do so. The biggest organic purchaser group in the United States is 18- to 34-year-old parents ( Jaenicke and Demko, 2017d). Nielsen (2015) conducted a nationwide comprehensive study from 2015 to 2016. Common organic food products were found in kitchens of most American households across the country, including both urban and rural areas. In this state-by-state representative study, 82.3% of 100,000 households participated in organic food purchasing, and their 2016 purchasing behaviors grew by 3.4% compared to the previous year. According to Nielsen’s study, most US households buy organic products on a regular basis, and the ratio of organic purchasing is variable but ranges from 69% to 92% (Fig. 1). Washington, Oregon, Arizona, California, Colorado, and Wyoming rank as the top six states in household organic purchasing with more than 90% organic purchasing. Moreover, North Dakota, Rhode Island, Wyoming, South Dakota, and Wisconsin are the top five states showing the biggest rise in household organic purchasing with a 14.2%, 12.3%, 10.8%, 10.0%, and 9.1% increase, respectively, when compared with previously reported organic purchases (Nielsen, 2015). The US Households Organic Purchasing Ratio 95%

90%

Percentage

85%

80%

75%

65%

WA OR AZ CA CO WY NH UT ID RI VT CT TX ND MA MD MT NV MI NM VA FL GA NJ NY IL ME KS MN OH IN KY PA TN WI NC MO DE NE WV SC AR LA OK AL IA MS MS SD

70%

State

FIG. 1 The US household’s organic purchasing ratio during years 2015–16.

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As a matter of fact, back in 2000–01, several industry groups investigated the preferences for organic foods of consumers and found that organic products had already started to become popular among US shoppers. It was reported by The Nutrition Business Journal (NBJ) that 11% of consumers purchased organic food in 2000; the Hartman Group reported 3% of consumers regularly bought organic food products in 2000; and furthermore, in 2001, 63% of respondent shoppers occasionally and 57% purchasers continually purchased organics for at least 3 years, according to the Walnut Group (NBJ, 2004, 2010). These significant findings display the importance and popularity of organic food products among US households, and that organic food has become the consuming diet trend of a majority of the US families. As Laura Batcha, CEO and Executive Director of OTA, pointed out, organics are expected to lead a healthy trend and keep leading it stronger and longer in the future.

3 PRODUCTION AND MARKET EXPANSION OF GLOBAL ORGANIC FOOD INDUSTRY Despite decelerated growing of the global economy, the global organic industry and market sales are steadily and gradually rising (Greene and Dimitri, 2002; Cunha and Pinto de Moura, 2004). Although organic farm practices are becoming attractive and trendy all over the world, the main demand for organic food products comes from North America and Europe. The organic markets of these two continents account for approximately 96% of the entire global organic market ( Jaenicke and Demko, 2017a). The rapid growing demand leads to highly focused, massive production, and further induces greater supply than the actual demand. As a matter of fact, oversupply has already existed in European organic markets, and the consistency between supply and demand will be unbalanced in the long term. Based on data from Forschungsinstitut f€ ur biologischen Landbau (FiBL), Figs. 2–4 in this chapter show the global organic agricultural farmland sizes, producers, and retail sales in 2015 (Willer, 2017a,b). Distribution and Growth of Global Organic Agricultural Farmland 24.0 22.0 20.0 18.0

Million hectares

16.0 14.0 12.0 10.0 8.0 6.0 4.0 2.0 0.0

Year

FIG. 2 Distribution and growth of global organic agricultural farmland for 2015.

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Distribution and Major Regions of Global Organic Producers 1%

1%

Itay Paraguay Turkey Peru Tanzania

19%

Philippines Uganda Mexico 30% Ethiopia India 0

100,000

200,000

300,000 Numbers of producers

400,000

500,000

600,000

FIG. 3 Distribution and major regions of global organic producers for 2015.

Global Retail Sales Share of Organic Food Products 25%

75%

China

Asia 8%

Oceania 2%

Others 0.10%

Others

Germany 10%

France

4% 29%

4%

North America 51%

Switzerland 6%

Sweden Spain

7% The United States Canada

The United Kingdom Italy

5%

18% 8%

Others

9%

0.10%

Denmark Netherlands Others

8%

92%

Europe 39%

FIG. 4 Global retail sales share of organic food products for 2015.

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3.1 The United States In the United States, organic food is one of the fastest growing agricultural industries, and the size of its domestic organic food market is gradually expanding (FMCG and Retail, 2013, 2015). As the variety of organic food products grows, the ways of selling organic foods has also become varied. Nowadays, people can purchase almost all kinds of organic food products, even from nonorganic food sales channels, and organic cereals, fruits, vegetables, wines, syrup, nuts, and spices markets have already been developed well in a proper scale. Also, organic tomato sauce, oil, cereals, and frozen vegetables are among the relatively rapiddeveloping categories of organic products ( Jaenicke and Demko, 2015a, 2017d). In the field of organic agriculture and marketing, the fastest expanding products might be organic eggs, milk, yogurt, cheese, and other series of dairy products (Willer, 2017a). Due to the increasing request for vitamin production and food ingredients, the market growth rate of organic Chinese herbal medicines, either wild or artificial, is expeditious. At the same time, the market for organic cotton is also expanding because of rising public demand for organic cotton-processed clothes, bedding, and other products (Winter and Davis, 2006; Crowder and Reganold, 2015; Jaenicke and Demko, 2017a). Since the beginning of organic food retail more than 3 decades ago, fresh vegetables and fruits have remained at the top of organic food sales (NBJ, 2004, 2010). To be specific, in 2012, produce accounted for 43% of the total US organic food sales, which was followed by dairy products (15%), packaged and specially processed foods (15%), beverages (11%), bread and grains (9%), snacks (5%), meat products (3%), and condiments (3%) (NBJ, 2004, 2010). According to OTA statistics, the vast majority of organic food (93% of total organic sales) is mainly sold through traditional or natural food supermarkets and chain stores, whereas the other 7% is sold through direct marketing channels such as farmers’ markets, restaurants, and nonretail markets ( Jaenicke and Demko, 2017a). According to a USDA follow-up survey, the number of US agricultural chain markets was 1755 in 1994, but this number reached 8144 in 2013, which was a 5-time increase compared with 9 years ago ( Jaenicke and Demko, 2015a). The rapid development of organic agriculture in the United States was stimulated by the burgeoning demand for organic products from the European and Japanese organic markets (Winter and Davis, 2006; Crowder and Reganold, 2015; Lernoud and Willer, 2017). Although the United States is a major producer of organic agricultural products, the local organic food industry still relies on imports, especially from Latin America, Africa, Europe, and Australia. A lot of organic fruits, vegetables, meat, beans, seeds, vanilla, seasonings, and other food ingredients are imported annually to the United States ( Jaenicke and Demko, 2015b, 2017c). Moreover, Latin America remains a major supplier of organic products in North America. For specific instance, 25%–40% of the US organic consumption of all vegetables and fruits depends on imports, and more than half of its imported organic products are from Mexico ( Jaenicke and Demko, 2015a). According to the research report, the best potential market for organic foods that producers have yet to capitalize on demand are products like coffee, tea, cocoa, flavors, tropical fruits, and vegetables for export-oriented countries where the local producers are not willing or have failed to produce. In addition to the supply of the off-season market of fruits and vegetables in these countries, US organic export could also supply on-season organic fruits, vegetables, and other food products that are in short local supply ( Jaenicke and Demko, 2015b; Lernoud and Willer, 2017).

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In the near future, it could be imagined that the US organic market could keep expanding by 20% or more per year. The import demand for organic food is likely to grow continually, and the US organic market is predicted to gradually develop from an insignificant position to the mainstream of both domestic and worldwide trade (FMCG and Retail, 2013, 2015).

3.2 Europe European organic food production not only remains in the world’s leading position but also introduced the world’s largest organic food consumer market. According to the International Trade Center report, in 2001 the European organic food and beverage sales value was around $12 billion (Lernoud and Willer, 2017). Among European countries, Germany is the largest organic food consumer market, which accounts for more than one-third of the European organic food sales across the world, ranking second after the United States. In addition to Germany, other European countries with substantial organic food consumption and sales include France, the United Kingdom, the Netherlands, Switzerland, Denmark, and Italy (Willer, 2017b). In most markets, the share of organic food sales compared to the total value of food sales is about 1%, which is expected to rise to 5%–10% within the next few years (Willer, 2017b). The entire European organic food market is composed of 37% organic cereal products, 11% organic dairy products, 11% organic meat, and 41% all other organic products (Willer, 2017b). However, the exact values or weights vary among different European countries. For instance, the French organic food market was formed with 42% organic cereals, 25% organic fruits and vegetables, 2% organic wine, and 3% organic poultry meat products; whereas, in the UK food market, organic fruit and vegetables accounted for 54%, organic cereals accounted for 14%, and organic dairy products accounted for 7%. Yet for the organic food market in Denmark, organic dairy products accounted for as high as 45%, whereas organic fruits and vegetables only accounted for 17% (Lernoud and Willer, 2017; Willer, 2017a,b). European countries have laid the foundation for the development of organic trade by undergoing massive organic agricultural production. The main suppliers of organic markets in Europe are domestic producers, especially for dairy products, vegetables, fruits, and meat (Willer, 2017a). For France, Spain, Italy, Portugal, and the Netherlands, the exports of organic food products are greater than imports, yet the reverse case applies for Germany, the United Kingdom, and Denmark, among which 60%–70% of the organic food sales value of the United Kingdom depends on imports, and the value for Germany is about 50% (Willer, 2017b). There are still many kinds of food products, especially dry foods, that European countries do not produce or process, so they rely on imports from other countries around the world, including developing countries (Lernoud and Willer, 2017). Argentina is one of the main exporters of organic food to Europe, accounting for more than 70% of total imports in the European organic markets (Lernoud and Willer, 2017). The European organic traders are working closely with companies in North America and Africa to facilitate the domestic translation from traditional farming to organic farming. Furthermore, promoted by the growing demand for organic products, European traders are also continually seeking potential sources of organic products, which include coffee, tea, cereals, nuts, dried fruits, oilseeds, spices, sugar, etc. (Lernoud and Willer, 2017; Willer, 2017a,b).

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3.3 Asia Asian organic markets and trade are stably growing, but they could be ranked and distinguished based on the production and consumption levels of organic food products (Paull, 2011a). The overwhelming majority of organic products sales are observed in wealthy countries or regions, such as Japan, Korea, Malaysia, Singapore, and China (including Taiwan and Hong Kong). However, local production of organic food products accounts for only a small share, whereas a large part of organic foods, especially processed foods, are imported from organic-productive countries and regions like Australia, Europe, and the United States (Willer, 2017a). Organic food industries in Asian countries could be categorized as export-oriented and demand-oriented (Cunha and Pinto de Moura, 2004). Several countries, including the Philippines, Indonesia, Sri Lanka, and Vietnam, with little or negative domestic organic desires, directed their cultivation of organic crops for only export. However, there are some other countries where their organic crop cultivation is now designed to meet the demand of domestic markets. For example, India, China, and Thailand used to be traditional export-oriented countries but are undergoing the transition to demand-orientation in recent times due to their own everincreasing domestic demands. For such categories, the rapid development of their organic markets directly caused the large expansion of the organic food retailers (Paull, 2011a,b). Organic foods in Asia are heading for mainstream retailers, and recently organic food products have been on sale in large supermarkets, especially in prosperous cities. Unfortunately, as a junior member in organic markets, Asian countries lack fully established organic product standards, which impedes their development of organic product trade, to some extent (FMCG and Retail, 2015). Only a few Asian countries, such as Japan and China, have mandatory organic agriculture and food standards, whereas most Asian countries still do not have national or organic industrial standards, which makes it difficult for Asian domestic consumers to identify legitimate organic products on the market (Motomura, 2013; Chandran and Eunice, 2015). The Japanese Organic Agriculture Association initially introduced standards for organic agricultural production as early as in 1993, and it stimulated the development of organic agriculture by encouraging both organic production and consumption activities in substantial groups such as local governments and multiple agricultural associations (Motomura, 2013). At present, Japanese organic agriculture production accounts for more than 30% of the total national agricultural production, providing people with more than 130 kinds of organic foods, among which more than 40 kinds are exported to Europe and the United States ( Jaenicke and Demko, 2017a). The main sales of organic food products include processed soy products, especially soy sauce, frozen vegetables, fruit beverages, edible vegetable oil, tea, coffee, spices, rice, etc. From the point of view of Japanese market scale, Japanese organic food markets have dramatically expanded since 1995, and its organic food sales are growing speedily with an average annual growth rate of more than 10% (Motomura, 2013). It was predicted that, in the near future, Japan would become the largest organic food sales market in the world. As the fourth largest domestic organic market in the world, counting organically managed land, the volume of production, and organic consumption, Chinese organic food still only made up about 1%–1.5% of the entire Chinese food market in 2015 (Chandran and Eunice, 2015). According to the market report, approximately 10 million tons of organic goods were produced in China during 2013, among which 70% are provided to the domestic market

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1. THE GROWING MARKET OF ORGANIC FOODS: IMPACT ON THE US AND GLOBAL ECONOMY

whereas the remaining 30% is exported. Moreover, more than 1% (3.5 million hectares) of the total agricultural land in China was utilized and focused on organic production, especially concentrated in northeastern China and the coast (Chen, 2014; Willer, 2017a). Chinese organic exports, as a proportion of total sales, have increased by 19.5% reaching $250 million over the last 5 years (Chandran and Eunice, 2015). Among all export sales, around $195 million worth of business is derived from the top 10 countries including the United States, Germany, Netherlands, Canada, Japan, Switzerland, Belgium, the United Kingdom, and France (Chen, 2014). With $67 million in sales, soy and other bean products ranks first in worldwide export products, followed by tea, fruits, nuts, and vegetables, each generating about $22 million in sales. Therefore it is reasonably forecasted that, by 2020, China will potentially become the leading organic producer across the entire world. Moreover, the organic agricultural land will be composed of 1.2%–1.5% of total agricultural land, and the share of domestic and export organic food market will reach up to 3% and 1%–1.5%, respectively (Harney, 2014).

3.4 Oceania The organic markets of Australia, New Zealand, and the Pacific Islands are relatively small (Cunha and Pinto de Moura, 2004). Although the area of Oceania organic agricultural land accounts for more than 40% of the entire organic agricultural land in the world, its organic food sales share is less than 2% of worldwide sales. Nevertheless, both Australia and New Zealand are crucial countries for the production, consumption, and most importantly export of organic food products. A huge quantity of organic beef, lamb, wool, kiwi, wine, apples, pears, and vegetables are exported to Asian as well as European and North American countries every year. Moreover, being encouraged and stimulated by the Pacific Organic and Ethical Trade Community, the domestic organic markets of the Pacific Islands have continually grown from undeveloped and even nonexistent moving toward the goals articulated in the Strategic Plan 2013–2017 (Willer, 2017a).

3.5 Other Developing Regions The enormous and continually increasing demand for organic food, coupled with limited domestic organic production, has resulted in the reliance of western developed countries on imported organic goods (Cunha and Pinto de Moura, 2004). With a 20%–50% higher price premium on organic food products than conventional foods, international trade in organic foods is becoming more and more attractive for developing countries, as these countries may gain profits in a much efficient way. For instance, the export sale of organic food products (mainly fresh fruits and early-seasoned vegetables) in Israel accounts for 2%–3% of the total agricultural exports. Turkish figs, nuts, and dried fruits; Moroccan oranges; Indian tea; and bananas from Western Indian and Caribbean islands are also frequently exported to Europe and North America (Willer, 2017a). Although both organic food production and market development in developing countries are still in their infancy, they might have a brilliant future following the fierce momentum. Such example countries include Brazil, Chile, and Peru in Latin America; India, Indonesia, and Nepal in South Asia; and Kenya and Mauritius in Africa (Willer, 2017a).

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4 SIGNIFICANT ORGANIC IMPACT ON LOCAL AND GLOBAL ECONOMY Organically produced foods have become a popular option among consumers. It is undeniable that environment and food industry economics are tightly connected. The organic terminology and application are not only fulfilling the rapidly increasing demand of consumers but also offering job opportunities and intensively stimulating local and global economies.

4.1 Organic Food Industry in Creation of US Job Market The production transition from conventional agricultural methods to organic agricultural systems provides a contemporary job market in the United States. According to the recent economic study conducted by OTA’s Policy Conference, the US organic food industry has generated more than 500,000 domestic jobs during 2010, and for the first time, sales of the US organic market in the same year have surpassed $31 billion ( Jaenicke and Demko, 2017b). The OTA’s 2011 and 2012 Organic Industry Survey both directly and indirectly investigated organic-induced impacts on job markets throughout the United States by comparing them with parallel outcomes that would have occurred from the same amount of food sales generated by conventional food production and marketing systems (Haumann, 2012). With the analysis based on different food categories, including meat products, dairy products, produce, beverages, breads and grains, sauces and condiments, snacks, packaged and prepared foods, etc., the OTA estimated that, for every $1 billion organic retail sales, 21,000 more new jobs were established throughout the US economy. In comparison with the traditional food industry where products from conventional farm systems are merely ingredients, the utilization of organically produced ingredients had a momentous economic impact by creating 21% more positions in job market. Furthermore, organic farms hire an average of 61 employees per year in the United States, compared to 28 per year on conventional farms. Organic farms also offer more opportunities to seasonal workers than conventional farms. According to the 2011 report “Organic farming for health and prosperity,” 96% of organic operations in the United States maintained or raised their employment levels under the support of the federal government, making the most of their economic potentials (Haumann, 2012; Jaenicke and Demko, 2017b).

4.2 Higher Cost and Price of Organic Products Organic food products typically cost 10%–40% more than similar traditional food products for market price (Winter and Davis, 2006). According to Kathleen Elkins, a US inside-business writer who investigated the Whole Foods supermarket located near Manhattan residence areas in New York, customers would annually spend $26 more on 1 pound of strawberries; $10 more on 1 pound of bananas; $26 more on 1 pound of peaches; $26 more on 1 pound of onions; $26 more on each cantaloupe; $45 more on each avocado; $52 more on 1 pound of tomatoes; $110 more on 0.5 pound of pork bacon; $105 more on 4 pounds of chicken; $95 more on 1 dozen eggs; $25 more on 1 pound of bread; $70 more on 8 oz of crackers; $20 more on a can of black beans; $130 more on a jar of peanut butter; $365 more on a jar of almond butter; and $135 more on 1 gal of milk on organic compared to conventional products, if they buy

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1. THE GROWING MARKET OF ORGANIC FOODS: IMPACT ON THE US AND GLOBAL ECONOMY

TABLE 1 Premium Prices of Popular Organic and Regular Food Products Products

Regular ($)

Organic ($)

Difference

Apple (lb)

1.58

2.07

31.01%

Baby carrot (lb)

1.76

2.31

31.25%

Banana (lb)

0.66

0.84

27.27%

Butter (lb)

3.79

6.07

60.16%

Cream cheese (oz)

0.34

0.43

26.47%

Eggs (dozen)

3.10

5.15

66.13%

Honey (lb)

5.65

6.01

6.37%

Lean ground beef (lb)

5.96

9.06

52.01%

Lettuce (lb)

2.01

2.82

40.30%

11.47

13.37

16.56%

5.28

7.80

47.73%

Olive oil (quart)

11.74

13.64

16.18%

Strawberry (lb)

4.31

6.61

53.36%

Whole chicken (lb)

2.02

3.73

84.65%

Zucchini (lb)

1.30

2.33

79.23%

Maple syrup (pint) Milk (gallon)

such items once a week (Elkins, 2015). Although Elkin’s investigation is not enough to represent all organic food industry prices in the United States, it was reported that the average price of organic food is usually more than 25% higher than nonorganic food products (Kremen et al., 2004; Winter and Davis, 2006; Kowitt, 2015). Based on the consumer reports collected from select grocers, including Amazon Fresh, Fresh Direct, Harris Teeter, Peapod, Price Chopper, Safeway, Walmart, and Whole Foods, comparing organic goods in the market basket with their conventional counterparts, identical food items as well as the entire assortment were chosen for their average premium comparison (Table 1) (Kremen et al., 2004; Winter and Davis, 2006; Kowitt, 2015). Consumers of organic foods spend more on food products due to multiple factors such as substituting human labor and intensive management for chemical-clean production, overwhelming demand over supply, higher cost of organic fertilizers, sophisticated crop rotations, additional cost for postharvest handling, extra cost for organic certification, shorter storage time and shelf life of organic foods, extra cost for organic livestock welfare, and extra manpower, time, and patience required in organic production (Pretty et al., 2005; Magkos et al., 2006; Blair, 2012; Baudry et al., 2017).

4.3 The US Organic Trade on Economy As the largest organic market across the world, the United States represents more than 50% of the global consumer sales for organic food products. The continuous growing and maturation of the global organic industry has resulted in the increased importance of global A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

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4 SIGNIFICANT ORGANIC IMPACT ON LOCAL AND GLOBAL ECONOMY

organic trade with the United States. More than 179 countries are actively associated with organic food product production, and they are also linked with more than 2.4 million organic producers throughout the entire world (Willer, 2017a). From 2011 to 2016, the United States exported organic food products to more than 100 different countries worldwide, with export values around $505 million annually and a total $3.03 billion for 6 years ( Jaenicke and Demko, 2017c). Canada and Mexico, as the major recipients, accounted for more than 75% of US organic exports and produced $247 million and $134 million annual export values for the United States, respectively. Except for Canada and Mexico, countries including Japan, China, Australia, South Korea, United Arab Emirates, etc. were among the other 20 top recipients of US organic exports who imported an average of more than $5 million US organic food products per year, and all together accounted for more than 97% of total US organic exports ( Jaenicke and Demko, 2015a,b, 2017c). Similarly, during 2013–16, the United States imported organic food products from at least 100 different countries across the world. The market for organic produce in the United States was even larger than its exports. The United States generated an average $1.5 billion of organic imports value, thus a total $5.9 billion value for the 4 years ( Jaenicke and Demko, 2017c). The top organic import source country was Mexico who produced $144 million import share for the United States, accounting for approximately 10% of the entire annual value. Italy with an annual $137 million and Peru with $101 million import contributed to the United States following Mexico as the second and third most organic import organic sources ( Jaenicke and Demko, 2015a,b, 2017c). Table 2 shows the top countries that the United States has both exported and imported the most organic food products since 2013 ( Jaenicke and Demko, 2017c).

TABLE 2

Top Countries of Origin for the US Organic Trade, 2013–16 Organic Trade Values Imports

Exports

Country

Annual Average ($ million)

Canada

247.48

49.00%

Mexico

Mexico

134.73

26.68%

China

31.38

Japan

Share

Country

Annual Average ($ million)

Share

118.39

10.05%

Peru

92.95

7.89%

6.21%

Italy

92.85

7.88%

28.13

5.57%

Canada

58.74

4.99%

Australia

9.81

1.94%

Brazil

57.52

4.88%

South Korea

7.1

1.41%

India

56.83

4.82%

United Arab Emirates

5.82

1.15%

Colombia

56.17

4.77%

United Kingdom

4.63

0.92%

Argentina

55.33

4.70%

Saudi Arabia

3.11

0.62%

Spain

51.23

4.35%

Singapore

2.84

0.56%

Turkey

50.05

4.25%

All others

30.03

5.94%

All others

487.89

41.42%

505.06

100.00%

1177.95

100.00%

Total

Total

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1. THE GROWING MARKET OF ORGANIC FOODS: IMPACT ON THE US AND GLOBAL ECONOMY

5 CHALLENGES AND FUTURE DIRECTIONS The growth of the global organic food market is tightly connected with the shape of world economy. Despite the fact that the consumer demand for organic products continues to increase, the market growth rate has declined slightly since 2008. Taking the impact of European debt crisis and the US financial cliff into consideration, the future of the global economy is entirely uncertain. Therefore the recent advancement of the organic market might be relatively slowed down (Hamzaoui-Essoussi and Zahaf, 2012). The downturn in market expansion has brought many challenges, the most important of which is the disequilibrium between organic food industry supply and consumer demand (Kearney, 2010). Organic crops are produced all over the world, with the demand concentrated mainly in European and North American regions. Along with the slowdown of economies in European and North American markets, the oversupply of organic food products will have big impacts on organic farmers and suppliers in Africa, Asia, and Latin America. If organic producers transfer back to conventional cultivation due to limited domestic demand, they will experience a new round of supply shortages when Europe and North America recover from the shadow of economic crisis (Kowitt, 2015). Food inflation is another major challenge for the organic industry (Winter and Davis, 2006). In the United States, Russia, and Latin America, poor agricultural outcomes have led to a new round of raising food prices. Based on the original higher price premium of organic products, the rise in food prices impedes farmers’ shift from traditional cultivation to organic production. On the other hand, the growing popularity of biofuel crops is also competing with food crops for land resources, which also induces higher food prices (Kremen et al., 2004; Pretty et al., 2005). Standards and certification are still a continuing challenge. The current lack of harmonized standards remains an obstacle to global trade of organic food products. The United StatesEuropean agreement on mutual recognition of organic agriculture implemented in July 2012 is committed to stimulating interregional trade for organic products. However, organic products certified by other regions do not apply to this valuable agreement (HamzaouiEssoussi and Zahaf, 2012). In Asia, an increased number of countries have already developed or started to develop organic standards, whereas these standards do not have mutual recognition, and the organic crops’ requirement for multiple certification is still not well resolved (Hamzaoui-Essoussi and Zahaf, 2012). All of these problems have discouraged certain farmers and producers from organic agriculture and production. In addition, the trend of global organic food market development was also analyzed and the following has been predicted: First of all, the demand for high quality organic food will steadily grow. Major organic demand will be especially focused on organic products with higher market share such as fruits, vegetables, baby food products, raw materials for processed food, and dairy. The growth in organic demand is driven by the middle classes’ pursuit of healthy foods and environmental sustainability. The needs for organic food products with a high potential for market expansion, including convenient foods, frozen foods, candies, and catering services, will be rapidly encouraged and boosted. The main force of organic frozen food product purchasers will be the next generation of consumers, with their current age between 20 and 30 years old. Single people, who are mostly highly educated, with an average or higher income, and who prefer both tasty and healthy food products, are also another main driver of the organic market. A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

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The organic market will become ubiquitous with affordability as the demand and supply buffer the initial costs of organic products. As a matter of fact, certain discount stores and supermarket chains have already introduced fresh organic foods on sale. The harmonization between different regulatory bodies overseeing organic food production will result in more certified establishments fulfilling consumers’ organic demands.

6 CONCLUSION Since the beginning of the 20th century, especially since the 1970s, rapid development of organic agriculture/ecological agriculture in Europe, the United States, Japan, and some developing countries, especially China, has occurred. These movements have been driven by the motivation of environmental protection and safe agricultural production. By the end of the 1990s, Europe, the United States, and Japan had turned into the major markets for ecofeatured agricultural products across the world. Export-oriented organic agriculture in developing countries also grew rapidly, as well as the domestic market gradually formed, with the driving force from the development of a local economy. Since the 1990s, organic farming production and trade have accounted for nearly 1% of the total food system. Organic food demand, production, and market have expanded specifically faster in regions where intensive sense of environmental protection is immersed, such as Europe, Japan, and the United States. In the context of the decelerated global economic growth, sales of international organic food products are still rising at a steady pace. The demand for global organic products is mainly concentrated in North America and Europe, whose market demand accounts for 96% of the global organic market. Despite the challenges in the near future, with the economic contribution from the organic sector, the organic food market will continue to expand aggressively, and the global organic food industry is still encouraging and promising, even under the current economic downturn circumstances caused by global economic crises.

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Jaenicke, E.C., Demko, I., 2017b. U.S. organic hotspots and their benefit to local economies. Report to the Organic Trade Association, https://www.ota.com/hotspots. Jaenicke, E.C., Demko, I., 2017c. U.S. organic trade data report: 2011 to 2016. Report to the Organic Trade Association, https://ota.com/sites/default/files/indexed_files/OTATradeReport.pdf. Jaenicke, E.C., Demko, I., 2017d. Consumer attitudes and beliefs study. Report to the Organic Trade Association, https://www.ota.com/resources/consumer-attitudes-and-beliefs-study. Kearney, J., 2010. Food consumption trends and drivers. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 365 (1554), 2793–2807. Kowitt, B., 2015. Special report: the war on big food. Fortune. http://fortune.com/2015/05/21/the-war-on-big-food/. Kremen, A., Greene, C., Hanson, J., 2004. Organic Produce, Price Premiums, and Eco-Labeling in U.S. Farmers’ Markets. Vegetables and Pulses Outlook No. (VGS-301-01), https://www.ers.usda.gov/webdocs/publications/ 39497/13895_vgs30101_1_.pdf?v¼41056. Magkos, F., Arvaniti, F., Zampelas, A., 2003. Organic food: nutritious food or food for thought? A review of the evidence. Int. J. Food Sci. Nutr. 54 (5), 357–371. Lernoud, J., Willer, H., 2017. Organic Agriculture Worldwide 2017: Current Statistics. http://orgprints.org/31197/1/ willer-lernoud-2017-global-data-biofach.pdf. Magkos, F., Arvaniti, F., Zampelas, A., 2006. Organic food: buying more safety or just peace of mind? A critical review of the literature. Crit. Rev. Food Sci. Nutr. 46 (1), 23–56. McEachern, M.G., McClean, P., 2002. Organic purchasing motivations and attitudes: are they ethical? Int. J. Consum. Stud. 26 (2), 85–92. Moisander, J., 2007. Motivational complexity of green consumerism. Int. J. Consum. Stud. 31, 103–128. Motomura, C., 2013. Japanese organic market report. Agricultural Trade Office of Japan. https://gain.fas.usda.gov/ Recent%20GAIN%20Publications/Japanese%20Organic%20Market_Osaka%20ATO_Japan_6-20-2013.pdf. Ngobo, P.V., 2011. What drives household choice of organic products in grocery stores? J. Retail. 87, 90–100. Nielsen, 2015. We Are What We Eat. Healthy Eating Trends Around the World. https://www.nielsen.com/content/ dam/nielsenglobal/eu/nielseninsights/pdfs/Nielsen%20Global%20Health%20and%20Wellness%20Report% 20-%20January%202015.pdf. Nutrition Business Journal, 2004. NBJ’s organic foods report 2004. New Hope Natural Media, Inc., Boulder, CO. Nutrition Business Journal, 2010. U.S. Organic Food Sales ($Mil) 1997-2009, 2010e-2017e, Chart 22. Penton Media, Inc., New York. Pagiaslis, A., Krystallis-Krontalis, A., 2014. Green consumption behavior antecedents: environmental concern, knowledge, and beliefs. Psychol. Mark. 31, 335–348. Paull, J., 2011a. The uptake of organic agriculture: a decade of worldwide development. JSDS 2 (3), 111–120. Paull, J., 2011b. Nanomaterials in food and agriculture: the big issue of small matter for organic food and farming. In: Proceedings of the Third Scientific Conference of ISOFAR (International Society of Organic Agriculture Research), Namyangju, Korea, pp. 96–99. Peng, M., Salaheen, S., Biswas, D., 2014. Animal health: antibiotic global issues. In: Encyclopedia of Agriculture and Food Systems. vol. 1. Elsevier Inc. Press, pp. 346–357. Peng, M., Salaheen, S., Almario, J.A., Tesfaye, B., Buchanan, R., Biswas, D., 2016. Prevalence and antibiotic resistance pattern of Salmonella serovars in integrated crop-livestock farms and their products sold in local markets. Environ. Microbiol. 18 (5), 1654–1665. Peng, M., Salaheen, S., Buchanan, R., Biswas, D., 2018. Alterations of antibiotic resistance in Salmonella typhimurium under environmental pressure. Appl. Environ. Microbiol. 84 (19), 1–14. Perrings, C., Jackson, L., Bawa, K., Brussaard, L., Brush, S., Gavin, T., et al., 2006. Biodiversity in agricultural landscapes: saving natural capital without losing interest. Conserv. Biol. 20 (2), 263–264. Pretty, J.N., Ball, A.S., Lang, T., Morison, J.I.L., 2005. Farm costs and food miles: an assessment of the full cost of the UK weekly food basket. Food Policy 30 (1), 1–19. Salaheen, S., Peng, M., Biswas, D., 2014. Replacement of conventional antimicrobials and preservatives in food production to improve consumer safety and enhance health benefits. In: Microbial Food Safety and Preservation Techniques. CRC press, pp. 305–328. Salaheen, S., Peng, M., Biswas, D., 2016. Ecological dynamics of Campylobacter in integrated mixed crop-livestock farms and its prevalence and survival ability in post-harvest products. Zoonoses Public Health 63, 641–650.

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Salaheen, S., Peng, M., Joo, J., Teramoto, H., Biswas, D., 2017. Eradication and sensitization of methicillin resistant Staphylococcus aureus to methicillin with bioactive extracts of berry pomace. Front. Microbiol. 8 (253), 1–10. Schuldt, J.P., Schwarz, N., 2010. The ‘organic’ path to obesity? Organic claims influence calorie judgments and exercise recommendations. Judgm. Decis. Mak. 5, 144–150. Smith-Spangler, C., Brandeau, M.L., Hunter, G.E., Bavinger, J.C., Pearson, M., Eschbach, P.J., et al., 2012. Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann. Intern. Med. 157 (5), 348–366. Srednicka-Tober, D., Bara
nski, M., Seal, C.J., Sanderson, R., Benbrook, C., Steinshamn, H., et al., 2016a. Composition differences between organic and conventional meat: a systematic literature review and meta-analysis. Br. J. Nutr. 115 (6), 994–1011. Srednicka-Tober, D., Bara
nski, M., Seal, C.J., Sanderson, R., Benbrook, C., Steinshamn, H., et al., 2016b. Higher PUFA and n-3 PUFA, conjugated linoleic acid, α-tocopherol and iron, but lower iodine and selenium concentrations in organic milk: a systematic literature review and meta- and redundancy analyses. Br. J. Nutr. 115 (6), 1043–1060. Teramoto, H., Salaheen, S., Biswas, D., 2016. Contamination of post-harvest poultry products with multidrug resistant Staphylococcus aureus in Maryland-Washington DC metro area. Food Control 65, 132–135. Tsakiridou, E., Boutsouki, C., Zotos, Y., Mattas, K., 2008. Attitudes and behavior towards organic products: an exploratory study. Int. J. Retail Distrib. Manag. 36, 158–175. Tucker, E.M., Rifon, N.J., Lee, E.M., Reece, B.B., 2012. Consumer receptivity to green ads: a test of green claim types and the role of individual consumer characteristics for green ad response. J. Advert. 41, 9–23. USDA, 2012. National Organic Program (NOP)‘s List of Allowed and Prohibited Substances. https://www.usda. gov/oig/webdocs/01601-0001-23.pdf. USDA, 2016. Guidance: Natural Resources and Biodiversity Conservation. https://www.ams.usda.gov/sites/ default/files/media/NOP%205020%20Biodiversity%20Guidance%20Rev01%20%28Final%29.pdf. Van Doorn, J., Verhoef, P.C., 2015. Drivers of and barriers to organic purchase behavior. J. Retail. 91, 436–450. Van Elsen, T., 2000. Species diversity as a task for organic agriculture in Europe. Agric. Ecosyst. Environ. 77 (1–2), 101–109. White, K.K., Duram, L.A., 2013. America Goes Green: An Encyclopedia of Eco-Friendly Culture in the United States. ABC-CLIO, California. Willer, H., 2017a. The World of Organic Agriculture, Statistics and Emerging Trends 2017. FIBL & IFOAM—Organics International. http://pae.gencat.cat/web/.content/al_alimentacio/al01_pae/13_observatori_pae/Estadistiquesi Fitxes/Fitxers/FiBLiFOAMOrganicWorld.pdf. Willer, H., 2017b. European Organic Market Data 2015. FiBL. http://orgprints.org/31200/31/willer-2017-europeandata-2015.pdf. Winter, C.K., Davis, S.F., 2006. Organic foods. J. Food Sci. 71 (9), R117–R124.

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Organic Farming Practices: Integrated Culture Versus Monoculture Serajus Salaheen*, Debabrata Biswas*,† *

Department of Animal and Avian Sciences, University of Maryland, College Park, MD, United States †Center for Food Safety and Security Systems, University of Maryland, College Park, MD, United States

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2 Classification of Organic Farming 2.1 Monoculture/Solely Livestock Production Systems 2.2 Minimum or Landless Solely LP Systems 2.3 Maximum Land Using Grassland-Based Systems 2.4 Monoculture/Solely Crop Production Farm 2.5 Mixed-Farming Systems/Integrated Farming

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1 INTRODUCTION An integrated crop-livestock farm (ICLF), also known as polyface or mixed crop-livestock farming (MCLF), is a common type of commercial agricultural practice associated with the production of both crops and animals on one farm (Thornton and Herrero, 2001; Russelle et al., 2007; Peng et al., 2016) and is a well-known traditional farming system around the

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world. The ICLF system can be divided into spatially separated farming, rotational farming, and fully combined farming. In spatially separated ICLF, crops and livestock are physically separated. In this system, animals are reared in a barn or pasture, and animal droppings are used for composting and soil fertilization. In rotational ICLFs, the farm animals and crops alternatively occupy the farmlands—all animal droppings are deposited and mixed with the soil by animal movements or other environmental parameters. In a fully combined ICLF system, animals can roam and interact with crops, feeding on crop residues, weeds, or pests for nutrition and depositing excreta, which fertilize the soil at the same time. In comparison to ICLF, monoculture farming incorporates either crop or animals in the farm. This is generally a commercial farming practice that was predominant in the last several decades and vastly occupied the food markets. Reports suggest that monoculture farming led to increased volume of products per farm (Altieri, 2002; Saysel et al., 2002). Monoculture type farms have been popular worldwide, which is evident from the geographical expansion of land dedicated to crops and yearly production of the same species of crop on the same farmland. The majority of these crops are grown under “modern monoculture systems” that show particular vulnerability to environmental stresses and climate change due to their ecological homogeneity, constituting a prominent threat to food security (Pimentel and Levitan, 1986; Heinemann et al., 2013; Altieri et al., 2015). As a result, ICLFs are returning and growing rapidly in the United States, especially in the Mid-Atlantic and Northeast regions (Thornton and Herrero, 2001). Many ICLF farms are noncertified organic or in organic transition and contribute a significant amount of food products, particularly fresh produce and meat products, specifically lamb and goat meat (Luna et al., 1994; Sulc and Tracy, 2007). Products from ICLFs are sold in either farmers’ markets, roadside stands, and/or local retail markets. Currently there are more than 8000 farmers’ markets listed in the National Farmers’ Market Directory ( Johnson et al., 2013). Recently, it has been reported that the products grown at ICLFs and available in local or regional retail or farmers’ markets are contaminated with several bacterial pathogens (Berger et al., 2010; Johnston et al., 2005; Mukherjee et al., 2006; Bolton et al., 2012; Kozak et al., 2013; Teramoto et al., 2015; Peng et al., 2016; Salaheen et al., 2016). Although the chances of large or widespread outbreaks with contaminated produce sold in farmers’ markets are very low, this sector may contribute to sporadic cases and localized outbreaks (Peng et al., 2016). The proximity of animal and produce operations on the same farm may increase the potential for cross-contamination of pathogens between animal reservoirs (poultry, pig, sheep, goat, cattle, and other livestock) and fresh produce (Hoffman, 2010; Strawn et al., 2013). On the other hand, a fundamental focus during transitioning to organic involves building soil health (Ohio Ecological Food and Farm Association, 2015) and microfloral diversity (Bullock et al., 2001). ICLFs involve sustainable manure management and use manure-based soil amendments to fertilize soils (van den Berg et al., 2007; Hoffman, 2010; Strawn et al., 2013). Animal manure and compost not only are fertilizers but also improve soil health by increasing soil organic matter and accompanying properties. Rich, complex soil amendments of animal origin could play a role in the survivability zoonotic pathogens and transfer to fresh produce (Sidhu, 1998; Ottoson et al., 2013). This chapter will discuss various aspects of organic farming in terms of integrated and monoculture and their potential impacts on food safety.

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2 CLASSIFICATION OF ORGANIC FARMING Economic Research Service (ERS) estimated the organic food market to be one of the most quickly expanding sectors in the US food industry. Growing consumer concerns with some of the conventional farming practices, such as growth hormones, antibiotic growth promoter usage, and overall quality of products are some (of the many) factors leading to this increased popularity of organic farming. It has been reported that sales of organic food products almost doubled (from $3.5 billion to more than $10 billion) during 1997–2003 (Adl et al., 2011; Dimitri and Oberholtzer, 2009). A higher level of biodiversity or positive impact on species richness are the most important ecological benefits of organic farming (Bengtsson et al., 2005; Clough et al., 2007; Gabriel et al., 2010; Hawesa et al., 2010). Both plant and animal food products can be grown organically. Plants are classified as agronomic crops, horticultural crops, cash crops, or catch crops. In this chapter, we focus only on plants used for human consumption as food. Organic farm animals cover the following animal species: cattle, buffalo, sheep, goat, pig, and chicken. According to the published literature (Ruthenberg, 1980; Jahnke, 1982; FAO, 1980, 1994; De Boer, 1992), most farming systems, both plant and livestock, are classified by various criteria including quantitative criteria, typologies, cluster, and methodologies of farming practices. Different types of organic farming practices are as follows:

2.1 Monoculture/Solely Livestock Production Systems In the solely livestock production (LP) system, dry matter from rangelands, pastures, animal forages, and purchased feeds are mainly (by more than 90%) used to feed animals, whereas nonlivestock farming activities contribute less than 10% of the total value of production (Ser
e et al., 1996).

2.2 Minimum or Landless Solely LP Systems Landless solely LP system is considered a subset of the solely LP system. In this system, less than 10% of the dry matter fed to livestock are produced on the farm, and annual average stocking rates are above 10 livestock units per hectare of agricultural land (Ser
e et al., 1996). The livestock are raised in a very limited land area or in an air/temperature-controlled environment. In the same system, farmers can raise both monogastric and ruminant farm animals. Raising monogastric species, specifically chickens, turkeys, rabbits, and pigs, involves most of the feed coming from outside of the farm. This same landless system can also be used to raise ruminants such as cattle, goats, sheep, and horses where feeds are also introduced from outside the farm. In these types of farms, farmers can compost and utilize the manure on fields to produce feed and/or cash crops that may increase dissemination of pathogenic bacteria in the farm environment and cause animal-to-animal transfer of pathogens.

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2.3 Maximum Land Using Grassland-Based Systems Another subset of the solely LP system, maximum land using grassland-based system, is now gaining popularity in developed countries including the United States, particularly the outside of colder zones where temperature is favorable to grow grasses at least 6 months a year. In this grazing system, a significant percent of the dry matter fed to animals is farmproduced. In this farming practice, the grazing periods are quite long and varied regionto-region or country-to-country. It seems to be concentrated more in the humid or subhumid regions, particularly in regions where access to markets or, for agronomic reasons, crop production is limited. Such farming practices produce a huge amount of animal food products, particularly milk and beef. With the recent increasing demand of organic or pasture dairy and animal products in the United States, this type of farming is growing faster than ever in regions such as Florida, Texas, New Mexico, California, and some other states.

2.4 Monoculture/Solely Crop Production Farm Monoculture/solely crop production farms are the farming types by which farmers grow only crops, both annual crops/trees and field crops, such as wheat, corn, rice, rapeseed, sugar cane, and cotton. Monoculture is widely used in industrial farming systems, including conventional and organic farming, and has allowed increased efficiency in planting and harvest. Continuous monoculture, or “monocropping” where the same species is grown year after year, can lead to unsustainable environments such as building up disease pressure and reducing particular nutrients in the soil. Under certain circumstances, monocropping can lead to deforestation. The practice has also been criticized for its environmental impacts, one of the major being soil degradation due to nonrotational cropping. Crop rotation is the practice of changing the types of crops in a farmland from year to year, which improves soil health and quality, whereas monocropping has been implicated in the loss of nutrients from the soil (Bennett et al., 2012).

2.5 Mixed-Farming Systems/Integrated Farming Mixed farming systems or integrated farming produce both crops and animals on one farm. This farming system permits wider crop rotations and thus reduces dependence on chemicals, allowing diversification for better risk management. Two subsets of mixed systems are (1) rain-fed ICLF systems and (2) irrigated ICLF systems. In rain-fed ICLF systems, more than 90% of the value of nonlivestock farm production comes from rain-fed land use. Some parts of the world still depend on natural rains for growing crops as well as grasses for animal grazing. Ponds or small lakes are common in such types of integrated farms and partly provide some water for the animal and emergency need of crops. As a source of stagnant water, these ponds can play a significant role in the transfer of pathogenic microbes. On the other hand, in irrigated ICLF systems, more than 10% of the value of nonlivestock farm production comes from irrigated land use. Due to potential water crises in animal and crop farming, deep wells were established in many parts of developing countries, and now many integrated farmers have their own or community-based water supply systems either from deep wells or canals from nearby rivers or falls.

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3 ICLF PRACTICES AND RESULTING COMPLEX MICROBIAL ECOLOGY OF THIS SYSTEM According to the National Agricultural Statistics Service, 14,093 certified and exempt organic farms in the United States sold a total of $5.5 billion in organic products in 2014, up 72% since 2008. Additionally, the industry showed potential for growth in production, with approximately 39% of organic producers reporting that they intended to increase organic production over the next 5 years. Another 688 large farms and a number of medium- and smallsized farms—including ICLFs—are in the process of transitioning into organic agriculture production. Integration of farming systems and shared spaces on farms can expose multiple routes of foodborne pathogen contamination. In ICLFs, shared/commonly used tools, newly added chicks, calves and other animals, birds, and wild animals may also add to pathogen loads (Natvig et al., 2002). It has been reported that contamination of produce samples from organic integrated farms in Europe were higher than those grown on organic produce farms with no livestock (Bolton et al., 2012). ICLFs recycle animal manure as fertilizer and plant residuals as animal feed (Fig. 1). Depending on the management practices used, such recycling can increase the potential of introducing pathogenic microbes to crop production environments and perpetuate pathogen reservoirs in livestock. The source of contamination of fresh produce with enteric pathogens can frequently be traced back to environmental reservoirs associated with farm operations and wild animals (Brinton et al., 2009; Park et al., 2012). The key components of ICLF practices that might impact microbial survival and the contamination processes to the products both in pre- and postharvest stages are (1) recycling of animal and crop residuals, (2) movement/addition of domesticated and wild animals, (3) contamination of water used for produce and livestock, and (4) postharvest produce washing and processing.

4 ADVANTAGES AND DISADVANTAGES OF MONOCULTURE From an economic viewpoint, larger or single-component production with mechanical- or technological-dependent system seems more practical. By cultivating the same species in a huge land area, farmers can maximize their profit by mass production via a single operation through unique growing/farming practices including planting, maintaining (including pest control), and harvesting with similar resources. This helps result in a greater yield at a lower cost. In addition, farmers can pick the best monoculture crops to grow considering the local climate and soil conditions. Further, it is much easier and straightforward to cultivate one kind of crop or breed one type of livestock in terms of the knowledge and experience needed to do it successfully. Monoculture farming has several disadvantages due to the ability to produce a larger volume of affordable products with less investment. Monoculture farming cultivates a single crop in an intensive manner and on a very large scale, such as current practices in the United States in which corn, wheat, soybeans, cotton, and rice are commonly grown. However, growing the same crops year after year can deplete the soil of appropriate nutrients or humus that

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Sunlight, water

Increased profits

Food Labor Biofuel Medicine Consumer goods Reduce need for pesticides

Recycling N2 Fodder

Manure

Humans

Reduce feed expense Food Labor Consumer goods

FIG. 1

Potential ecological pathways and economic relationships within an integrated crop-livestock farm (ICLF)

system.

play key roles in soil fertility. In some cases, monocultures are more susceptible to certain weeds and pests, which means that farmers will depend vastly on pesticides to save their crops, which may have environmental impacts.

5 ADVANTAGES AND DISADVANTAGES OF ICLF FARMING ICLF farming is associated with higher levels of biodiversity of plants and biota (Clough et al., 2007; Gabriel et al., 2010; Hawesa et al., 2010). ICLF farming systems may result in greater biodiversity than their conventional counterparts, mainly because of reduced soil disturbance and little to no chemical applications. Ecological studies assessing the impact of soil management practices such as conventional till and zero till on total bacterial communities and phytopathogens have shown that these practices affect not only bacterial diversity but also the bacterial community structure, microbial biomass, and phytopathogen survival (Ceja-Navarro et al., 2010; Chellemi et al., 2012; Ibekwe et al., 2002; Sipil€a et al., 2012).

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Typically, because the products of small- to medium-sized ICLFs are sold on a local or regional scale, the chances of any contamination of produce causing large or widespread outbreaks are low. However, locally sold produce that has been contaminated with foodborne pathogens may play an important role in sporadic cases or localized outbreaks. Due to the nature of ICLF systems, cross-contamination between animals and fresh crop produce may occur because animals may serve as reservoirs for pathogens (van den Berg et al., 2007; Hoffman, 2010; Strawn et al., 2013) that could also colonize farm crops. Identifying the prevalence, identity, and antibiotic resistance patterns of microbial pathogens in ICLF products—specifically fresh produce available at farmers’ markets, roadside stands, and local grocery stores and their production facilities—are crucial to fully assess the risks of sporadic cases or localized outbreaks. Such information could significantly contribute to enhance the safety and biosecurity of the products and farming systems. Most studies have investigated only major and mostly known foodborne pathogen prevalence, such as Salmonella, Escherichia coli O157:H7, and Listeria monocytogenes, in organic produce grown in the United States (Berger et al., 2010; Kozak et al., 2013; Bolton et al., 2012; Johnston et al., 2005; Mukherjee et al., 2006). In a study in the US upper Midwest region, Mukherjee et al. (2006) researched the contamination level of organic produce with common zoonotic bacterial pathogens at pre- and postharvest levels and concluded that some of the conventionally produced fruits and vegetables had significantly lower coliform counts than semiorganic or organic produce. In another study in Canada, Kozak et al. (2013) found that, in addition to bacterial pathogens, several parasites were also often associated with produceborne infections. This may vary depending on commodity. But to our knowledge, no data appears to exist on on-farm cross-contamination for other microbial pathogens that are not commonly found in produce grown on the large-scale produce-only farms but are more likely to occur in the ICLF environment and their products due to the presence of livestock and recycling of animal waste. Such under research, produce-borne pathogens include bacteria, viruses, and parasites. Farm livestock are recognized as major reservoirs of potential zoonotic pathogens including underresearched foodborne pathogens. In addition, the possibility of contamination of the produce grown in ICLFs with parasites such as Cryptosporidium parvum/ hominis and Giardia duodenalis is potentially high, and these parasites are mostly unknown because of the complex methods of isolation and identification. In a European study, it was found that the contamination level in produce samples of organic-integrated farms was higher than those grown in organic produce farms in absence of livestock (Bolton et al., 2012). Parasites such as Giardia, Cryptosporidium and many bacterial pathogens such as Salmonella, E. coli O157:H7, Staphylococcus, and Yersinia could be introduced to integrated or mixed crop-livestock farms and its products at the preharvest level through contaminated water, dirt, insects, animal waste green fertilizer, shared/commonly used instruments, and/or farm animals, birds, and wild animals (Natvig et al., 2002). Several researchers detected eggs of parasites in apples in the United States and in a variety of salad blends from Canada. The source of contamination of fresh produce with enteric pathogens can frequently be traced back to environmental reservoirs associated with farm and wild animals (Brinton et al., 2009; Park et al., 2012). Moreover, in ICLFs, produce and livestock such as poultry, cattle, swine, goat, and sheep coexist in a single facility, and feral animals, birds, and rodents commonly coexist. This increases the possibility of introducing

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pathogenic microbes to crop production environments. The survival/multiplication ability during recycling of animal waste as a sole source of fertilizer is also high if manure is not fully composted.

6 CONCLUSION Improving the sustainability of organic, naturally, or pasture-grown leafy green produce for human raw consumption and the microbial safety of these products therefore requires information of possible contaminants and intervention strategies. Nevertheless, the need exists for both interventions and alternatives or replacements for synthetic chemicals and antibiotics with natural bioactive extracts to offer several benefits including increased microbial safety, consumer confidence, and public health benefits. Therefore to make organic or pasture and/or integrated farming sustainable, further intensive research is required for a greater understanding of the risks and to explore possible measures against microbial contamination of farm products.

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FAO, 1980. The Classification of World Livestock Systems. A study prepared for the Animal Production and Health Division of FAO. AGA/MISC/80/3. FAO, 1994. Integrating Livestock and Crops for the Sustainable Use and Development of Tropical Agricultural Systems. AGSP-FAO. Gabriel, D., Sait, S.M., Hodgson, J.A., Schmutz, U., Kunin, W.E., Benton, T.G., 2010. Scale matters: the impact of organic farming on biodiversity at different spatial scales. Ecol. Lett. 13, 858–869. Hawesa, C., Squirea, G.R., Hallett, P.D., Watsonb, C.A., Young, M., 2010. Arable plant communities as indicators of farming practice. Agric. Ecosyst. Environ. 138, 17–26. Heinemann, J.A., Massaro, M., Coray, D.S., Agapito-Tenfen, S.Z., Wen, J.D., 2013. Sustainability and innovation in staple crop production in the US Midwest. Int. J. Agric. Sustain. https://dx.doi.org/ 10.1080/14735903.2013.806408. Hoffman, I., 2010. Climate change and the characterization, breeding and conservation of animal genetic resources. Anim. Genet. 41 (Suppl. 1), 32–46. Ibekwe, A.M., Kennedy, A.C., Frohne, P.S., Papiernik, S.K., Yang, C.H., Crowley, D.E., 2002. Microbial diversity along a transect of agronomic zones. FEMS Microbiol. Ecol. 39, 183–191. Jahnke, H.E., 1982. Livestock Production Systems and Livestock Development in Tropical Africa. Kieler Wissenschaftsverlag Vauk, Kiel. Johnson, R., Aussenberg, R.A., Cowan, T., 2013. The Role of Local Food Systems in U.S. Farm Policy. Congressional Research Service. March 7-5700. www.crs.gov. Johnston, L.M., Jaykus, L., Moli, D., Martinez, M.C., Anciso, J., Mora, B., Moe, C.L., 2005. A field study of the microbiological quality of fresh produces. J. Food Prot. 68 (9), 1840–1847. Kozak, G.A., MacDonald, D., Landry, L., Fabber, J.M., 2013. Foodborne outbreaks in Canada linked to produce: 2001 through 2009. J. Food Prot. 76 (1), 173–183. Luna, J., Allen, V., Fontenot, J., Daniels, L., Vaughan, D., Hagood, S., Taylor, D., Laub, C., 1994. Whole farm systems research: an integrated crop and livestock systems comparison study. Am. J. Altern. Agric. 9 (1–2), 57–63. Mukherjee, A., Speh, D., Jones, A.T., Buesing, K.M., Diez-Gonzalez, F., 2006. Longitudinal microbiological survey of fresh produce grown by farmers in the upper Midwest. J. Food Prot. 69 (8), 1928–1936. Natvig, E.E., Ingham, S.C., Ingham, B.H., Cooperband, L.R., Roper, T.R., 2002. Salmonella enterica serovar Typhimurium and Escherichia coli contamination of root and leaf vegetables grown in soils with incorporated bovine manure. Appl. Environ. Microbiol. 68 (6), 2737–2744. Ohio Ecological Food and Farm Association, 2015. Organic Transition Guide, third ed. The Ohio State University, Columbus, OH. 124 pp. Ottoson, J.R., Anna, N.H., Eva, S., 2013. Measures to mitigate nitrogen and phosphorous losses can reduce the risk of disease transmission from manure. Ramiran Symposium Proceeding. http://www.ramiran.net/doc13/ Proceeding_2013/documents/S2.08.pdf. Park, S., Szonyi, B., Gautam, R., Nightingale, K., Anciso, J., Ivanek, R., 2012. Risk factors for microbial contamination in fruits and vegetables at the preharvest level: a systematic review. J. Food Prot. 75 (11), 2055–2081. Peng, M., Salaheen, S., Almario, J.A., Tesfaye, B., Buchanan, R., Biswas, D., 2016. Prevalence and antibiotic resistance pattern of Salmonella serovars in integrated crop-livestock farms and their products sold in local markets. Environ. Microbiol 18, 1654–1665. https://dx.doi.org/10.1111/1462-2920.13265. (in press). Pimentel, D., Levitan, L.C., 1986. Pesticides: amounts applied and amounts reaching pests. Bioscience 36, 514–515. https://dx.doi.org/10.2307/1310108. Russelle, M.P., Entz, M.H., Franzluebbers, A.J., 2007. Reconsidering integrated crop-livestock systems in North America. Agron. J. 99, 325–334. Ruthenberg, R., 1980. Farming Systems in the Tropics. Clarendon Press, Oxford. 424 pp. Salaheen, S., Peng, M., Biswas, D., 2016. Ecological dynamics of Campylobacter in integrated mixed crop-livestock farms and its prevalence and survival ability in post-harvest products. Zoonoses Public Health 63, 641–650. Saysel, A.K., Barlas, Y., Yenig€ un, O., 2002. Environmental sustainability in an agricultural development project: a system dynamics approach. J. Environ. Manag. 64 (3), 247–260. Ser
e, C., Steinfeld, H., Groenewold, J., 1996. World Livestock Production Systems. Food and Agriculture Organization of the United Nations.

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Sidhu, G.S., 1998. Role of microorganism in soil fertility. Ultra grow report, http://www.ultragro.net/pdf/newsletters/ NL%20Role%20of%20Microorganisms%20in%20Soil%20Fertility.pdf. Sipil€ a, T.P., Yrj€al€a, K., Alakukku, L., Paloj€arvi, A., 2012. Cross site soil microbial communities under tillage regimes— fungistasis and microbial biomarkers. Appl. Environ. Microbiol. 78, 8191–8201. Strawn, L.K., Fortes, E.D., Bihn, E.A., Nightingale, K.K., Gr€ ohn, Y.T., Worobo, R.W., Wiedmann, M., Bergholza, P.W., 2013. Landscape and meteorological factors affecting prevalence of three food-borne pathogens in fruit and vegetable farms. Appl. Environ. Microbiol. 79, 588–600. Sulc, R.M., Tracy, B.F., 2007. Integrated crop-livestock systems in the US corn belt. Agron. J. 99, 335–345. Teramoto, H., Salaheen, S., Biswas, D., 2015. Contamination of post-harvest poultry products with multidrug resistant Staphylococcus aureus in Maryland-Washington DC metro area. Food Control 65, 132–135. Thornton, P.K., Herrero, M., 2001. Integrated crop–livestock simulation models for scenario analysis and impact assessment. Agric. Syst. 70 (2001), 581–602. van den Berg, M.M., Hengsdijk, H., Wolf, J., Van Ittersum, M.K., Guanghuo, W., Roetter, R.P., 2007. The impact of increasing farm size and mechanization on rural income and rice production in Zhejiang province, China. Agric. Syst. 94 (3), 841.

Further Reading McDonald, E., Heier, B.T., Nyga˚rd, K., Stalheim, T., Coudjoe, K.S., Skjerdal, T., Wester, A.L., Lindstedt, B.A., Stavnes, T.L., Vold, L., 2012. Yersinia enterocolitica outbreak associated with ready-to-eat salad mix, Norway, 2011. Emerg. Infect. Dis. 18 (9), 1496–1499. National Agricultural Statistics Service (NASS), 2010. Noncitrus Fruits and Nuts 2009 Preliminary Summary. U.S. Department of Agriculture, Washington, DC. http://usda.mannlib.cornell.edu/usda/nass/NoncFruiNu// 2010s/2010/NoncFruiNu-01-22-2010_revision.pdf. [(Accessed 10 February 2014)].

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Governmental Policies and Regulations Including FSMA on Organic Farming in the United States and Around the Globe M. Nazim Uddin*, Md. Latiful Bari† *

Bangladesh Agriculture Research Institute (BARI), Gazipur, Bangladesh †Center for Advanced Research in Sciences, University of Dhaka, Dhaka, Bangladesh

O U T L I N E 1 Introduction 1.1 Historical Background of Organic Agriculture 1.2 Overview of Organic Agriculture Policy 1.3 Trends in Organic Agriculture Policies in Developed Countries 1.4 Trends in Organic Agriculture Policies in Developing Countries

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2 Organic Farming Legislation 2.1 Keys Elements to the Standard 2.2 EU Organic Farming Policy: Background History 2.3 EU New Labeling Regulation 2.4 EU Imported Organic Products

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Safety and Practice for Organic Food https://doi.org/10.1016/B978-0-12-812060-6.00003-9

3 Brief History of Organic Agriculture in Japan 3.1 Overview of the Organic Japanese Agricultural Standard System 3.2 Key Features of the Japanese Standard for Organic Products

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4 Organic Regulation Worldwide: Current Status 4.1 International Federation of Organic Agriculture Movements 4.2 IFOAM Organic Agriculture Guideline

44 44 45

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4.3 The IFOAM Standard for Organic Production and Processing 4.4 Development of Harmonization and Equivalence Tools 5 US FDA Food Safety Modernization Act 5.1 Labeling

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6 Opportunities and Future Development/Future of Organic Farming Policy

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7 Conclusion

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1 INTRODUCTION Organic agriculture is a system for crops, livestock, and fish farming that emphasizes environmental protection and the use of natural farming techniques. It is concerned not only with the endproduct but also with the entire system used to produce and deliver the agricultural product. To this end, the entire farm cycle, from production and processing to handling and delivery, excludes the use of artificial products such as genetically modified organisms (GMOs) and certain external agricultural inputs such as pesticides, veterinary drugs, synthetic additives, and fertilizers. Organic farmers rely instead on natural farming methods and modern scientific ecological knowledge to maximize the long-term health and productivity of the ecosystem, enhance the quality of the products, and protect the environment. It is believed that organic farming methods are more sustainable and less damaging to agriculture. Organic agriculture has rooted in traditional agricultural practices in small communities around the world and became visible on a wider scale in the 1960s when farmers and consumers became concerned that the amount of chemicals used in crop and animal production could have negative consequences for human health and the environment. Since then, it has developed into a more cohesive and organized movement and now is the fastest growing food sector globally.

1.1 Historical Background of Organic Agriculture The concept of organic agriculture began in the early part of the twentieth century, primarily in Europe, but also in the United States. The pioneers of the early organic movement were motivated by a desire to reverse the perennial problems of agriculture—erosion, soil nutrient depletion, decline of crop varieties, low quality food and livestock feed, and rural poverty. The overall notion was that the health of a nation built on agriculture is dependent on the long-term vitality of its soil. The soil’s health and vitality are believed to be embodied in its biology and in the organic soil fraction called humus. A soil management strategy called “humus farming” emerged, which employed traditional farming practices that not only conserved but also regenerated the soil. These practices—drawn mainly from stable European and Asian models—included managing crop residues, applying animal manures, composting, green manuring, planting perennial forages in rotation with other crops, and adding lime and other natural rock dusts to manage pH and ensure adequate minerals. A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

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1 INTRODUCTION

FIG. 1

Feed the plant vs. Feed the Soil

Leaf

Conventional soluble fertilizers

Flower

Organic matter (from crop residues, manure, green manure, mulch, compost, natural fertilizers, etc.)

“Feeding the soil” meant feeding the organic or top-most layer of soil and food web. Reproduced with permission from Kuepper, George, 2010. A Brief Overview of the History and Philosophy of Organic Agriculture. Kerr Center for Sustainable Agriculture, pp. 1–23.

Stem Available nutrients Chelates, antibiotics, growth factors, golmalin, vitamins

Soil food web

Roots

The soil food web is the living fraction of the top-most layer of soil, composed of bacteria, fungi, earthworms, insects, and varieties of microorganisms that digest organic matter and provide nutrition to crop plants (see Fig. 1). This contrasts with the (then-emerging) strategy of using soluble fertilizers, which bypass the soil food to fertilize plants directly. Humus farmers felt that soluble fertilizers led to imbalanced plant nutrition and reduced food and feed quality. Many farmers also believed that synthetic fertilizers actually harmed the soil biology—either by killing organisms or upsetting the natural balance. The danger of pesticide use was also visible; thus they were either excluded from organic farming in general or they followed an official set of created guidelines at this point. The common notion of organic agriculture is simply farming as practiced before the advent of synthetic chemicals. However, the term “humus farming” went out of vogue in the 1940s as the term “organic” became more popular. The word “organic” was first described in the book Look to the Land by Lord Northbourne, published in 1940, which intended and used the word “organic” to describe the process of a farming system that involved production without the use of chemical fertilizers, pesticides, or other artificial chemicals. The unifying principle is that healthy food will produce healthy people, and that healthy people were the basis for a healthy society. These ideas gained popularity in Europe and the United States from the 1940s through 1960s among those concerned about the effects of chemicals and pesticides on their foods, most notably after scientist Rachel Carson’s 1962 book, Silent Spring, illustrated the effects of pesticides and other chemicals on food and in the environment.

1.2 Overview of Organic Agriculture Policy Because organic foods cannot be distinguished from conventional products at a glance, consumers depend entirely on third-party certification, that is, the process according to which public or private certification bodies provide assurance that organic products have been produced and handled according to applicable standards. Organic standards have long been used to represent a consensus about what an “organic” claim on a product means and to convey that information to consumers. Certification not only leads to consumer trust in the organic system and products but also gives organic farming a distinct identity and makes

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market access easier. Thus in contrast with food labeled as “natural,” “green,” or “free range,” the organic label denotes compliance with very specific production and preparation methods. As organic agriculture production and trade has increased significantly worldwide, thus the organic label has greater credibility. Therefore a harmonized legislation was required to set the minimum requirements for organic agriculture and to create the institutional framework for certification. Legislation ensures fair competition among producers and facilitates equivalence with other countries for international trade. Because of the health and environmental benefits and trade opportunities associated with organic agriculture, governments sometimes write policy that incentivizes farmers to shift to organic methods through tax reductions/exemptions, subsidies, or support for research and marketing. In addition, national legislation may allow organic agriculture to grow from localized products to national and international trade commodities. Prior to the 1980s, the organic agriculture movement was driven by a collection of grassroots organizations, farmers, and traders who formed national associations to advocate for their cause—Demeter International in Germany, the Soil Association in the United Kingdom, and Rodale Press in the United States, to name a few. Many of these associations banded together in 1972 to form the International Federation of Organic Agriculture Movements (IFOAM), an international umbrella for the organic movement. Today, IFOAM unites more than 784 organizations in 117 countries. In contrast, governments were slow to prepare draft legislation and to set these standards; however, the first such legislation appeared in Oregon and California in the United States, in 1974 and 1979, respectively. In the beginning of 1980s, organic farming had become the focus of significant attention from policy-makers, consumers, environmentalists, and farmers around the world. As a result, state institutions became increasingly involved in regulating and supporting the organic sector (Table 1). Reflecting the multiple goals of organic farming and agricultural

TABLE 1 Key Events on Organic Agriculture Policy Year

Key Events on Organic Agriculture Policy

1911

F.H. King, an American agronomist, toured China, Korea, and Japan in 1909, studying traditional methods of fertilization and tillage. In 1911, he published Farmers of Forty Centuries: Permanent Agriculture in China, Korea, and Japan, which later served as a repository of information for a new generation of organic farmers searching for information on soil fertility

1924

Rudolf Steiner, an Austrian philosopher presented the first organic agriculture course to a group of more than 100 farmers and others at Koberwitz (Poland). His lecture was published in 1924, which led to the popularization of biodynamic agriculture, probably the first comprehensive organic farming system

1938

In Japan, Masanobu Fukuoka, a microbiologist working in soil science and plant pathology, began to doubt the modern agricultural movement. He quit his job as a research scientist, returned to his family’s farm in 1938, and devoted the next 60 years to developing a radical no-till organic method for growing grain and many other crops, which is now known as natural farming (shizen n
oh
o), nature farming, “do–nothing” farming, or Fukuoka farming

1939

Lady Eve Balfour launched the Haughley Experiment on farmland in England. It was the first side-by-side comparison of organic and conventional farming. Four years later, she published The Living Soil based on the initial findings of the Haughley Experiment. It was widely read and led to the formation of a key international organic advocacy group, the Soil Association

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TABLE 1

37

Key Events on Organic Agriculture Policy—cont’d

Year

Key Events on Organic Agriculture Policy

1940

The first use of the term “organic farming” is coined by Lord Northbourne. The term derives from his concept of “the farm as organism,” which he expounded in his book, Look to the Land (1940), in which he described a holistic, ecologically balanced approach to farming

1944

An international campaign called the Green Revolution was launched in Mexico with private funding from the United States. It encouraged the development of hybrid plants, chemical controls, large-scale irrigation, and heavy mechanization in agriculture around the world

1947

Pioneer botanist Sir Albert Howard’s book, An Agricultural Testament, published in 1940, promoted organic techniques, and his other book, The Soil and Health, published in 1947, was the first book to include “organic” agriculture or farming in its title

1950

During this decade, “sustainable” agriculture was a research topic of interest. The science tended to concentrate on new agriculture research. In the United States, a New York farmer named J.I. Rodale began to popularize the term and methods of organic growing. In 1959, the first edition of Rodale’s Encyclopedia of Organic Gardening was published

1962

Rachel Carson, a prominent scientist and naturalist, published Silent Spring, chronicling the effects of Dichlorodiphenyltrichloroethane (DDT) and other pesticides on the environment, drawing on the research in “biodynamic agriculture”—a form of alternative agriculture very similar to organic farming. This book was widely read around the world and was instrumental in the US government’s banning of DDT in 1972

1972

The International Federation of Organic Agriculture Movements (IFOAM) was founded in Versailles, France

1975

Masanobu Fukuoka released his book, The One-Straw Revolution, which spearheaded natural farming. His approach to small-scale grain production emphasized a meticulous balance of the local farming ecosystem and a minimum of human interference and labor

1980

In this decade, various farming and consumer groups around the world began seriously pressuring for government regulation of organic production to ensure standards of production. This led to various legislation and certification standards being enacted through the 1990s and to date

1984

Oregon Tilth established an early organic certification service in the United States

1990

Since the early 1990s, the retail market for organic farming in developed economies has been growing by about 20% annually due to increasing consumer demand. Concern for the quality and safety of food, and the potential for environmental damage from conventional agriculture are apparently responsible for this trend

2000

In this decade, the world market for organic products (including food, beauty, health, body care, household products, and fabrics) has grown rapidly. More countries are establishing formal, government-regulated organic certification. Monitoring and challenging certification rules and decisions have become regular, a part of high-profile activists in the organic movement

2001

After 10 years of political debate, the final National Organic Standards rule was published in the Federal Register on December 21, 2000, establishing US Department of Agriculture (USDA) standards for organic food in the United States

2009

The Chinese Organic Certification was founded on December 14, 2009

2010

The European Union (EU) organic logo was made mandatory on all prepackaged organic products. The logo can be accompanied by national or private logo for labeling and advertising organic products

2011

On December 6, 2011, the European Commission published the first list of control bodies recognized as implementing equivalent organic standards and control measures in third countries (EU regulation 1267/2011)

2017

On June 28, 2017 the Maltese presidency and the European Parliament reached a preliminary agreement on an overhaul of the existing EU rules on organic production and labeling of organic products

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policy, a varied and complex range of policy measures have been developed and implemented to support the organic sector. However, balancing societal and consumer/ market goals with institutional and private stakeholder interests in the organic sector created particular challenges for policy-making. The recognition that organic agriculture could help countries achieve environmental objectives further encouraged governments to adopt agrienvironmental laws to promote organic farming (e.g., 1992 reform of the European Community’s Common Agricultural Policy).

1.3 Trends in Organic Agriculture Policies in Developed Countries In developed countries, organic agriculture has often evolved bottom-up, that is, through initiatives and networks between farmers, rather than being advanced by government, research, or extension agencies (Padel, 2001). Organic agriculture currently covers 37 million hectares globally, which corresponds to 0.9% of global agricultural land. In 2010, the global market for organic produce was worth 59 billion US dollars, growing by almost 300% since 2000, and 96% of organic sales are made in European and North American markets (Willer and Kilcher, 2011). Modern agricultural farming practices employing irrational use of chemical inputs over the past four decades have resulted in loss of natural habitat balance and soil health. Apart from this, hazards such as soil nutrient depletion, decreased groundwater level, soil salinization, pollution due to fertilizers and pesticides, genetic erosion, ill effects on environment, reduced food quality, and increased cost of cultivation are other serious manifestations associated with the irrational use of chemical inputs (Badgley et al., 2007). As a result, farmers do not find agriculture a viable proposition anymore in addition to the substantially high price of factory-made external inputs and, more significantly, shifting of subsistence farming (mainly with homegrown inputs) to commercial farming (largely with purchased inputs). These negative consequences have forced farmers to find the alternate methods of farming (i.e., organic/ecological/biodynamic) around the world. Furthermore, farmers and consumers’ demand for conserving environmental health triggered the introduction of organic farming policy in developed countries. In the United States, organic farming and food are regulated by the United States Department of Agriculture’s National Organic Program (USDA NOP). The Congress authorized the USDA to create a uniform standard that would override all private and state standards. The USDA has the authority to recognize other governmental programs as equivalent to guarantee consumers’ confidence in organic products. In the European Union (EU), the European Council of Agricultural Ministers adopted Regulation (EEC) No. 2092/91 on organic farming and the corresponding labeling of agricultural products and foods to provide sustainable development of organic sector and ensure the effective and efficient functioning of the organic market. Additional regulations were adopted in June 2007 and apply to living or unprocessed products, processed foods, and animal feed. Furthermore, seeds and propagating material, as well as collection of wild plants and seaweed are also included in the scope of this regulation. Developed countries adopted policies to support sustainable agricultural development that involves ensuring and maintaining productive capacity for the future and increasing productivity without damaging the environment or jeopardizing natural resources. Also providing support in creating a sustainable agricultural development path means improving the

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quality of life in rural areas, ensuring enough food for present and future generations, and generating sufficient income for farmers. The EU supports: 1. The promotion of agricultural practices and technologies that are environmentally sustainable that raise rural incomes, such as integrated pest management, soil and water conservation methods, agro-ecological approaches, and agro-forestry; 2. Improvement of access to productive assets such as land and capital, and measures to ensure better delivery of essential services; 3. Initiatives improving income and reducing vulnerability for producers through capacity building and a comprehensive value chain approach. In addition, the EU supports respect for and recognition of local knowledge and local management of natural resources, and the efforts to promote the capabilities of current generations without compromising the prospects of future ones.

1.4 Trends in Organic Agriculture Policies in Developing Countries Organic agriculture currently covers only a small area in developing countries, but the demand for organic products is increasing, hence developing countries need to change their food system to achieve more sustainable agriculture that adequately feeds people, contributes to rural development, and provides livelihoods to farmers without destroying the natural resources. Organic agriculture shows several benefits, as it reduces many of the environmental impacts of conventional agriculture, it can increase productivity in small farmers’ fields, it reduces reliance on costly external inputs, and it guarantees price premiums for organic products. However, organic farmers in developing countries need to access international markets, and they often require costly certification and have increased demand for labor. On the contrary, current agriculture fails in achieving these goals on numerous ends; agriculture today is not only a leading driver of environmental degradation but also a major cause of undernourishment due to lack of sufficient access to nutritious food (Ghattas, 2014). Furthermore, doubling the food production will be required by 2050 to feed nine billion people with increasing demands for meat and dairy products (Foley et al., 2011). Therefore we need to produce more food at affordable prices to improve farmers’ livelihoods and reduce the environmental cost of agriculture. In developing countries, where three out of four poor people live in rural areas and where more than 80% of rural people are involved in agriculture, improving poor farmers’ livelihoods is central for addressing rural development (World Bank, 2018). Many studies have suggested that “organic” agriculture could contribute substantially to farmers’ food security and improve their livelihoods (Scialabba, 2007; IFAD, 2003; FAO, 2008; Peramaiyan et al., 2009; Halberg et al., 2006). Organic agriculture has several benefits for farmers, including cheaper inputs, higher and more stable prices, and organization in farmer cooperatives. Organic cash crop production is, however, also associated with problems, including potentially reduced yields compared to intensive conventional methods, the costs of certification, and high labor requirements. Whether the benefits of organic agriculture overcome the problems depends on the socioeconomic and agronomic context, for example, the magnitude of the organic price premium, the cost of certification, and the availability of agricultural labor and organic inputs.

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Several characteristics of organic agriculture, like its requirement of high management skills and more agricultural labor, as well as its incorporation into an international commodity market, can provide considerable barriers for small farmers to adopt organic management or to gain benefits from organic farming. To achieve environmental sustainability, good organic management practices need to be applied to achieve high yields, and organic practices need to be adapted to local conditions. Economic sustainability of organic agriculture depends on adequate prices for organic produce and the accessibility of international organic markets. To enhance the social sustainability of organic agriculture, certification costs should be kept to a minimum and, even better, should be shared by both consumers and producers (Fig. 2). Some developing countries are still reluctant to consider organic farming approaches instead of the existing food systems because of lower yields in organic farming compared to conventional farming, which may lead to food shortages and public anger. Nonetheless there are a number of organic agricultural techniques that could be applied to enhance traditional and other agricultural practices to promote sustainable agriculture and rural development. The international community needs to assist developing countries to use and take advantage of this sustainable technology. Thus not many policy changes in support of organic agriculture have occurred.

FIG. 2 Organic agricultural land and other areas, 2014. Data from Willer, H., Lernoud, J. (Eds), 2017. The World of Organic Agriculture: Statistics and Emerging Trends 2017. FiBL/IFOAM, Frick/Bonn, p. 21.

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2 ORGANIC FARMING LEGISLATION Organic agriculture legislation is usually circumscribed by two criteria: (1) which production systems and products thereof are governed by the legislation and (2) the operations requiring formal certification to qualify for labeling as organic. The standard details which practices, inputs, ingredients, and so forth, are required, permitted, and prohibited in organic food production and processing. Farmers and processors submit plans that explain how they will meet the standard and submit to an annual inspection by the certification agent. Voluntary standards and certification were, however, only successful to a certain level, and in the beginning of 1980s, several states put in place laws or regulations on organic production and labeling, leading to a variety of organic standards and approaches to certification. As the organic market grew nationally, pressure mounted for the adoption of regulatory measures at the federal level. In fact, the “Alar Report,” published in 1989, revealed that the US domestic market was flooded with produces that were fraudulently claimed to be organic. This revelation helped to solidify political and stakeholder support for a national organic program that would require certification to one common set of organic standards. In 1990, the US Congress passed the Organic Foods Production Act (OFPA) 187 (last amended in 2005). OFPA mandated creation of a National Organic Program (NOP) and a National Organic Standards Board (NOSB). The NOP is the federal body responsible for writing, interpreting, and enforcing the Organic Regulations, which are the National Organic Standard. The NOP is part of the USDA and is administered under the Agricultural Marketing Service (AMS).

2.1 Keys Elements to the Standard The National Organic Standard is a large document. However, highlighting some of the key elements of the Regulation can aid in understanding the evolution of organic agriculture and the present state of affairs. In general, key elements of the National Organic Standard include: Certification requirement. All organic producers and handlers must be certified through accredited certifying agents. Certification is optional for operations selling less than $5000 of organic product annually. Organic system plans. Every operation must submit an Organic System Plan (OSP) as part of the application for certification. The OSP details how the operation will comply with the National Organic Standard. A complete OSP includes all inputs to be used, production practices, strategies to prevent contamination and commingling, monitoring procedures, and records to be kept. Records keeping. Detailed documentation of inputs, field activities, crop yields, and sales must be kept. These records should accurately reflect the OSP. Most operations need to develop an audit control system to track production, ensure NOP compliance, and provide critical information in the event of product recall. For crop production, additional key elements include: Land integrity. For land to become certified organic, it must have distinct boundaries and be buffered from chemical sprays and other forms of contamination. The National Standard

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does not specify the width of buffer zones or even specifically require them. It requires only that contamination be prevented. So, in most circumstances, buffers are a practical option. Customarily, certifiers accept 25-foot-wide buffer zones when neighboring farmland or roadsides are ground-sprayed. However, much wider buffers are usually required where aerial application is used. Biodiversity and natural resource protection. Biodiversity and natural resource protection are at the core of humus/organic farming. Crop rotation is one of the main supportive practices; it is specifically required by the National Organic Standard under §205.205. Because crop rotation is a practice associated with annual crops, it would appear to leave perennial systems without a requirement or a strategy. However, the definition of crop rotation under §205.2 includes the statement: “Perennial cropping systems employ means such as alley cropping, intercropping, and hedgerows to introduce biological diversity in lieu of crop rotation.” Therefore the National Standard requires a temporal biodiversity strategy for annual crops and a spatial strategy for perennial plantings. As for resource protection, there are several provisions within the National Standard similar to §205.203(c), which reads: “The producer must…not contribute to contamination of crops, soil, or water by plant nutrients, pathogenic organisms, heavy metals, or residues of prohibited substances.” As in the case of land integrity, the National Standard is “nonprescriptive.” It requires that contamination be prevented and allows the farmer and the certifier to agree on the strategy. Food safety. The National Standard becomes quite “prescriptive,” requiring that livestock manure either be composted or applied a minimum number of days prior to harvest; it prohibits sewage sludge completely. The composting requirements in the Regulation reflect EPA requirements for the composting of biosolids to ensure safe use. Seed and planting stock. The NOP made it clear at the outset that it sought to create more sources for organic seed and planting stock to bolster organic agriculture. As a result, organic production requires organic seed and planting stock. Only if a needed variety is not commercially available may the grower use untreated, non-GMO, nonorganic seed and stock. Annual transplants must be grown organically, although variances may be granted in cases where a farm’s organic transplants are accidentally destroyed. Prohibited substances. The rule of thumb is that nonsynthetic (natural) materials may be used in organic crop production unless they are specifically prohibited and cataloged on the National List under §205.602. Synthetic materials are automatically prohibited unless specifically allowed on the National List under §205.601. Although this appears straightforward, there are many “real world” complications. Among the problems: • Although manures from conventional confined animal feeding operations are allowed, high levels of contamination with heavy metals or other substances may prohibit their use. • Multiingredient pest control products may contain only EPA List 4 and a few select List 3 inert ingredients. • The definitions of synthetic and nonsynthetic lack clarity. This has been discussed by the NOSB for several years, but resolution is slow in coming. Organic agriculture emphasizes systems design and cultural practices and shuns input substitution—the strategy of simply replacing conventional inputs with organically

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acceptable methods. Still, at the farm level, the issue of what can and cannot be used in organic agriculture has become the most compelling. The reason is clear: a single misapplication of a prohibited substance to a crop not only decertifies that crop, the entire field becomes decertified for 3 years. For those producers dependent on a market premium, such mistakes can be catastrophic. For livestock production, the National Organic Standard contains additional key elements. These include: Origin of livestock. Essentially, the Regulation requires that slaughter stock be under organic management from the last third of gestation. Dairy stock, by contrast, can, in many instances, be transitioned to organic milk production in 12 months. Poultry can be transitioned if under organic management from the second day of life. Livestock feed. Organic livestock must be fed 100% organic feed. Synthetic hormones and antibiotics are prohibited in organic feed; so are plastic pellets, urea, manure, and slaughter by products. Synthetic feed supplements and additives are allowed only if they are on the National List at §205.603(c) or §205.603(d), respectively. Living conditions. When it comes to living conditions, the National Standard reflects the considerable influence the animal welfare community has had on its development. Living conditions must accommodate the natural behavior of each livestock type. Outdoor access, fresh air and sunlight, and space to exercise are required. Shelter must also be provided and must allow natural maintenance and behavior, must provide protection from temperature extremes, have adequate ventilation, and be safe. Some specific details include required pasture access for ruminants and provision of bedding, which must be organic if it is consumed. Temporary confinement is allowed only as protection from inclement weather, if required for a specific stage of production, to protect soil and water quality, or to ensure the health and safety of the animals. Waste management. Manure must be managed in a manner that does not contribute to contamination of crops, soil, or water by plant nutrients, heavy metals, or pathogenic organisms, and which optimizes recycling of nutrients. Under ideal circumstances, manure is returned to the land from which feed is harvested, preferably on the same farm. Health care. Organic livestock health care begins with prevention. This includes selection of livestock species and type, nutrition, proper housing and pasture, sanitation, stress reduction, and vaccination. There are also restrictions on physical alterations. Producers may not withhold treatment from a sick animal in an effort to preserve its organic status. Sick animals may be treated using natural therapies such as herbs, homeopathics, flower remedies, essential oils, acupuncture, radionics, etc. Synthetic medications on the National List at §205.603(a) may also be used. All appropriate medications must be used to restore an animal to health when methods acceptable to organic production fail. Synthetic parasiticides on the National List at §205.603(a) may also be used, but they are highly restricted. External parasites and other pests may be controlled using nonsynthetic pest means such as traps, botanicals, biologicals, and mineral-based materials like diatomaceous earth. Livestock treated with a prohibited substance must be clearly identified and may not be sold, labeled, or represented as organically produced. GMO crops. There is a clear and thorough prohibition against genetically engineered Bacillus thuringiensis (Bt) crops, which is capable of making a biological poison toxic to some

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insect pests. Organic growers were already using various commercial spray and dust formulations of Bt in the field and had no compunctions about it. Still, genetically engineered crops, including those with Bt genetics, were rejected by the organic community. The impacts of genetically engineered crops, animals, and agricultural inputs are not yet well understood and have not been clearly proven harmful, but in the eyes of the organic community, enough concern has been raised to prohibit their use for the foreseeable future.

2.2 EU Organic Farming Policy: Background History In the beginning of the 1990s, organic farming had rapidly developed in almost all Member States of the EU. In 1991, in the context of EU farm policy reform, the European Council of Agricultural Ministers adopted Regulation (EEC) No 2092/91 on organic farming and the labeling of organic farm produce and foods. Initially it covered only plant products. Further rules on animal products were introduced later, covering (1) animal feed, (2) prevention of illness, (3) veterinary treatment, (4) animal protection, (5) livestock breeding, and (6) the use of livestock manure. In 2007, the European Council of Agricultural Ministers agreed on a new Council Regulation (Council Regulation EC No. 834/2007, 2008) setting out the principles, aims, and overarching rules of organic production and labeling of organic products. The regulation set a new course for developing organic farming further, with the following aims: (1) sustainable cultivation systems, (2) a variety of high-quality products, (3) greater emphasis on environmental protection, (4) more attention to biodiversity, (5) higher standards of animal protection, (6) consumer confidence, and (7) protecting consumer interests. Organic production respects natural systems and cycles. Closed cycles using internal resources and inputs are preferred to open cycles based on external resources. If the latter are used, they should be (1) organic materials from other organic farms, (2) natural substances, and (3) materials obtained naturally or mineral fertilizers with low solubility. Exceptionally, however, synthetic resources and inputs may be permissible if there are no suitable alternatives. Such products, which must be scrutinized by the Commission and EU countries before authorization, are listed in the implementing regulation (Commission Regulation [EC] No. 889/2008).

2.3 EU New Labeling Regulation Foods may be labeled “organic” only if at least 95% of their agricultural ingredients meet the necessary standards. In nonorganic foods, any ingredients that meet organic standards can be listed as organic. To ensure credibility, the code number of the certifying organization must be provided. The regulation on genetically modified food and feed lays down a threshold (0.9%) under which a product’s GMO content does not have to be indicated. Products with GMO content below this threshold can be labeled organic. Since July 1, 2010, producers of packaged organic food have been required under EU law to use the EU organic logo. However, this is not a binding requirement for organic foods from non-EU countries. When the EU organic logo is used, the place where any farmed ingredients were produced must be indicated.

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2.4 EU Imported Organic Products Organic products from non-EU countries can be distributed to the EU market only if produced and inspected under conditions identical or equivalent to those applying to EU organic producers. The rules introduced by the 2007 regulation are more flexible than the previous set-up, under which organic goods could be imported from outside the EU only if they were EU-certified, their production was monitored by the EU countries, and an import license had been issued. The import license procedure has been replaced by new import rules. Control bodies (certifying organizations) operating in non-EU countries are now directly authorized and monitored by the European Commission and EU countries. Nevertheless, the original regulation was important because it laid down EU-wide minimum standards enabling consumers to buy organic products in any EU country with the certainty that they met the same minimum requirements. EU governments and private organizations were free to introduce stricter standards when they so wished. On March 24, 2014, the European Commission adopted legislative proposals for a new regulation on organic production and labeling of organic products. The legislative proposals are accompanied by an impact assessment that evaluates alternative scenarios for the evolution of the policy. The Commission also adopted an Action Plan on the future of organic production in Europe to help organic farmers, producers, and retailers adjust to the new policy and meet future challenges. On June 28, 2017, the Maltese presidency and the European Parliament reached a preliminary agreement on an overhaul of the existing EU rules on organic production and labeling of organic products. The agreed-upon regulation sets more modern and uniform rules across the EU with the aim of encouraging sustainable development. The new rules also: – aim to guarantee fair competition for farmers and operators, – prevent fraud and unfair practices, – improve consumer confidence in organic products. The much “anticipated agreement” comes after 3 years of intense negotiations and will have to be formally endorsed by the Council and the Parliament.

3 BRIEF HISTORY OF ORGANIC AGRICULTURE IN JAPAN The Japanese Agricultural Standard (a broad system of standards concerning agricultural and forestry products, consisting of the “Japanese Agriculture Standards (JAS) System” and the “Quality Labeling Standards System”) regulates labeling of agricultural products (not only organic) and is governed by the Ministry of Agriculture, Forestry, and Fisheries of Japan (MAFF). The labeling standard came into force in 1950 with Law N° 175, “The Law Concerning Standardization and Proper Labeling of Agricultural and Forestry Products.” In 2000, the JAS Standard has been extended by requirements for organic production and processing of plant products. Enforcement date of the organic certification program was April 1, 2001. Since this date, all agricultural plant products meant for human consumption sold in Japan must carry the JAS organic seal. In 2005, regulations for the organic production of livestock and feed have been added.

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3.1 Overview of the Organic Japanese Agricultural Standard System Production and processing of organic products for the Japanese market is regulated by the JAS. Certified products are identified with the official JAS organic seal of the Japanese government. In 1999, inspection and certification system for organic foods was first introduced; the principle of organic production was in line with the Codex Guideline and must be certified according to Organic JAS in 2000. Only producers certified by registered certifying bodies accredited by the Minister of Agriculture, Forestry, and Fisheries are able to label as organic and use the Organic JAS mark on the products. All organic products (foodstuffs) that shall be labeled with “organic” for sales in Japan must be labeled with the JAS seal and the JAS standard (Fig. 3).

3.2 Key Features of the Japanese Standard for Organic Products See Table 2.

Minister of agriculture, forestry and fisheries Accreditation

Registered certifying bodies Certification

Manufacturers

Consumers

Repackers

Retailers

Production process managers

FIG. 3 The inspection and certification system of Japan. TABLE 2 Key Features of the Japanese Standard for Organic Products (MAFF, 2012) Key features of the JAS standard for organic agricultural products

1. Use of composts and “nonuse” of prohibited agricultural chemicals and fertilizers for no less than 2 years before sowing or planting 2. “Nonuse” of prohibited agricultural chemicals and fertilizers for production periods 3. “Nonuse” of recombinant DNA technology

The criteria for the method of organic production

Natural recycling function of agriculture should be maintained or increased by: – “Nonuse” of chemically synthesized fertilizers and agricultural chemicals – Exercising the productivity of the soil – Applying the cultivation method to minimize load to the environment as much as possible

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Key Features of the Japanese Standard for Organic Products (MAFF, 2012)—cont’d

Conditions for fields

– Use of composts and “nonuse” of prohibited agricultural chemicals and fertilizers for no less than 2 years before sowing and planting (3 years for perennial plants) – Under the proper management so as to prevent drifting and flowing of prohibited substances during the production periods

Manuring practice

– The productivity of the soil should be maintained or increased by composts from residues of products in the fields and the use of functions of organism in the fields or in the surrounding areas – The use of fertilizers and soil conditioners may be permitted only in cases where the methods previously identified are not effective for maintaining or increasing the productivity of the soil

Major fertilizers and soil conditioners

Natural substances or those derived from natural substances without the use of chemical treatment and chemical additives – composts – fertilizers of animal and plant origins (substances from food industries) – fertilizers of mineral origin (source of P, K, Ca, Mg, S, Si) – trace elements – soil conditioners of mineral origin (perlite, vermiculite, and others)

Criteria for seeds and seedlings

Use of organically produced seeds and seedlings – Use of seeds for seed reproductive plants and the youngest available seedlings for vegetative reproductive plants – “Nonuse” of recombinant DNA technology

Controlling noxious animals and plants

Mechanical cultivate, physical or biological protections, or in combination – The use of agricultural chemicals may be permitted only in cases of imminent or serious threat to the crop and where the measures previously identified are not effective – Those of plant origin: pyrethrins, canola oil, lecithin, lentinus edodes mycelium extract liquid – Those of mineral origin: sulfur, bordeaux mixture – Biological control and biopesticide formulation, natural enemies – Other: sex pheromone agent, metaldehyde, carbondioxide

The JAS for organic processed foods; Key features of the standards

– The use of chemically synthesized food additives and chemicals should be a last resort – Final products contain no less than 95% of organic ingredients, other than water and salt – “Nonuse” of recombinant DNA technology

The JAS for organic livestock products; Key features of the standard

– Provide organically produced feeds – Rearing management such as regular exercise and access to pasture and/or open-air runs, so as not to stress livestock – “Nonuse” of antibiotics for the purpose of preventing diseases – “Nonuse” of recombinant DNA technology

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FIG. 4 Number of countries across the world that have adopted organic farming regulations. FI*, fully implemented standards and regulations officially endorsed as organic by IFOAM; FI, fully implemented but not endorsed as organic by IFOAM; NFI, not fully implemented; UP, under process.

23

33

9

Africa Asia and Pacific region The Americans and Caribbean Non-EU Europe EU Europe Total

FI*

FI

NFI

107 3 2 6 7 0 18

18 0

28

43

0

2 3 12 1

7 14

7

28

0

2 4 8

1

28

14

48

UP

Total

4 ORGANIC REGULATION WORLDWIDE: CURRENT STATUS According to the FiBL 2016 survey on organic rules and regulations, there are 105 countries with organic standards either fully implemented, not fully implemented, or under process. Huber et al. (2016) have grouped these into regions such as EU Europe, non-EU Europe, Asia and Pacific Region, The Americas, Caribbean, and Africa, and documented that 41 out of 87 countries have fully implemented standards and regulations officially endorsed as organic by IFOAM (as shown in Fig. 4).

4.1 International Federation of Organic Agriculture Movements IFOAM is the international nongovernmental organization providing an umbrella for all organic agriculture organizations. Currently uniting around 784 member organizations in more than 172 countries, its goal is the worldwide adoption of ecologically, socially, and economically sound systems based on the principles of organic agriculture. Through international conferences, meetings, and other forums, IFOAM facilitates an ongoing dialogue about the status and future of organic agriculture. IFOAM has developed and maintains the Organic Guarantee System (OGS), which seeks to provide a common system of standards, verification, and market identity for the organic world. IFOAM also implements specific projects that facilitate the adoption of organic agriculture methods, particularly in developing countries, and represents the organic agriculture movement at the United Nations and other intergovernmental agencies. According to the IFOAM, there are 172 countries adopting organic agriculture in the world, consisting of 43.7 million hectares of organic agricultural land, which is 0.5 million hectares more than in 2013; almost 1% of the agricultural land on this planet is organic, and 11 countries have more than 10% organic agricultural land. More than three-quarters of the organic agricultural lands are in developing countries used by 2.3 million organic farmers. The worldwide scenario of organic agriculture is given in Table 3.

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TABLE 3

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The Worldwide Organic Agriculture Scenario

Indicator

World

Leading Countries

Countries with data on certified organic agriculture

2014: 172 countries

New countries: Kiribati, Puerto Rico, Suriname, United States Virgin Islands

Organic agricultural land

2013: 43.7 million hectares (1999: 11 million hectares)

Australia (17.2 million hectares, 2013) Argentina (3.1 million hectares) United States (2.2 million hectares, 2011)

Share of total agricultural land

2014: 0.99%

Falkland Islands (Malvinas) (36.3%) Liechtenstein (30.9%) Austria (19.4%)

Further, nonagricultural organic areas (mainly wild collection)

2014: 37.6 million hectares

Finland (9.1 million hectares) Zambia (6.18 million hectares) India (4 million hectares)

Producers

2.3 million producers (2013: 2 million producers; 2012: 1.9 million producers)

India (650,000; 2013), Uganda (190,552), Mexico (169,703; 2013)

Organic market size

80 billion US dollars (1999: 15.2 billion US dollars)

United States (35.9 billion USD; 27.1 billion euros) Germany (10.5 billion USD; 7.9 billion euros) France (6.8 billion USD; 4.8 billion euros)

Per capita consumption

2014: 11 US dollars

Switzerland (210 euros) Denmark (163 euros) Luxemburg (157 euros)

Number of countries with organic regulations 2015

87 countries

Number of IFOAM affiliates

2015: 784 affiliates from 117 countries

Germany—91 affiliates, China—57 affiliates, India—44 affiliates, United States—40 affiliates

Reproduced with permission from Willer, H., Lernoud, J. (Eds), 2017. The World of Organic Agriculture: Statistics and Emerging Trends 2017. FiBL/IFOAM, Frick/Bonn, p. 21.

4.2 IFOAM Organic Agriculture Guideline The IFOAM World Board, based upon the recommendation of the IFOAM membership, appoints members to IFOAM’s many official committees, working groups, and temporary task forces, which address specific aspects of organic agriculture management. The IFOAM Standard Committee and the Accreditation Requirements Committee play an essential role in the development and continual improvement of the OGS. These committees work on the development and maintenance of the IFOAM Standards, requirements of organic standards, and accreditation. In 2005, the IFOAM offered the OGS of products and services, designed to facilitate the development of quality organic standards and certification worldwide and

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to provide an international assurance of those standards and certification. The IFOAM OGS includes the following: 1. 2. 3. 4. 5.

The IFOAM Family of Standards The IFOAM Standard for Organic Production and Processing The IFOAM Community of Best Practice Standards The Global Organic Mark IFOAM Accreditation and the Global Organic System Accreditation (GOSA)

The IFOAM Standards Requirements are composed of the Common Objectives and Requirements of Organic Standards (COROS), which was jointly developed by the IFOAM OGS and the Global Organic Market Access (GOMA). In the context of the IFOAM OGS, COROS serves as an international reference against which organic standards and technical regulations can be assessed for the purpose of inclusion in IFOAM’s Family of Standards. Governments could also consider using the Family of Standards as a basis for authorizing imports of organic products. Governments may also use the equivalence assessments done by IFOAM against COROS as a resource to facilitate their own unilateral or bilateral assessments on equivalence. IFOAM accreditation and the GOSA are two means to be accredited certification bodies. Both accreditations are based on the IFOAM Accreditation Requirements for certification of organic production and processing. The IFOAM Accreditation Requirements is the new name for the former Accreditation Criteria for Certification of Organic Production and Processing (IAC), which derive from the ISO norms for the operation of certifying bodies (ISO 65),but also reflect the particular circumstances of organic production and processing. IFOAM established its requirements for certification bodies to conduct the organic activities. Certification bodies can apply to the International Organic Accreditation Service (IOAS, a daughter company of IFOAM) to obtain either: • IFOAM Accreditation, if their procedures are in compliance with the IFOAM accreditation requirements and they use the IFOAM Standard or a compliant standard to certify operators, • GOSA, if their procedures are in compliance with the IFOAM accreditation requirements and they use any standard listed in the IFOAM Family of standards to certify operators. Although IOAS operates as an independent body, it is a key organ of the OGS accepting and reviewing accreditation applications, conducting site evaluations, and granting accreditation.

4.3 The IFOAM Standard for Organic Production and Processing The IFOAM Standard is based on four principles considering the “roots” of the organic agriculture diversity. The principles include: • Health: Organic agriculture is expected to “sustain and enhance the health of soil, plant, animal, human, and planet as one and indivisible,” with the understanding that health is not only the absence of illness but also the maintenance of physical, mental, social, and ecological well-being (thereby including the concepts of regeneration, immunity, and resilience). This principle underlines the need to avoid in organic agriculture the use of fertilizers, pesticides, animal drugs, and food additives having negative health effects.

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• Ecology: Organic agriculture is expected to be “based on living ecological systems and cycles, work with them, emulate them and help sustain them.” This principle calls for reducing agricultural inputs by reusing, recycling, and efficiently managing materials and energy with a view to maintaining and improving environmental quality, conserving natural resources, and maintaining genetic and agricultural diversity. • Fairness: Organic agriculture is expected to rely on relationships that ensure fairness toward the environment and life opportunities, therefore characterized by equity and respect, contributing to food sovereignty and poverty reduction, requiring open and equitable production, distribution and trade, and accounting for real environmental and social costs. • Care: Organic agriculture is expected to be managed in a precautionary and responsible manner to protect the health and well-being of current and future generations and the environment. This should be not only based on scientific knowledge but also on practical experience and traditional and indigenous knowledge. Besides providing definitions, the IFOAM Standard covers the following: • Organic ecosystems: Ecosystem management, soil and water conservation, genetic engineering, wild harvested products, and common/public land management; • General requirements for crop production and animal husbandry: Conversion requirements, split production and parallel production, maintenance of organic management; • Requirements specific to crop production: Choice of crops and varieties; length of conversion period; diversity in crop production; soil fertility and fertilization; pest, disease, weed and growth management; contamination avoidance; • Requirements specific to animal husbandry: Animal management, length of conversion period, animal sources/origin, breeds and breeding, mutilations, animal nutrition, veterinary medicine, transport and slaughter, bee keeping; • Processing and handling: Ingredients; processing methods; pests and disease control; packaging; cleaning, disinfecting, and sanitizing of food processing facilities; and textile fiber processing; • Labeling: A slip of paper, cloth, or other material marked or inscribed for attachment to something to indicate its manufacturer, nature, ownership, destination, etc. • Social justice: Concerning labor and human rights, nondiscrimination, and equal opportunities for all; • Criteria for the evaluation of inputs, additives, and processing aids authorized in organic production and processing; • Lists of permitted substances, including fertilizers and soil conditioners, crop protectants and growth stimulators, additives and processing aids, and equipment cleansers and disinfectants.

4.4 Development of Harmonization and Equivalence Tools In spite of the IFOAM, there still exist numerous and disparate national and private organic standards. The emergence of multiple organic standards and highly technical regulations has created trade barriers between markets. A product produced according to one set of

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organic standards and certification requirements may also need to comply with other organic standards and requirements to be traded. The labyrinth of requirements in both governmental and private sectors constitutes an obstacle to trade, which constrains organic market development and denies market access to many, including hundreds of thousands of small producers in developing countries. Thus an international task force on harmonization and equivalence in organic agriculture (ITF) was formed in 2003, which consists of individuals working in government agencies, intergovernmental agencies, civil society, and other private sector organizations involved in organic agriculture regulation, standardization, accreditation, certification, and trade. The goals of the ITF were to address and seek solutions to trade barriers arising from the many different standards, technical regulations, and certification requirements that function in the organic sector, and to enable developing countries to have more access to organic trade. It focused on opportunities for harmonization, recognition, equivalence, and other forms of cooperation within and between government and private OGS. The ITF reviewed all documents (technical papers, recommendations, tools, etc.) for 5 years and, in 2008, the IFT established two practical tools for harmonization and equivalence: 1. The International Requirements for Organic Certification Bodies (IRoCb), a reference norm that can be used by governments, and private accreditation and certification bodies as a means of accepting certification of organic products outside of their own system. 2. The Guide for Assessing Equivalence of Organic Standards and Technical Regulations (equiTool), a set of procedures and criteria for deciding when a standard applicable in one region of the world is equivalent to a standard applicable in another region.

5 US FDA FOOD SAFETY MODERNIZATION ACT Despite having one of the safest food supplies in the world, it is estimated by the US Centers for Disease Control and Prevention that nearly 48 million people (roughly 1 in 6 Americans) are sickened annually. Furthermore, frequent high profile and deadly foodborne outbreak incidences occurring in 2008–10 have prompted policy-makers and their constituents to improve food safety. In response to such events, the US Congress has passed historic new legislation, the first major reform of the US Food and Drug Administration (FDA) food safety authority in more than 70 years. The FDA Food Safety Modernization Act (FSMA) was signed into law by President Barack Obama on January 4, 2011. The law is intended to shift FDA focus to better protect public health by preventing food safety issues rather than reacting to outbreaks. The regulations continue to evolve with each new event and with the continued engagement of the FDA with stakeholders including farmers, researchers, educators, university extension, state departments of health and agriculture, produce buyers, consumers, and the food industry. FSMA alters the role of FDA in food safety through five key changes: 1. A shift of focus from reaction to prevention, including preventing intentional contamination 2. More authority to inspect and assure compliance with inspection frequencies based on risk

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3. Mandatory recall authority 4. Authorities to strengthen import safety to ensure that US food safety standards are met 5. Stronger partnerships with other government agencies and private entities. The law provides the FDA with new enforcement authorities designed to achieve higher rates of compliance with prevention and risk-based food safety standards and to better respond to and contain problems when they do occur. The law also gives the FDA new tools to hold imported foods to the same standards as domestic foods and directs the FDA to build an integrated national food safety system in partnership with state and local authorities. Building a new food safety system based on prevention may take time, thus Congress has established specific implementation dates in the legislation. The FDA is committed to implementing the requirements through an open process with opportunity for input from all stakeholders. For the first time, the FDA will have a legislative mandate to require comprehensive, science-based preventive controls across the food supply, as everyone has a role in the “food safety continuum.” The job of the FDA is to regulate food safety, but it is the responsibility of each producer/company to ensure the safety of their food products until the consumer takes over responsibility. FSMA is in the midst of a lengthy rule-making and guidance process, which means the FDA is turning the bill passed by Congress into actual rules, regulations, and related guidance documents. Guidance documents, although not regulations, can be equally as important to industry as formal regulations. Failing to follow issued guidance could significantly increase liability risk in the event of a food safety incident. FSMA is mainly focused on human health implications, and failing to address food safety risks from genetically engineered crops, pesticide use, or antibiotic resistance. On the contrary, the organic programs not only offer attention to human health but also give thrust at a time to sustain and enhance the health of soil, plant, animal, and human as one and indivisible. Therefore the principle is entirely different and not comparable or supplement each other as the certification process also unalike. In the United States, NOP is regulated by USDA and FSMA by FDA, two separate organs of the state. However, after introduction of FSMA, it has created a need to clarify details concerning how organic operations will be impacted by the new requirements and to answer stakeholders. How does FSMA, compliance to food safety practices, and organic certification meet, and how can growers encounter new federal regulations aimed at preventing food safety issues while expanding practices to increase biodiversity? FSMA and the NOP are based in two different federal agencies, but there are areas of common ground as both are focused on production practices. Therefore this part of the chapter will address stakeholder’s clarification. Specifically, there are many aspects of FSMA that touch the USDA and NOP. In fact, the NOP and the FSMA share at least three significant similarities: (1) set standards must be met, (2) documentation is required, and (3) size of operation influences compliance levels. A comparison of organic and FSMA is given in Table 4.

5.1 Labeling FSMA: A package of produce in a labeled container (like a clamshell) “must include prominently and conspicuously on the food packaging label the name and the complete business address of the farm where the produce is grown.” This must be implemented by January 1,

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TABLE 4 Key Comparison of Organic and FSMA to Fulfill the Stakeholder Interests Organic

FSMA

Authority and regulation

“USDA Organic Regulations”

“FDA Produce Safety Rule”

• Law: Organic Foods Production Act (OFPA) • Regulation: National Organic Program, USDA Organic Regulations 7 CFR Part 205 http://www.ecfr.gov/cgi-bin/text idx?tpl¼/ecfrbrowse/ Title07/7cfr205_main_02.tpl • Guidance: NOP Handbook http://www.ams.usda.gov/rulesregulations/organic/ handbook

• Law: Food Safety Modernization Act (FSMA) • Regulation: Final Rule on Produce Safety 21 CFR Part 112 Standards for Growing, Harvesting, Packing, and Holding Produce for Human Consumption http://www.fda.gov/Food/GuidanceRegulation/FSMA/ ucm334114.htm

NOP §205.100: Any production or handling facility selling less than $5000 annually is exempt from the requirement for certification

FDA FSMA Exempt Farms Subpart A §112.4: Any farm or mixed farm facility that has a $25,000 average annual sales or less of covered produce during the previous 3-year period

Exemptions

• Exempt operations selling as organic must follow all other regulatory requirements, including recordkeeping Written plan

To get USDA organic certification, it is mandatory to include a description of: – – – – –

Land

practices and procedures list of materials to be used monitoring recordkeeping system contamination prevention

Land use history mandatory including conversion time – No use of materials (synthetic fertilizers, pesticides, sewage sludge, etc.) for 36 months before harvest of a crop to be sold or represented as organic – Boundaries and buffers prevent contamination (describe in OSP; attach map)

Worker health and hygiene

This topic is not addressed directly by USDA organic regulations

The FDA does not specifically require a food safety plan – Regulations do require an operational assessment of food safety risks and documentation of practices and procedures to minimize pathogen risks – Non-FDA third-party food safety certification requires a Food Safety Plan; format and content vary according to standards to be met Operational risk assessment is required but conversion time is not mandatory: – Evaluate past or present land use; including adjacent and nearby lands: – industrial uses – landfill or waste disposal – animal husbandry – flooding Risks may affect requirements for water testing profiles Supervisor or responsible party must successfully complete an FDA-approved training in food safety and the importance of personal health and hygiene

3. POLICIES AND REGULATIONS ON ORGANIC FARMING WORLDWIDE

A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

Features

Natural resources and domesticated and wild animals

– Maintain or improve the natural resources of the operation, including soil, water, wetlands, woodlands, and wildlife – Prevent contamination of crops, soil, or water by plant nutrients, pathogenic organisms, heavy metals, or residues of prohibited substances

– Monitor crop production and handling areas for evidence of domestic or wild animal intrusion – Prevent contamination of produce by pathogens from animals, both domesticated and wild, and the environment

Crop nutrient and pest management

Producers track all inputs used in crop production:

– Produce Safety Rule doesn’t directly address this topic. – For third party food safety certification, producers must verify and document that inputs do not present a food safety hazard, and record all inputs including application method

1. Biological soil amendments not of animal origin

– OSP materials list – Purchase receipts – Application records (date, rate, crop, location)

Crop nutrient and pest management

Composting process for plant and animal materials with an initial C:N ratio of 25:1 to 40:1.

2. Biological soil amendments of animal origin

• In vessel or static aerated pile, the temperatures maintained between 55°C and 77°C at least 3 days, or • In a windrow, temperatures maintained between 55°C and 77°C for 15 days during which it is turned a minimum of 5 times. • Raw manure must be incorporated – Not less than 90 days prior to harvest of a crop that does not have direct contact with the soil – Not less than 120 days prior to harvest of a crop that does have direct contact with the soil surface.

Scientifically validated treatment process was used and: • Handling, conveyance, and storage of product is adequate to minimize the risk of contamination by an untreated or in process BSAAO – If purchased from a third party, Certificate of Conformance and Certificate of Analysis required at least annually – If self-prepared, record of treatment process controls: time/temperature/turning schedule with signature of responsible party • Raw manure—further research will provide future regulation; currently, no application interval is given

5 US FDA FOOD SAFETY MODERNIZATION ACT

A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

• Personnel and volunteers must receive basic training in principles of food safety, and the importance of health and personal hygiene • Those harvesting crop receive training on preharvest inspection of produce and harvest equipment/ packaging materials • Record: Worker Training Log/certificates required

Continued

55

Organic

FSMA

Crop nutrient and pest management

Use preventative practices: crop rotation, cultural, biological, physical, and mechanical controls

Produce Safety Rule does not directly address this topic

3. Pest management practices and plant protection products

Crop nutrient and pest management 4. Seed and planting stock

• Allowed materials may be applied to prevent, suppress, or control pests, weeds, or diseases only when preventative controls are insufficient; and • OSP includes: preventive pest management practices, allowed materials list, and conditions for intended use Annual seedlings and seed for edible sprouts must be organic • Must use organically grown seed and planting stock; – May use nonorganic, untreated, non-GMO seed or stock when an equivalent organic variety is commercially unavailable (form, quality, or quantity) Document of • Inoculants must be non-GMO • Seed treatments must be allowed • Perennial stock sold as organic must be managed organically 1 year

Water 1. Crop production: Irrigation, fertilizer, and pesticide application

Water

Any material used to clean or sanitize the irrigation system must be listed in OSP and approved by certifier for its intended use • Allowed: – Alcohols (ethanol and isopropanol) as algaecides, disinfectants, sanitizers, irrigation system cleaning – Chlorine (see Guidance) – Copper sulfate, as algaecide in aquatic rice systems – Ozone gas, as an irrigation system cleaner only Any material used in wash water or surfaces that come into contact with crops must be in your OSP and approved for

• Local County Agriculture Commissioners require Pesticide Use Reports

Produce Safety Rule gives detailed measures to prevent and mitigate food safety hazards for seeds or beans for sprouting only – Treatment of seeds or beans for sprouting is required – Bacterial test of growing environment for Listeria required – Bacteria test of spent irrigation water or sprouts for E. coli O157:H7 and Salmonella required About GMO contamination is reluctant.

All agricultural water must be safe and of adequate sanitary quality for its intended use. • – – –

Requirements Inspection of water system Water source sampling methods, frequency, analysis Bacterial analysis: generic E. coli 126 CFU/100 mL and STV – 410 CFU/100 mL – Data collection: verify treatment efficiency, delivery, and any mitigation strategies All agricultural water must be safe and of adequate sanitary quality for its intended use

3. POLICIES AND REGULATIONS ON ORGANIC FARMING WORLDWIDE

A. ORGANIC FOOD PRODUCTS, DIVERSE PRODUCTION PRACTICES, AND POLICIES

Features

56

TABLE 4 Key Comparison of Organic and FSMA to Fulfill the Stakeholder Interests—cont’d

Harvest and postharvest: Tools, equipment, containers, and produce

its intended use • – – – –

Allowed sanitizer materials: Alcohols Chlorine materials 0.05) was observed for polyunsaturated or monounsaturated fatty acid contents (Tables 2 and 3). TABLE 1 Contents of Fat and Fatty Acid in Conventional (C) or Organic (O) Ready-To-Eat Chicken (Shown in Least Square Means; mg/100 g Ready-to-Eat Chicken) (Dalziel et al., 2015) Breast meat (With Skin) Class of Fat and Fatty Acid

C

Leg meat (With Skin)

O bc

C cd

O a

Total fat

5.6

4.9

13.8

11.9a

14:0

25.9b

23.5bc

55.6a

59.7a

16:0

1201b

1070bc

2541a

2478a

16:1 cis-9

246c

176cd

552a

486ab

18:0

350b

363b

716a

790a

18:1 cis-9

2071c

1412d

4518a

3535b

18:2 cis-9,12 (n-6)

815b

910b

1975a

2415a

18:3 cis-6,9,12 (n-6)

5.0b

4.4b

12.1a

12.5a

18:3 cis-9,12,15 (n-3)

123c

76.8c

344a

230b

20:0

1.8b

2.8b

5.7ab

10.0a

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2 BASIC NUTRITIONAL CONTENTS

TABLE 1 Contents of Fat and Fatty Acid in Conventional (C) or Organic (O) Ready-To-Eat Chicken (Shown in Least Square Means; mg/100 g Ready-to-Eat Chicken) (Dalziel et al., 2015)—cont’d Breast meat (With Skin) Class of Fat and Fatty Acid

C

20:1 cis-8

2.4

20:1 cis-11

5.6

Leg meat (With Skin)

O a

C a

1.9

4.4a

3.0

5.4 b

O a

4.7

11.5

20:2 cis-11,14 (n-6)

14.6

13.2

21.2

21.9a

20:3 cis-8,11,14 (n-6)

15.7abc

14.0bc

21.5a

19.8ab

20:4 cis-5,8,11,14 (n-6)

49.1c

70.8bc

87.3ab

105.6a

22:0

3.4abc

1.7c

5.5ab

5.9a

22:1 cis-13

2.5

1.0

4.7

6.2

22:2 cis-13,16 (n-6)

0.91

1.3

1.8

1.1

22:4 cis-7,10,13,16 (n-6)

11.2b

12.5b

18.9a

19.3a

EPA (n-3)1

9.0

10.6

12.1

18.9

DPA (n-3)2

17.1b

20.4ab

28.6ab

31.8a

DHA (n-3)3

12.2b

24.5ab

14.4ab

37.5a

24:0

2.6

1.8

5.7

2.1

24:1 cis-15

1.5

1.1

1.3

1.6

Total SFA4 5

bc

a

1582b

1461bc

3323a

c

cd

a

3343a

Total cis-MUFA

2501

1722

5439

4325ab

Total cis-PUFA6

1074b

1159bc

2538a

2915a

Total n-6 PUFA

911b

1026b

2138a

2595a

Total n-3 PUFA

162c

132cd

399a

318ab

EPA + DHA

21.2

35.0

26.5

56.4

EPA + DPA + DHA

38.3

b

ab

ab

55.4

55.2

88.2a

Numbers sharing same superscript within one row are meant to be significantly different (P < 0.05). 1 EPA: 5,8,11,14,17-eicosapentaenoic acid (20:5, n-3); 2DPA: 7,10,13,16,19-docosapentaenoic acid (22:5, n-3); 3DHA: 4,7,10,13,16,19-docosahexaenoic acid (22:6 n-3); 4SFA: saturated fatty acids5; MUFA, monounsaturated fatty acids; 6 PUFA, polyunsaturated fatty acids. (Reprinted with permission.)

TABLE 2 Components of Conventional and Organic Eggs (Samman et al., 2009) Production Type

Egg Weight (g) a

Yolk (g)

Albumen (g) a

a

Yolk Fat (g/100 g)1

Conventional

61.70
3.70

16.10
1.80

38.3
3.58

4.43
0.55a

Organic

59.62
4.17a

15.87
1.95b

37.3
2.61a

4.45
0.71b

Numbers sharing same superscript within one column are meant to be significantly different (P < 0.05). 1 Data for egg yolk fat are shown as means of conventional (n ¼ 48) and organic (n ¼ 36) samples. (Reprinted with permission.)

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5. FROM A PERSPECTIVE OF NUTRITION: IMPORTANCE OF ORGANIC FOODS

TABLE 3 Composition of Conventional and Organic Egg Fatty Acids (Samman et al., 2009) Content of Fatty Acid (%) Fatty Acid Class

Conventional

Organic

C14:0

a

0.36
0.06

0.35
0.04b

C16:0

25.1
1.07a

25.5
0.94a

C16:1 (n-7)

3.23
0.61

3.03
0.77

a

C18:0

8.37
0.59

8.77
0.69a

C18:1 (n-9)

46.7
3.02

46.0
3.19

C18:2 (n-6)

13.1
3.14

13.1
2.24

C18:3 (n-3)

a

0.51
0.20

0.50
0.15b

C20:4 (n-6)

1.83
0.16a

1.88
0.14b

C22:6 (n-3)

0.85
0.16a

0.84
0.17b

Total saturated

33.8
1.20a

34.6
1.10a

Total monounsaturated

50.0
3.35

49.0
3.12

Total polyunsaturated

16.3
3.50a

16.4
2.56b

Total n-6

15.0
3.23

15.0
2.30

Total n-3

1.36
0.33a

1.34
0.30b

Numbers sharing same superscript within the same column have no significant difference (P 0.05). Generally speaking, part of these scientific reports provided evidence that organic eggs were healthier and could provide more nutrition for consumers compared with their conventional counterparts (Table 12). Ryan, Derrick, and Dann reported that only slight variations were observed for grains regarding the concentration of minerals including potassium, magnesium, nitrogen, calcium, sulfur, and iron. Also, organic grains displayed higher levels of copper and zinc and lower levels of phosphorous and manganese compared with their conventional counterparts. As seen in Table 13, despite all the predictions, organic grains did not show significantly higher levels of minerals compared with their conventional counterparts (Ryan et al., 2004). Giannenas et al. (2009) reported that, in egg yolks, selenium concentration was much lower in conventional eggs compared to their organic counterparts. However, zinc contents of organic eggs were significantly lower compared with the conventional counterparts. No significant difference was observed regarding manganese, cobalt, copper, molybdenum, vanadium, nickel, titanium, arsenic, and chromium concentrations in egg yolks of organic and conventional eggs. As for the egg white part, the concentration of trace elements displayed no significant difference between conventional and organic eggs (Table 14). However, Kristensen et al. (2008) reported that no proven trend was observed for the differences in the content of elements of food products produced organically or conventionally. Actually, the differences caused by the year of harvest were shown to be more obvious than those caused by different cultivation systems. Therefore, this study stood against the theory that organic food products contain higher level of trace elements compared with their conventional counterparts (Table 15). TABLE 12 Mineral Concentration of Organic and Conventional Eggs Based on their Edible Parts (Dry Weight Basis) (K€ uc¸€ ukyılmaz et al., 2012) Minerals (mg/kg)

Conventional

Organic

Ca

2633

2460

a

P

9800

5778b

Mg

533

578

Fe

95.4 a

81.2

Zn

60.0

41.6b

Cu

12.8

11.6

Numbers with different superscripts are significantly (P < 0.05) different in the same row. (Reprinted with permission.) a,b

B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

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5. FROM A PERSPECTIVE OF NUTRITION: IMPORTANCE OF ORGANIC FOODS

TABLE 13 Grain Mineral Concentrations from Organic and Conventional Wheat Crops at Ardlethan (1991, 1992, and 1993) (Ryan et al., 2004) 1991

1992

1993

Element

Conventional

Organic

Conventional

Organic

Conventional

Organic

N(g/kg)

25

23

20

21

22

22

a

b

a

b

a

P(g/kg)

3.0

3.1

3.8

2.8

3.1

2.9b

K (g/kg)

4.1

4.5

2.8

3.0

3.5

3.9

Mg(g/kg)

0.72

0.78

0.46

0.46

0.50

0.55

Ca(g/kg)

0.41

0.49

0.35

0.41

0.35

0.40

S (g/kg)

1.8

1.6

1.2

1.3

1.4

1.4

Fe(mg/kg)

33

29

19

18

21

20

Mn(mg/kg)

43

33

53

30

49

29

Zn(mg/kg)

15a

20b

16a

20b

16a

21b

Cu(mg/kg)

4.4a

5.1b

2.7a

3.7b

2.4a

3.8b

In each year, different letters indicate significant differences between organic and conventional wheat crops (P 1% in heavily farmed organic vegetable-growing systems unless residues with high C:N ratios are used. SOM can supply many of the most important nutrients to plants as some of the nitrogen in the organic matter is converted to plant-available nitrogen (PAN). PAN is the quantity of nitrogen made available to plants in the form of nitrate (NO3) and ammonium (NH4) during the growing season (Berry et al., 2002). A practical estimate of 10–20 pounds of nitrogen per acre is made available each growing season from each 1% of SOM (the assumption is that there are 2000 tons of soil in the top 6 in. of an acre, and each 1% of SOM contains 5% N of which 2% will be mineralized that crop season). Other elements supplied by SOM include phosphorus, potassium, sulfur, iron, copper, and zinc (Gaskell and Smith, 2007).

3 IMPORTANCE OF SOIL PH One of the simplest and most important factors in all plant-growing systems is maintaining optimal pH levels. The optimum pH for the growth of most vegetable crops is between 6 and 7. The pH level of soil influences nutrient solubility, microbial activity, and root growth (Hartz, 2002). High pH (>7.5) favors weathering of minerals, increased bacterial populations, and an increase in the release of cations; however, it also reduces the solubility of salts including carbonates and phosphates (Crozier et al., 2010). Typically, low pH levels (35 results in microbial immobilization. A ratio of 20–30 results in an equilibrium state between mineralization and immobilization. Soil microorganisms have a C:N ratio of around 8. They must acquire enough carbon and some nitrogen from the soil to maintain that ratio in their cells and have been found to do best on a “diet” with a C:N ratio of 24 (Howell, 2005).

B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

197

5 USE OF ANIMAL MANURES

Mineralization: nitrogen is released for plant uptake Immobilization: microbes utilize and tie up nitrogen C:N ratio 5:1 10:1

Mineralization

Immobilization

Equilibrium

*********

Blood, fish, and soybean meal

*********

15:1

Clovers, vetch, peas

*********

20:1

Grasses in vegetative stage

*********

30:1

Rotted manure, compost

*********

40:1

Grasses at seed set, pea straw

*********

>50:1

Feather meal, grass hay

********* Faster

Organic examples

Slower

Slower

Straw, corn stalks

Faster

1

The C:N ratios vary over a range for any organic material and these values represent an average of the range.

FIG. 1 The C:N ratio of some organic material and their mineralization and immobilization rates.

4.3 Linking N Mineralization and Plant Uptake One of the difficulties with using organic nitrogen fertilization occurs when the mineralization of organic matter is not linked to the optimum time when the plant needs and can best utilize N. This can occur when the N is mineralized early in the crop growth cycle before peak crop demand (Crews and Peoples, 2005). For organic vegetable growers, this means that nitrogen mineralization oftentimes cannot supply N during periods of rapid crop growth (i.e., high N demand), and the vegetable crop can deplete the PAN resulting in loss of yield or quality (Hartz et al., 2000; Gaskell et al., 2006). This situation is challenging and, as a result, growers sometimes rely on supplemental N from commercial organic fertilizers to meet peak crop demand.

5 USE OF ANIMAL MANURES The National Organic Standards Final Rule (USDA, 2017) states that “Raw animal manure must either be composted, applied to land used for a crop not intended for human consumption, or incorporated into the soil at least 90 days before harvesting an edible product that does not come into contact with the soil or soil particles and at least 120 days before harvesting an edible product that does come into contact with the soil or soil particles.” These restrictions represent limitations for the use of raw manure by vegetable growers, and many commercial vegetable operations tend to use only composted manure as a nitrogen source (Watson et al., 2002). However, raw manure can be used in rotations out of vegetables to build SOM and in some other limited applications.

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9. MANAGEMENT STRATEGIES FOR ORGANIC VEGETABLE FERTILITY

The precise nutrient content of any manure is dependent upon the animal species, the rations it was fed, the kind of bedding used, and the amount of liquid added. It is advisable to test manure to assess its fertilizer value. Liquid manure may not contribute significantly to organic matter build-up if it does not contain any solids (Castellanos and Pratt, 1981). Fresh manure that has not been composted will have greater nitrogen content than composted manure; however, the use of composted manure will contribute more to SOM content. Fresh manure is high in soluble forms of nitrogen, which can lead to leaching losses when overapplied. Fresh manure may contain high amounts of viable weed seeds, which can lead to weed problems. Heavy metals also can be problematic with regards to manure (USDA, 2017). In addition to these concerns, a problem has been observed when growers use fresh manure or even compost from animals that were fed hay or grass treated with an herbicide containing the active ingredient aminopyralid. This herbicide does not break down easily and can pass through the digestive system of a horse or ruminant and appear in its manure. If the manure (or compost made from this manure) is spread onto a field, the active ingredient can adversely affect vegetables (especially tomatoes) by causing new growth to become twisted and reduced in size. Animal manures (and composts made from manures) used for supplying nitrogen may also contribute to high phosphorus levels in the soil after repeated use, a condition known as “phosphorus loading” (Hartz et al., 2000). Excess phosphorus levels occur because the ratio of phosphorus to nitrogen in most manure types exceeds that required by most vegetable crops, and the excess is retained in the soil (Sharpley et al., 1994). Thus the use of manure in any vegetable production system must be approached cautiously and practically, that is, it may not be the best choice for all growers. Rapid-dried manure or compost (that has been heated to rapidly dry out) can be easier to handle and applies more uniformly to fields—especially those that have been processed into pellets (e.g., Perdue AgriRecycle# OMRI-approved pelleted poultry manure 4:2:3). Heatdrying of manure and immature compost may increase volatilization of ammonia-nitrogen and reduce the total nitrogen content of the finished product (Watson et al., 2002). Partially composted material that has been dried rapidly at high temperatures rather than cured at normal temperatures will not be as biologically active as mature compost. Prior to using rapidly dried manure/compost, growers must verify that the manure/compost has been certified for organic crop production.

6 COMPOST Composted manure is preferred by many organic vegetable growers because composting reduces potential health and environmental risks of applying raw manure, and the compost contributes to more long-term soil fertility and health (Buchanan and Gliesmann, 1991). According to organic standards (USDA, 2017), “composted plant or animal materials must be produced through a process that establishes an initial carbon-to-nitrogen (C:N) ratio between 25:1 and 40:1 and achieves a temperature between 130°F and 168°F” (54.4–75.6°C). The C:N ratio is an important consideration when using various composts; it also is a controlling factor in the composting process itself. Composting operations that utilize windrow composting systems must maintain a temperature within the prescribed range for a minimum of 15 days. During this time materials must be turned four or five times (Fig. 2).

B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

6 COMPOST

199

FIG. 2 Making compost. Organic material (green plants, manure, straw, etc.) is aerated over time, which induces heating of the material and eventually transforming it into compost.

Heat generated during the composting process kills most weed seeds and pathogens. The microbial-mediated composting process lowers the amount of soluble nitrogen forms by converting animal wastes, bedding, and other raw products into humus—the relatively stable organic fraction found in soil (Tyson and Cabrera, 1993). In stable humus, there is little free ammonia or soluble nitrate; as a large amount of nitrogen is bound as proteins, amino acids, and other biological components (Buchanan and Gliesmann, 1991; He et al., 2003). Other nutrients are stabilized in compost as well. A disadvantage of composting is that some of the ammonia-nitrogen will be lost as a gas. Alone, compost may not adequately supply sufficient nutrients—particularly nitrogen during rapid growth phases of crops with high nutrient demands (e.g., watermelon, tomato, and pepper at fruiting) (Tyson and Cabrera, 1993). In addition, composted manure typically is more expensive than fresh or partially aged manure. Because composts are relatively low in N, P, and K, application rates of 25–30 tons/acre or more (Drinkwater and Snapp, 2007) must be used if compost is the principal supplier of N to a vegetable crop. In one study, compost applied for muskmelon and broccoli crops did increase yields but not at rates economical for most growers (Roe and Cornforth, 2000). Compost is typically only 1%–2% nitrogen on a dry weight basis, so when 100–200 lbs per acre of N are needed for a crop, using compost as the primary source of nitrogen does not make economic or practical sense. However, there are other benefits from applying compost besides its N value, such as its use in increasing SOM, improving soil tilth and aeration, and increasing other plant nutrients, such as phosphorus, potassium, and some micronutrients (Gaskell et al., 2006; Mikkelsen, 2000). The best use of composts may be for preplant incorporation in situations when no cover crop can be used. A compost with a low C:N ratio could release small, but steady quantities of nitrogen for a 4- to 6-week period after incorporation thus serving as an early nitrogen source for a transplanted vegetable crop or as the only source of nitrogen for a short season crop (i.e., leafy vegetables) (Gaskell et al., 2006).

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9. MANAGEMENT STRATEGIES FOR ORGANIC VEGETABLE FERTILITY

7 COVER CROPS AND GREEN MANURES Cover crops are any plants grown specifically to manage soil erosion, soil fertility, soil quality, water, and several other ecological aspects in a field (Fageria et al., 2005). Green manures are frequently used in vegetable crop production and are grown for their nutrient value. They are a subcategory of cover crops grown specifically to provide nitrogen and scavenge nutrients in the soil, which reduces nitrate leaching, nutrient runoff, and soil erosion. The terms green manures and cover crops are often used interchangeably. These crops when incorporated can play an important role in managing nitrogen for organic vegetable production. Cover crops are traditionally planted after vegetable crops are harvested and allowed to grow through the fall, winter, and early spring, at which time they are terminated usually by plowing the crop under. Cereals, other grasses, and mustards (Brassica spp.) are particularly efficient at absorbing residual soil nitrate but will not fix nitrogen. They can be very effective in adding organic matter and/or scavenging nutrients from the soil. Grass cover crops have been shown to reduce nitrate leaching by 65%–70% compared with bare ground (Wyland et al., 1996). Legumes are also able to absorb some residual N and add additional nitrogen through fixation of atmospheric N but only in the presence of Rhizobium bacteria that have a mutualistic, synergistic relationship with leguminous plants. Legumes make excellent green manures because they have low carbon-to-nitrogen ratios, which result in a relatively fast release of nitrogen as the plants decompose (Fig. 1), but the amount of organic matter contributed to the soil is limited over the long term (Kuo and Sainju, 1998). Cover crops/green manures can be one of the most sustainable ways to provide nitrogen and other nutrients to vegetable crops (Tourte et al., 2003). In contrast to manure or compost, cover crops do not cause phosphorus loading, and there is reduced leaching of nitrogen because nutrients are released slowly. A strong green manure crop can add 80–200 lbs/acre of nitrogen to the soil for the following vegetable crop. Only a small to moderate portion (10%–50%) of the nitrogen from a green manure cover crop will be used by the following crop (Hadas et al., 2004). This is due in part to immobilization of nitrogen by soil microorganisms or by a cover crop with a very low C:N ratio resulting in poor nitrogen linking, that is, the N is released from the green manure very quickly, before the greatest need of the crop (Crews and Peoples, 2005). However, much of the nitrogen released from green manure crops usually remains in the soil humus system for a period of years and slowly becomes available to subsequent crops over time (Crews and Peoples, 2005).

7.1 Terminating a Cover Crop The challenge for organic growers is to time nitrogen release to coincide with the demands of the next crop. Of importance is the C:N ratio of green manures. Grasses have a moderate to high C:N ratio especially when they go to seed. In general, young grass growth (tiller to just before joint stage) has a lower C:N ratio and can release more N rapidly than at the boot stage (Fig. 1). As the crop ages and becomes more fibrous, the C:N ratio increases, and the material becomes more resistant to rapid mineralization (Douglas and Magdoff, 1991). Legumes on the other hand have a low C:N ratio throughout most of their growth period and continue to add

B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

7 COVER CROPS AND GREEN MANURES

201

FIG. 3 Rye cover crop on right in spring with few yellow flowered weeds compared with the legume-only cover crop on the left with weeds.

biomass that is highly conducive to mineralization. A mixture of both grasses and legumes can be used to obtain the advantages of each and is a common strategy in organic vegetable production as the grass grows more vigorously at the outset and can compete more effectively with weeds (Horwath, 2004) (Fig. 3). The grass also uses residual soil N, reducing high soil N concentrations that might otherwise inhibit N fixation by the legume. Mixtures also ensure that the cover crop is productive under a wide range of weather conditions because of the different environmental tolerances of the various plant species (Kuo and Sainju, 1998; Horwath, 2004). As has been discussed, cover or green manure crops have an important function of absorbing excess nitrogen and other nutrients from soils and as a nitrogen source enhancing SOM. The challenge for organic growers is the effective use of these cover crops for vegetable fertility by selecting the appropriate combinations that fit the specific needs of the subsequent vegetable crop ( Jarvis et al., 1996; Kuo and Sainju, 1998). However, managing cover and green manure crops is a very large subject, worthy of a whole book in itself and we can only discuss important concepts in this chapter. An excellent source of information about managing cover crops is a book published by the Sustainable Agriculture Research and Education (SARE, 2007) program entitled Managing Cover Crops Profitably.

7.2 Legume Cover Crops On organic farms, the main source of nitrogen for the vegetable crop is atmospheric N fixed by legume cover crops. In a well-designed crop rotation, plow-downs of legume cover crops can provide almost all the nitrogen required to grow most vegetables. Research has shown that an effective cover crop (2500–3200 pounds of dry matter per acre) will supply the necessary nitrogen for most vegetables, except for sweet corn, peppers, and tomatoes (Berry et al., 2002; Cline and Silvernail, 2002). These three crops would benefit from an additional 2000–3000-pound application of compost during the spring. Legumes usually require good drainage and fertility to establish and grow. At first, most legumes grow slowly; therefore they do not compete well with weeds until they become well-established (Fig. 3). An excellent practice is to sow the legumes with a companion crop such as oats, rye, or in mixes with perennial grasses (Ranells and Wagger, 1996). Selection of companion green manures

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should be based on soil type, climatic conditions, cultural factors, and water availability (Cherr et al., 2006). Deep rooted cover crops may deplete soil of moisture in the spring, which may present a problem for subsequent crops during dry years. 7.2.1 Clovers Red clover Trifolium pratense is a short-lived perennial that is mildly tolerant of soil acidity and poor drainage; a good stand can add 60–90 pounds/acre of nitrogen to soil. Crimson clover Trifolium incarnatum grows rapidly but has poor drought tolerance, and can add 75–100 pounds/acre of nitrogen to soil. White clover Trifolium repens is a low-growing perennial that is tolerant of shade and slightly acidic soil, and a good stand can add 75–110 pounds/acre of nitrogen to soil. Yellow sweet clover Melilotus officinalis matures earlier and is somewhat less productive than white sweet clover M. albus; a good stand of a sweet clover can add 80–130 pounds/acre of nitrogen to soil. Ladino clovers T. repens are taller than the White or Dutch white clovers (T. repens) and can add 70–100 pounds/acre of nitrogen to soil (SARE, 2007). 7.2.2 Hairy Vetch Hairy vetch Vicia villosa is a hardy winter annual cover crop and can add 80–150 pounds/ acre of nitrogen to soil (Fig. 4). Vetch produces little growth during the fall; therefore it is advisable to grow it with a grass companion during late August to mid-September to ensure adequate soil coverage during the winter (Cherr et al., 2006). Utilizing rye allows the vetch to climb during the spring; this can reduce matting and increase its incorporation into the soil. Vetch can be spring-planted and used as a fallow crop because it provides a valuable cover through late summer. Vetch has drought tolerance and is the most cold tolerant of the winter annual legumes. 7.2.3 Austrian Winter Peas This legume establishes more effectively in cool weather and does not tolerate hot humid conditions. Austrian winter peas Pisum sativum var. arvense have a shallow root system and do not overwinter north of about 40o latitude; a good stand of Austrian winter peas can add an average of 60–100 pounds/acre of nitrogen to soil (SARE, 2007).

FIG. 4 Hairy vetch cover crop before flowering (left) in early spring and a few weeks later at flowering (right).

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7.3 Grass Cover Crops Winter rye Secale cereale is a popular choice for a winter cover crop—it can be planted well after most vegetable crops are finished because it produces enough vegetative growth through fall and early winter and outcompetes weed species (Fig. 3). Oats Avena sativa or other small grains (e.g., wheat Triticum aestivum, triticale Triticosecale [Secale  Triticum]) also can be sown after vegetable crops are finished being harvested; however, they do not grow as well as rye. All these grasses are effective scavengers of any residual nitrogen left from the summer vegetable crop (Ranells and Wagger, 1996). Rye produces significant biomass in the spring, which helps maintain SOM levels. It also produces an extensive root system early in its growth cycle that effectively captures any late season nitrogen present after vegetable crops have been harvested. However, a potential concern regarding the use of rye is the occasional excessive amount of residue that must be handled during the spring (Cline and Silvernail, 2002). Growers who desire to plant an early spring crop may not wish to plant a cover crop of rye, because if the spring is very wet the rye becomes more difficult to manage. In such instances, growers usually plant wheat or oats in fields that must be turned under in early spring—these cover crops are less likely to become rank and unmanageable in wet seasons. Annual or Italian ryegrass Lolium multiflorum is less expensive than perennial ryegrass Lolium perenne but is more likely to winter-kill than other rye grass species. All these cover crop grasses form a dense sod that reduces erosion. Oat as a winter cover crop can protect the soil without requiring intensive management in the spring, because it is frost-killed. To protect the soil, it is recommended that growers plant by late August in the Midwest and Eastern United States to ensure that an adequate amount of growth is present before the first frost. Oat residues remaining on the soil surface may chemically suppress weed growth and act as a physical barrier (SARE, 2007). Also, oat may be used as a spring cover when mixed with hairy vetch. Other small grains, such as winter wheat T. aestivum, barley, Hordeum vulgare, and triticale, have been used successfully as winter and early spring cover crops. Small grains provide an effective rotation crop when coupled with vegetables because they generally do not host most of the diseases and few of the insect pests of vegetables (Cherr et al., 2006).

7.4 Summer Cover Crops Summer cover crops such as buckwheat Fagopyrum tataricum, sunn hemp Crotalaria juncea, cowpea Vigna unguiculata, and sorghum-Sudangrass Sorghum  drummondii grow quickly in warm weather, effectively smothering weeds, and in general do not have frost tolerance (Creamer and Baldwin, 1998). These summer cover crops are drought-tolerant, are easy to incorporate into the soil, and decompose rapidly; most do not significantly contribute to the organic matter of the soil. Buckwheat flowers serve as a favorite nectar source for bees and natural enemies of insect pests; however, if allowed to flower and set seed, hundreds of these plants will sprout the following year. To smother weedy fields, some growers plant a fallow cycle of two successive crops of buckwheat followed by winter rye. Other summer cover crops such as Sudangrass and sorghum-Sudangrass are fast-growing crops that require superior fertility and moisture to perform well (Creamer and Baldwin, 1998). Under these conditions, the rank growth of these crops provides exceptional weed suppression, although

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it should be noted that this type of heavy growth can be difficult to incorporate. Midseason mowing provides the opportunity for regrowth before the crop winter-kills and reduces the production of fibrous plant material. Pearl Pennisetum echinurus and Japanese Echinochloa esculenta millets also are warm season crops that generate rapid growth if they have been planted by early June. Pearl or Japanese millet is not as tall or rank as sorghum-Sudangrass and can be easily incorporated in the fall or spring. Cowpeas thrive in hot, moist zones and are one of the most productive heat adapted legumes used as a cover crop in the United States. They also are an excellent source of nitrogen ahead of fall-planted crops and can be used on poor land as part of a soil-building cover crop sequence (SARE, 2007). As with buckwheat, flowering cowpeas attract many beneficial insects that prey on pests.

7.5 Forage Brassicas This cover crop includes varieties of several species of mustard-family crops such as rape Brassica napus, turnip Brassica rapa subsp. rapa, and forage radish Raphanus sativus var. longipinnatus. These cool-season crops (especially forage radish) help break up compacted soils or pans with their tap roots. Weil et al. (2009) have shown that other potential benefits of using forage radish include suppressing weeds, building SOM, releasing nitrogen early in the season, and reducing both nitrate leaching and soil erosion. The crop will winter-kill in most areas north of 40° latitude (Fig. 5).

7.6 Other Methods of Establishing Cover Crops Interseeding or undersowing a cover crop into a standing vegetable crop allows an earlier establishment of a winter cover crop. Earlier establishment increases the selection of cover crops, compared with waiting to sow a cover crop after the full-season vegetable crop is done. Cover crop sowing must be delayed long enough to minimize competition with the vegetable crop, yet early enough to ensure that the cover crop can survive competition with the vegetable and withstand the harvest traffic (SARE, 2007). Vigorous vegetables, such as winter squash and sweet corn, are suitable for interseeding. This method requires effective soil-seed

FIG. 5 Forage radish cover crop in late fall on left and late winter on right after winter-kill.

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contact, sufficient rainfall, and adequate weed control early in the season to guarantee that the cover crop can become well established. Interseeding immediately after the last cultivation is the most effective method.

7.7 Mowing Green Manure Crops Mowing is an essential part of growing some of the legume green manures. Early mowing can make the difference between a well-established green manure crop and one that is persistently weedy. Most species, including red clover, white clover, Lucerne, Persian clover, and yellow trefoil, can tolerate being topped close to the ground because the mowing stimulates lateral growth, improving weed control. Some green manures, such as hairy vetch, can become weed problems in crops if they develop viable seeds that germinate later in the cash crop. It is probably best to mow green manure crops before they set seed.

8 PROBLEMS WITH N LOSS Contrary to general understanding, there is a significant potential for nitrogen loss from organic sources in organic farming systems. The period between peak residue nitrogen mineralization and crop uptake (poor N linking, discussed earlier) creates a period of time whereas large amounts of nitrate may be available to leach or runoff with a rainfall event (Poudel et al., 2001). There also can be N losses from volatilization of ammonia from surface-applied compost on some soils (He et al., 2003). Because nitrate is water-soluble, whenever there is more nitrate than plants can absorb, the excess may leach with a heavy rain or irrigation. Heavy, constant disking or other soil disturbances can cause a rapid decomposition of green manures, which can provide too much nitrogen too early in the cropping season. No-till systems will have a reduced and more gradual release of nitrogen, but some of that nitrogen may be vulnerable to gaseous loss. Finer-textured and loam soils have a greater potential to retain nitrogen mineralized from a cover crop or compost even when there is considerable lag time between incorporation and crop uptake (Cherr et al., 2006). Cover crops and composts with a higher C:N ratio (25) may be useful for managing excess nitrogen by encouraging microbial immobilization and slowing the mineralization rate (Poudel et al., 2001).

9 OTHER PLANT NUTRIENTS 9.1 Phosphorus and Potassium Most (80%) of the phosphorus and potassium in manure or compost will be available to the crop in the first year of application, but poor storage of the manure or compost will lead to losses of potassium through leaching (Gaskell et al., 2006). Phosphorus sources other than manure for organic production include bone meal, fish and poultry meal, and rock phosphate. Potassium sources other than manure for organic production include alfalfa meal, kelp meal, greensand (or glauconite, which is a clay-type mineral with a potassium content of 7%), wood ash, langbeinite (listed by OMRI as allowable in certified organic production if it is used

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in the raw form without any alteration), and potassium sulfate. Growers should be aware that there are two forms of potassium sulfate available: one comes from the reaction of sulfuric acid with potassium chloride, and it not allowed in certified organic vegetable production. The other is developed from natural sources, and it is allowed in organic crop production. Because phosphorus and potassium are relatively immobile in the soil, they should be incorporated to a depth of 6–10 in. before planting (Drinkwater and Snapp, 2007).

9.2 All Other Nutrients Using various inputs such as cover crops, manure, compost, and liming amendments usually satisfy secondary macronutrient (Ca, Mg, S) and micronutrient (Fe, Mn, Cu, Zn, B, Mo) requirements. A major advantage of organic nutrient sources is that they usually contain at least a small amount of these essential plant nutrients. Deficiencies of some secondary and micronutrients may occur on susceptible crops under certain soil conditions conducive to deficiencies, therefore soil tests and foliar tissue analysis should be used to determine whether supplemental applications of these nutrients are needed.

10 COMMERCIAL ORGANIC FERTILIZERS Many types of commercial organic fertilizers are available for use in certified organic crop production. These products include liquid fish, pelleted poultry manure, pelleted seabird guano, Chilean nitrate, feather and blood meal, and others. These commercial fertilizers are more concentrated nitrogen sources than compost, with improved handling (less water) and nitrogen availability, and are important for supplementing nitrogen from SOM, manure, cover crops and compost. They are particularly important in supplying late-season N to optimize crop yield and quality (Hartz and Johnstone, 2006). However, commercial organic fertilizers can be an expensive method on a per-acre basis for supplying nutrients to a cash crop but at times are necessary when the nutrient demand of the crop exceeds what can be supplied. Therefore a grower should examine closely the cost/benefit of using commercial fertilizers.

11 FERTIGATION Liquid organic fertilizers can offer opportunities for more efficient nitrogen use when they are applied through a drip irrigation system—such an application is called fertigation. Any nutrient in a water-soluble form is readily available for plant uptake just after application, leading to a more efficient use of fertilizers (Buchanan, 2000). When nutrients are applied shortly before they are needed, growers can reduce loss of nutrients from the root zone. These liquid fertilizers may be applied on a regular basis, depending on the nutrient need of the crop. This allows the grower greater control over nutrient availability to their crop (Marr, 1993). Some of the liquid fish-derived and soybean-based fertilizer materials are widely used in organic vegetable production. A few important considerations before using fertigation are: (1) only use fertilizers that either dissolve completely or have particles that stay in suspension and pass through emitters without clogging, (2) the drip irrigation system

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should be fully pressurized before injection begins, (3) there should be a filter between the injector and the laterals to ensure that any particles are filtered out, and (4) the irrigation system must be flushed of nutrients to keep drip lines clean and prevent clogging (Marr, 1993).

12 RIGOROUS CROP ROTATION AND FERTILITY Crop rotation should be the fundamental practice of every organic vegetable farm, but many organic growers do not practice a rigorous system of rotation, mostly because of not having enough land to develop an effective rotation scheme. Instead, many growers use a system that only allows a field to rest for a few years between related crops (Grubinger, 1999). In most cases rotation is almost exclusively among cash crops with little land ever taken out of crop production. A good ecologically sound rotation results in a much more fertile, healthy soil, as well as improved insect, disease and weed control (Havlin et al., 1989). A good rotation includes integrating cover crops and cash crops into the rotation, if possible in equal amounts. It can be challenging to fit cover crops into a cash crop-only rotation, but it is important to develop rotations that take full advantage of the different cover crops’ benefits. Most successful organic vegetable systems will practice a rigorous crop rotation, which will include 20%–25% of the farm’s crop land be in a cover crop and out of vegetable production each year (Grubinger, 1999).

13 TILLAGE/CULTIVATION Tillage and cultivation are an integral part of almost all organic systems. Current organic systems usually require tillage prior to planting and cultivation after planting to control weeds (Silgram and Shepherd, 1999). However, tillage destroys SOM critical in improving soil fertility and soil water-holding capacity (Sarrantonio and Scott, 1988; Silgram and Shepherd, 1999). Tillage should be performed when soil moisture is low enough to prevent compaction, which can result in long-term yield reduction and much time and effort to loosen compacted soil (Sarrantonio and Scott, 1988). Because primary tillage operations are usually performed at least a month before a crop is planted, careful planning to take advantage of periods of dry weather is required. Reduced tillage and no-tillage systems have become more common because of the many benefits of minimally disturbing the soil system.

14 NO-TILL VEGETABLE SYSTEMS No-till vegetable systems have the potential for wider adoption by commercial organic growers. However, it is important to select cover crops that have adapted to the specific region and specific cropping system. For example, hairy vetch as compared with other legumes has been successfully utilized as a no-till mulch for tomatoes and other crops (Anon., 2017). Nonchemical weed control is an available option for managing cover crops; however, success is often dependent on specialized equipment, cultural practices, and fortuitous timing. Several types of equipment are described in the following sections.

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FIG. 6

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Roller crimper implement used for the laying down of cover crops to plant no-till vegetables into residue.

14.1 No-Till Equipment (1) Flail mowers can chop cover crops until they remain only an inch above the ground, while shredding the cover crop material and leaving the mulch in place (Hooks et al., 2015). Rotary mowers (brush-hogs) clip higher and usually distribute vegetative residue throughout a wider area. It is very important to determine the optimum time to mow cover crops because if they are mowed too early they will re-sprout and compete with the vegetable crop—like a weed. Hairy vetch must be mowed when it begins to flower, whereas rye should be mowed when the anthers shed pollen. (2) A roller crimper rolls down and crimps a cover crop by using heavy-duty drum rollers with horizontal-welded blunt-steel strips (Fig. 6). When the drum rollers go through the field, they crush and crimp the cover crop, which leaves residue lying flat on the soil surface and discourages regrowth (Fig. 6). Studies have shown that rolling/crimping cereal grains such as winter rye, wheat, hairy vetch, or a combination of rye and vetch is most effective during the pollen-shed stage (Hooks et al., 2015). Rolling/crimping at that stage can kill cover crops just as effectively as herbicides. (3) The undercutter-roller is a specialized implement designed to slice through the soil and sever cover crop roots underground (Treadwell and Alligood, 2006). It consists of a V-shaped sweep blade mounted on a toolbar, followed by a rolling harrow to crimp and roll the cover crop residue as it falls to the ground. Undercutting suppresses weeds more effectively than a flail mower or sicklebar mower. The undercut mulch is thicker and better equipped to prevent light penetration to the soil surface, which results in fewer weeds. In addition, residue from this method remains on the soil surface for a longer period.

15 SOIL HEALTH A healthy soil can overcome stress and is usually high in biological diversity. The greater the biodiversity within the soil, the quicker the soil ecosystem can return to initial conditions after exposure to disturbances (Wang and Hooks, 2010). There are five main characteristics of a healthy soil: (1) high biological diversity, (2) high community stability, (3) ability to maintain the integrity of nutrient cycling and energy flow, (4) suppression of multiple pests and

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pathogens, and (5) maintenance of water and air quality (Wang and Hooks, 2010). There is a great diversity of biological organisms that constitute the soil food web such as bacteria, algae, fungi, protozoa, nematodes, mites, earthworms, insects, and other organisms. Most of these soil organisms play an important role in creating and maintaining soil health. Therefore the conservation and preservation of this biological aspect of the soil is essential to the preservation of soil quality. Some of the best ways to accomplish the goal of a biologically diverse soil system is through means we have already discussed, via the use of various cover crops and organic amendments within a well-planned rotational system. Bacteria are the most abundant microorganisms in the soil, which serve many important purposes, including nitrogen fixation. One of the most notable features of bacteria is their biochemical versatility. Bacteria can metabolize a wide range of chemicals and fertilizers, turn nitrite into nitrate, and convert atmospheric nitrogen into nitrogen-containing compounds (nitrogen fixation) used by plants. Actinomycetes are a type of soil bacteria, but they share several characteristics with fungi. They are instrumental in decomposing organic matter and in nutrient mineralization. Although a great majority of soil fungi are beneficial to plants, some can be plant pathogens. Most beneficial soil fungi colonize organic matter and begin the decomposition process and mineralization. Mycorrhizal fungi are beneficial soil organisms that contribute to soil health (Cavagnaro et al., 2006). Mycorrhizal fungi form a symbiotic mutualistic relationship with plant roots. The fungus acts as an extension of the root system, exponentially expanding the surface area of those roots, giving the plant greater access to phosphorous and other nutrients. In return, the fungus receives carbohydrates and growth factors from the plant. Nematodes are abundant in most soils, and only a few species are harmful to plants. The beneficial species eat decaying plant litter, bacteria, fungi, algae, protozoa, and other nematodes. Like other soil decomposers, nematodes speed the rate of nutrient cycling and are often used as indicators of a healthy soil (Wang and Hooks, 2010). Soil-inhabiting arthropods include sowbugs, millipedes, and springtails. These are primary decomposers. Their role is to consume and shred the large particles of plant and animal residues. Some bury residue, bringing it into contact with other soil organisms that further decompose it. Earthworms play a major role in the conversion of large pieces of organic matter into rich humus, thus improving soil fertility. They accelerate nutrient cycling in the soil system through the fragmentation and mixing of plant debris (Bhadauria and Saxena, 2010). Earthworm excretions in the form of casts enable minerals and plant nutrients to be accessible in forms for plants to use. Earthworms create many channels through the soil, which are of great value in maintaining soil structure, improving aeration, and drainage.

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Hooks, C., Leslie, A., Chen, G., 2015. Managing weeds in vegetables organically. Found at: http://extension.umd. edu/sites/extension.umd.edu/files/_images/programs/mdvegetables/OrganicWeedMgntVeg21May2016(1). pdf. [(Accessed 22 April 2017)]. Horwath, W., 2004. The importance of soil organic matter in the fertility of organic production systems. In: Proc. California Organic Production and Farming in the New Millennium: A Research Symposium. Berkeley, CA, 15 July 2004. Univ. of California Sustainable Agr. Res. and Educ. Program, Univ. of California, Davis, pp. 8–12. Horwath, W.R., Dev^evre, C., Doane, T., Kramer, A., van Kessel, C., 2002. Kimble, J.M., Lal, R., Follett, R.F. (Eds.), Soil C Sequestration Management Effects on N Cycling and Availability, Agricultural Practices and Policies for Carbon Sequestration in Soil. Lewis Publishers, CRC Press, Boca Raton, FL, pp. 155–164. Howell, J., 2005. Organic Matter: Key to Soil Management. Available at: http://www.hort.uconn.edu/ipm/veg/ croptalk/croptalk1_4/. [(Accessed 25 April 2017)]. Jackson, L., 2000. Fates and losses of nitrogen from a nitrogen-15 labeled cover crop in an intensively managed vegetable system. Soil Sci. Soc. Am. J. 64, 1404–1412. Jarvis, S., Stockdale, E., Shepherd, M., Powlson, D., 1996. Nitrogen mineralization in temperate agricultural soils: processes and measurement. Adv. Agron. 57, 187–237. Kuo, S., Sainju, U.M., 1998. Nitrogen mineralization and availability of mixed leguminous and non-leguminous cover crop residues in soil. Biol. Fertil. Soils 26, 346–353. Leiro’s, M.C., 1999. Dependence of mineralization of soil organic matter on temperature and moisture. Soil Biol. Biochem. 31, 327–335. Marr, C.W., 1993. Commercial vegetable production, fertigation of vegetable crops. In: MF-1092. Kansas State University Agricultural Experiment Station and Cooperative Extension Services, Manhattan, KS. Available online at: http://www.ksre.ksu.edu/library/hort2/mf1092.pdf. [(Accessed 9 April 2017)]. Mikkelsen, R., 2000. Nutrient management for organic farming: a case study. J. Natural Res. Sci. Educ. 29, 88–92. Poudel, D.D., Horwath, W.R., Mitchell, J.P., Temple, S.R., 2001. Impacts of cropping systems on soil nitrogen storage and loss. Agric. Syst. 68, 253–268. Ranells, N.N., Wagger, M.G., 1996. Nitrogen release from grass and legume cover crop monocultures and bicultures. Agron. J. 88, 777–882. Roe, N.E., Cornforth, G.C., 2000. Effects of dairy lot scrapings and composted dairy manure on growth, yield, and profit potential of double cropped vegetables. Compost Sci. Util. 8, 320–328. SARE, 2007. Managing Cover Crops Profitably, third ed. http://www.sare.org/Learning-Center/Books/ManagingCover-Crops-Profitably-3rd-Editionn. [(Accessed 12 April 2017)]. Sarrantonio, M., Scott, T.W., 1988. Tillage effects on availability of nitrogen to corn follow a winter green manure crop. Soil Sci. Soc. Am. J. 52, 1661–1668. Schimel, J.P., Bennett, J., 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602. Scow, K.M., 1996. Jackson, L.E. (Ed.), Soil Microbial Communities and Carbon Flow in Agroecosystems, Ecology in Agriculture. Academic Press, New York, pp. 367–412. Sharpley, A., Chapra, S., Wedepohl, R., Sims, J., Daniel, T., Reddy, K., 1994. Managing agricultural phosphorus for the protection of surface waters: issues and options. J. Environ. Qual. 23, 437–451. Silgram, M., Shepherd, M., 1999. The effects of cultivation on soil nitrogen mineralization. Adv. Agron. 65, 267–311. Stevenson, F., 1994. Humus Chemistry: Genesis, Composition, Reactions, Second ed. Wiley, Hoboken, NJ. Tourte, L., Buchanan, M., Klonsky, K., Mountjoy, D., 2003. Estimated Costs of Potential Benefits for an Annually Planted Cover Crop. University of California Coop. Ext, Watsonville, CA. Treadwell, D., Alligood, M., 2006. 2nd Installment of the “Cover Crop Corner” Management Considerations for Annual Cover Crops in Florida Vegetable Systems. Vegetable Crops Extension Publication, Gainesville, FL. Tyson, S., Cabrera, M., 1993. Nitrogen mineralization in soils amended with composted and uncomposted poultry manure. Commun. Soil Sci. Plant Anal. 24, 2361–2374. United States Department of Agriculture, 2017. Program Handbook: Guidance and Instructions for Accredited Certifying Agents & Certified Operations. Agriculture Marketing Service, National Organic Program. Available online at: https://www.ams.usda.gov/services/organic-certification. [(Accessed 15 April 2017)]. United States Department of Agriculture-National Organic Program (NOP), 2016. The National Organic Program Handbook. https://www.ams.usda.gov/about-ams/programs-offices/national-organic-program. [(Accessed 15 April 2017)].

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Wang, K., Hooks, C., 2010. Managing Soil Health and Soil Health Bioindicators Through the Use of Cover Crops and Other Sustainable Practices. Found at: http://extension.umd.edu/sites/extension.umd.edu/files/_docs/ programs/mdvegetables/Chap4-Soil-Health-web-version.pdf. [(Accessed 12 April 2017)]. Watson, C., Atkinson, D., Gosling, P., Jackson, L., Rayns, F., 2002. Managing soil fertility in organic farming systems. Soil Use Manag. 18, 239–247. Weil, R., White, C., Lawley, G., 2009. Forage Radish: New Multi-Purpose Cover Crop for the Mid-Atlantic. UME Fact Sheet 824, College Park, MD. Wyland, L., Jackson, L., Chaney, W., Klonsky, K., Koike, S., Kimple, B., 1996. Altering surface soil dynamics with cover crops in a vegetable cropping system: Impacts on yield nitrate leaching, pests and management costs. Agric. Ecosyst. Environ. 59, 1–17.

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Alternatives to Pest and Disease Control in Preharvest, and Washing and Processing in Postharvest Levels for Organic Produce Aishwarya Pradeep Rao, Sadhana Ravishankar School of Animal and Comparative Biomedical Sciences, University of Arizona, Tucson, AZ, United States

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1 INTRODUCTION Food crops grown in fields are subject to contact with vehicles of pathogen contamination. These could include environmental factors such as soil, water, air, and human handling/ processing techniques. Increased consumption of ready-to-eat, fresh, and/or minimally

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processed fruits and vegetables has been accompanied by an increase in outbreaks of foodborne illnesses associated with these commodities (Rao, 2017). Organic food products are consumed more frequently than foods produced by conventional methods as seen in the trends spanning 1998–2016 (Thompson and Kidwell, 1998; Willer and Lernoud, 2016). Fresh organic produce, certified by the US Department of Agriculture, have emerged as the highest consumed organic commodity with salad vegetables such as leafy greens, tomatoes, and cucumbers being the highest in demand. Milk and meats were considered to be the second highest consumed groups among the organic commodities (Willer and Lernoud, 2016). A number of factors are responsible for the surge in consumer demand for organic products, and these reasons vary from market to market. The general opinion for the preference of organic over conventionally produced foods is that people prioritize their health over the presence of pesticide residues in the food (Hughner et al., 2007). However, some consumer sections put their environmental concerns as primary factors for opting for organically produced food (Hughner et al., 2007; Tregear et al., 1994). Goldman and Clancy (1991) also found that approximately 70% of the population that consumed organic products in the UK cited health benefits as the primary reason for their organic product preferences. However, consumers in Germany had a preference for environmental reasons (Goldman and Clancy, 1991). Smith-Spangler et al. (2012) surveyed the US populations’ preferences and found that the general product, its sensory attributes, environmental impact, nutritional value, health benefits, and food safety influenced consumers to prioritize organic food over conventionally produced food. Certain sections of the communities across the country also looked at the protection of wildlife and water sources in correlation to organic and conventional agriculture before they looked at the protection of consumers from pesticide and chemical fertilizer residues. A group of organic produce consumers from Norway seemed more concerned about the safety and health aspects as compared to prices and aesthetic appeal (Goldman and Clancy, 1991). This trend has continued through to 2014, where consumers were definitely more likely to consume organic produce due to the quality, believing that they thought it was value for their money. Also, based on the supply-demand ratio gap decreasing, the prices of organic foods have not increased but have actually decreased over the decade (Willer and Lernoud, 2016). Organic agriculture is characterized by the use of environmentally friendly practices that include monitored crop rotations to renew depleted nutrients from the soil, ecologically based pest management and reduction systems, and the use of natural fertilizers such as compost and manure in place of chemical pesticides, hormones, and fertilizers (Dimitri and Greene, 2000). The organic industry is constantly looking for natural yet effective alternatives to replace existing harmful practices, and it is expected that these alternatives will provide a secure and economically sound food supply. The organic food industry is a multibilliondollar segment in the market with production and consumption increasing from about $1 billion in the early 2000s to about $80 billion in 2014 (Bourn and Prescott, 2002; Willer and Lernoud, 2016). In 2001, about 40% of the total organic sales comprised of fresh fruits and vegetables, which was higher as compared to meats and meat-based products (Economic Research Service, 2001). This trend continues into 2014, where consumers reported preferring organic produce to meats and milk. Sprouts and cheeses were also among the top organic foods chosen by habitual consumers (Willer and Lernoud, 2016). According to Willer and Lernoud (2016), organic produce sales comprised of approximately 60% of the total organic food sales, owing to the high availability of agricultural land.

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Organic fruit and vegetable farming options can have potential financial advantages for both existing and new farmers in the way that these practices cover the narrow margin of profitability and high land-associated costs in states such as Minnesota and Wisconsin, among others. Organic agriculture allows for the production of high value and yield crops on relatively small land farms, thus bridging the gap in finances (Mukherjee et al., 2004). Differential sensory attributes of the fresh produce and the fact that organic farming employs the use of natural pest control methods and fertilizers are responsible for the high consumer demand for these products (IFOAM, 1998). According to Willer and Lernoud (2016), organic production has increased due to higher consumer demand and increased land availability. Organic farming aims to provide an enhanced biological cycle in the farming system to maintain the genetic diversity of the farming system and all its components such as soil, crops, and water; control the long-term fertility of the soil; mitigate pollution; and simultaneously manage the ecological and social impacts of food production with high quality food in sufficient quantities (IFOAM, 1998). To be certified as organic, producers need to maintain proper documentation and standards. Various organic certification authorities around the world have their own standards and documentation procedures. Irrespective of home country’s rules and regulations, for import and export purposes, each producer must conform to the receiving country’s rules and regulations (Sloan, 2002). Regulatory agencies from other countries may have personnel on site to inspect the processing and harvesting methods and technologies (Agricultural Marketing Service, 2000). Many factors have been used as parameters and investigated in studies that compare the two food production systems: conventional and organic. Commonly studied factors include agro-economics, crop yields, soil chemistry, microbial activity, pest and disease possibilities, farm management practices, aesthetic and nutritional quality, impacts on the environment and consumer’s health, biodiversity of the region, nutritional and calorific requirements of consumers, and social, trade, and political aspects associated with each of the production systems (Gussow, 2000). The chief basis of designing a sustainable food production process is to ensure a sufficient and healthy food supply over a long period of time. This chapter deals with organic farming practices and the alternatives used that can differentiate between conventional and organic farming.

2 PREHARVEST STRATEGIES 2.1 Composts and Fertilizers Synthetic pesticides and fertilizers have been used in agriculture since around 2000 BC, with sulfur and other inorganic elements being the favored pesticides among farmers. The use of pesticides increased in the 1940s with the increased supply of dichlorodiphenyltrichloroethane (DDT), β-Hexachlorocyclohexane (BHC), aldrin, endrin, and 2,4-Dichlorophenoxyacetic acid (2,4-D). These products were inexpensive, especially DDT, and had broad spectrum activity according to the International Union of Pure and Applied Chemistry. Today’s consumers understand the risks associated with these harmful compounds and tend to prefer natural alternatives (Shepherd Jr et al., 2007). Organic farming practices make use of fertilizers and pesticides from natural sources as approved by the United States Department of Agriculture, National Organic Program (USDA-NOP).

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These include animal manure, plant wastes, fish and poultry waste, seaweed, and fruit and vegetable product waste (Celik et al., 2004). The disadvantage of using animal-derived manure is that any gastrointestinal pathogens can cross-contaminate the produce and the surrounding soil, resulting in a potential outbreak (Mukherjee et al., 2004). There have been suggestions put forward to state that organic products may contain higher numbers of pathogenic bacteria as compared to produce that may have been grown with synthetic fertilizers (Mukherjee et al., 2004); however, food safety standards mandate that organic manure only be applied to the crops and soil 90 days before harvesting the crops or only if certain specific procedures have been used to compost it (Agricultural Marketing Service, 2000). Composting is a process that controls the spread of enteric pathogens and crop pests using exothermic natural chemical reactions that can kill any bacterial and fungal pathogens that may be responsible for contaminating the food supply. The effect of composting in reducing the presence of foodborne pathogens is dependent on the processing time and the temperature at which the composting process is carried out (Eghball and Power, 1999; Shepherd Jr et al., 2007). The application of manure after composting has been shown to not only improve soil quality for future crop cycles but also has been known to improve crop quality by providing nutrients required for the increase in crop yield (Bandyopadhyay et al., 2010). Crops such as soybean and corn grown on compost-treated soil yielded higher protein content when samples taken from Nitrogen, Phosphorus, and Potassium (NPK)-treated and compost-treated soils were compared. The root mass was higher, indicating higher crop grounding, which could help in preventing erosional changes in the field as well (Bandyopadhyay et al., 2010; Celik et al., 2004; Lung et al., 2001). Novel ways of applying compost and manure to food crops have been developed and researched. To prevent pathogens from contaminating the food crops, manure or compost can be fractionated in water, resulting in compost extracts, also called compost teas (Ingham, 2005). According to the compost tea brewing manual, composts and manures of different natures can be converted into teas for a dilution specific effect on the target crops (Ingham, 2005). Compost teas with added nutrients are becoming increasingly popular with the organic industry and home farmers. The factors that need to be considered when preparing industryready teas include those that can promote pathogen suppression such as pH, temperature, compost to water ratios, manure enrichment, compost age, and fermentation time (Ingham, 2005). The nature and efficacy of the compost tea also largely depend on the original feedstock from which the compost is made. Additions such as manure and vermicompost only enrich the compost teas, resulting in better yield, by increasing root mass and length, thus, influencing erosion action (Pant et al., 2011). The use of compost teas in organic agriculture governed by careful thought of dilution ratios, choice of equipment used for applications of the teas, times and rates of application, and enrichment agents may result in an integrated plant and soil health management strategy (Scheuerell and Mahaffee, 2002). An advancement from traditional composts and manures is the use of vermicompost. The use of earthworms to compost feedstocks such as vegetable peel wastes and other kitchen wastes is popular among home farmers and organic producers (Buckerfield et al., 1999). Vermicompost is nutritionally enriched with substances such as lectins and other glycoproteins, secreted by earthworms, resulting in increased nutritional values of the crops it is applied to (Atiyeh et al., 2001). Physicochemical properties of the soil are also influenced by the addition of these substances. The addition of synthetic fertilizers can change the

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chemical properties of the soil by inducing chemical interactions with molecules in the soil. The soil in turn affects the quality of the crop. Three varieties of tomatoes were grown in the presence and absence of vermicompost, and parameters such as biomass allocation, crop quality, and germination were assessed (Zaller, 2007). All three varieties grown with the addition of vermicompost were seen to have better crop quality with increased root and fruit biomass, indicating that vermicompost was a valuable addition to the potting mixture (Zaller, 2007). Guti
errez-Miceli et al. (2007) found that the addition of vermicompost from pig manure not only enhanced the soil and crop quality, but also significantly increased the yield of two varieties of tomatoes, belonging to the cultivar, Rio Grande. The addition of chemical fertilizers and pesticides can be harmful not only to the consumers but also the environment. These substances, recognized as xenobiotics or foreign substances by the human immune system, are nondegradable and leave residues that interact with other chemical molecules in the environment, resulting in the formation of potential carcinogens (Kindt et al., 2007). The residues left behind also damage natural systems such as the underlying bedrock, leading to increased erosion, which in turn, affects the pH and stability of the aquifer or water table (Gardner and Stern, 1996). Considering all the potential negative effects synthetics can have on the environment and consumers, the organic industry will benefit from further research being carried out into natural alternatives such as natural manure, composts, and compost teas, as well as vermicomposts from various feedstocks that are recyclable and readily available.

3 INTRUSION OF WILDLIFE, INSECTS, AND BIRDS To provide safe, nutritious, and sustainable produce for current day consumers by the organic industry, it is necessary to maintain a pest-free environment. Organically produced fruits and vegetables are at a higher risk of contamination by pathogens due to minimal implementation of control measures (Williams and Hammitt, 2001). Appropriate on-farm safety measures need to be implemented with strict regulation to ensure long-term economic, social, and environmental sustainability (Williams and Hammitt, 2001). Bringing pest infiltration levels down to acceptable levels or the bare minimal levels is what constitutes pest control. It is unrealistic to even attempt complete eradication. However, for sanitary reasons, it is important to maintain or control pest numbers through scat management, traps, containment measures, and the use of deterrents. Due to the proximity of some farms to wooded areas, the intrusion by wildlife such as deer, moose, elk, and other ruminants is imminent. Also, a common source of contamination is rainwater runoff from these wooded areas that may harbor animal feces (Sibanda et al., 2000). In 2011, a strawberry farm in Oregon was subjected to an outbreak of E. coli O157: H7 recovered from the soil that had been flooded with rainwater containing deer scat (Laidler et al., 2013). In such conditions, farm owners and management personnel are encouraged to employ containment measures. These would include building physical structures that prevent stray animals from wandering into fields and include structures such as wired fences, electric wires, and metal barriers that can withstand animals trying to break the fence (Sibanda et al., 2000). Spraying or placing of natural animal deterrents such as ground coffee beans, castor oil, and flowers of sulfur, vinegar, and pepper can also be done at the bottom of B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

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these fences to keep burrowing animals such as rabbits, mice, and other rodents away (Sibanda et al., 2000). Modern farms generally set up these fences in deep trenches to collect possible runoffs of rainwater that may contain fecal contamination, preventing it from entering the fields (Williams and Hammitt, 2001). However, all these measures must be efficient yet humane toward wild animals. Measures that may cause bodily harm to wildlife are usually not implemented to maintain levels of coexistence (Sibanda et al., 2000). Pests of primary concern are insects, which include flies, beetles, and locusts (Landis et al., 2000). Flies are common in the produce production environment due to the presence of several luring factors, which include open manure, moist conditions, heavy organic matter load, and warm temperatures. They are responsible for the spread of disease-causing microorganisms and can transmit bacteria from fecal contamination to fresh leafy greens or various plant parts as well. The only way to prevent flies from settling on fresh produce is to keep manure storage secured and under covered conditions (Landis et al., 2000). Different types of pesticides such as dusts, wet table powder, liquid sprays, and resin strips approved for organic agriculture are available depending on the types of infestations that must be controlled (McCrea, 2005). Beetles can be kept at bay by spraying insecticides around the food crops. Organic industries prefer to use natural alternatives to chemical insecticides such as plant essential oils and their active components (Isman, 2000). Peach aphids and tobacco beetles have been known to be repelled by the applications of clove bud oil and its active component, eugenol, as well as oregano oil and its active component, carvacrol, at concentrations of 0.18%, 0.225%, 0.3%, 0.45%, and 0.9% (Isman, 2000). Insects and wildlife can be contained by the use of sprays and other physical barriers. However, the real challenge is posed by bird intrusion. The presence of insects and other soil flora is a natural attractant for various species of birds (Landis et al., 2000). Also, the availability of nesting material in the form of discarded produce makes the farm environment a place for birds to frequently fly over or into. Bird feces can be a source of in-field contamination due to the presence of several pathogens such as Campylobacter and Salmonella (Sibanda et al., 2000). Some farms still make use of scarecrows and balloons in the field to keep birds away (Sibanda et al., 2000). Some farms, depending on their net profit, are able to afford and install rotatory devices at regular intervals that create a flutter in the air stream, disrupting bird flight patterns. Small holding farms in Zimbabwe also have water jets that shoot streams of water high up in the air to prevent birds from flying over the fields (Sibanda et al., 2000). Because the complete eradication of most kinds of pests is impossible, certain measures are generally used to control the intrusion and infestation. Farm and management personnel are trained to implement control measures to ensure safe and sustainable production of fresh produce, especially in the field of organic agriculture, wherein certifying authorities have strict permissible limits and monitoring schedules.

4 POSTHARVEST STRATEGIES 4.1 Chlorine Postharvest decontamination is an important step in the production lines associated with fresh cut produce including leafy greens and fruits (Sy et al., 2005a,b). Minimally processed B. QUALITY AND SAFETY CONCERNS OF ORGANIC FOOD

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fruits and vegetables (MPFV) have a short shelf life due to their metabolism and the action of spoilage microorganisms (Sy et al., 2005a,b). The produce industry has been using chlorine in both gaseous form as well as liquid bleach as sanitizers (Sy et al., 2005a,b). Gaseous chlorine in the form of chlorine dioxide (ClO2) has been used widely to prevent contamination of fresh produce. The permissible levels in the organic industry are 50–100 ppm in such a way that the residual chlorine in the wash water is only 4 ppm (Sy et al., 2005a,b). A study evaluated the sanitizing properties of various concentrations (50, 75, 100 ppm) of gaseous chlorine dioxide against common foodborne pathogens such as Salmonella, Listeria monocytogenes, and Escherichia coli O157:H7 as well as yeasts and molds on foods such as fresh cut, organic cabbage, lettuce, apples, peaches, carrots, tomatoes, and onions. Though there was no significant reduction in the yeast and mold population, substantial reductions in populations were seen of the pathogens on apples, tomatoes, and onions but not on cabbage, carrots, and lettuce (Sy et al., 2005a,b). This study also indicated that there were no marked adverse sensory effects on the lettuces, cabbages, onions, tomatoes, carrots, or peaches after treatments with the gas (Sy et al., 2005b). Kim et al. (2006) investigated the sanitizing effect of chlorine dioxide and other sanitizers against Enterobacter sakazakii on produce such as organic strawberries, lettuce, cantaloupes, tomatoes, and apples. Among the sanitizers evaluated, with effects of storage temperatures being taken into consideration, chlorine dioxide at 50 μg/mL turned out to be the most effective with liquid chlorine at 50 μg/mL being an equally good sanitizer (Kim et al., 2006). Chlorine dioxide is a powerful oxidizing agent that can be used as a decontaminant. It does not form significant amounts of chlorinated byproducts as elemental chlorine (Go´mez-Lo´pez et al., 2009). The efficacy of chlorine dioxide on both organically and conventionally grown minimally processed foods such as lettuce, carrots, blueberries, and strawberries was investigated, and no adverse effects both in visual and sensory analyses were observed (Go´mezLo´pez et al., 2007; Sy et al., 2005a). An approach to develop sanitizers that reduces the use of water led to the application of gaseous chlorine as a preventive sanitizer for fresh produce € (Olmez and Kretzschmar, 2009).

4.2 Hydrogen Peroxide Hydrogen peroxide is a sanitizer that has been used both in the produce industry as well as € in grocery stores to wash produce, including fresh fruits and vegetables (Olmez and Kretzschmar, 2009). Depending on the reaction and substrates, this sanitizer is a popular choice attributed to its strong oxidation and reduction potential. The mode of action of hydrogen peroxide is to interfere with the redox reactions in the bacterial cell (Rao, 2017). The reactive oxygen species (ROS) generated by an enzyme catalyzed reaction affect the basic biomolecules in cells, which include the nucleic acids, proteins, and sugar and lipid moieties in a cell (DeQueiroz and Day, 2007). Hydrogen peroxide is used to sanitize produce in the field, both in organic as well as conventional agriculture (Sy et al., 2005a,b). According to the USDA-American Marketing Service (AMS), a 30% solution of hydrogen peroxide is used to generate working solutions of 0.01%–0.3%. There are usually no side effects associated with the use of this sanitizer as none of the sensory attributes are influenced (Rao, 2017). However, some noticeable effects such as browning and discoloration of the fruits including strawberries and raspberries have

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been observed with 0.5% hydrogen peroxide (Sy et al., 2005) due to the oxidation of fruit tissue. However, this trait could be considered undesirable in the produce industry, which relies on sensory attributes and aesthetic appeal as marketing strategies. Also, the presence of organic matter has to be taken into consideration while evaluating the efficacy of H2O2 as a sanitizer, because the efficacy is reduced in the presence of organic matter (Rao, 2017).

4.3 Natural Plant-Based Antimicrobials Consumers today are more aware of the health implications associated with chemical and synthetic sanitizers and prefer natural and organic sanitizers (Gould, 1996). The demand for these compounds has catapulted these sanitizers into the spotlight. It is a well-known fact that essential oils derived from plant sources have been used as flavorings and fragrances in the food and perfume industry, and have gained popularity due to their antimicrobial activity. Several studies have shown that phytoantimicrobials can be potent bactericidal compounds even in small concentrations such as 0.1%–1% (Ravishankar et al., 2008; Zhu et al., 2014). However, the main drawback of phytocompounds is that they can offset the flavor profile of the food product. These compounds are good candidates for application in a multiple hurdle approach and can be used in small quantities. As an added advantage, these compounds have residual activity and do not lose efficacy in the presence of organic matter (Nazer et al., 2005).

4.4 Essential Oils and Their Active Components Essential oils are composed of organic, aromatic compounds, which include polyphenols, aldehydes, and alcohols in plant-based extractions. These compounds are extracted from various parts of the plants such as leaves, bark, flowers, fruits, and seeds, among others. Already popular for their flavors and fragrances, these extractions are used extensively in the food and cosmetic industry (Bakkali et al., 2008). Essential oils and their active components are well known for their potent antimicrobial activity. Ravishankar et al. (2008) showed that the active components of cinnamon and oregano oils, namely, cinnamaldehyde and carvacrol, are effective in reducing Campylobacter jejuni and also were effective against multidrug resistant Salmonella serotypes on both celery and oysters (Ravishankar et al., 2010). Essential oils and their active components are preferred natural substitutes to chemical antimicrobials. However, little is known about their mode of action, and there could be multiple targets of action in a microbial cell due to the presence of multiple active components and, therefore, it is difficult to predict if and when resistance patterns will emerge in foodborne bacteria. Also, the flavor and sensory profiles need to be determined before implementation at the field level to identify consumer preferences and responses.

4.5 Plant Extracts Plant extracts are powders or liquids sourced from parts of the plants that include flowers, fruits, leaves, roots, etc. The juice of these plant parts can be lyophilized and powdered, or manufactured in liquid form by just purifying the juice or pulp (Bakkali et al., 2008).

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Plant extracts have been evaluated for antimicrobial activity, and many studies have proven the efficacy of these compounds against foodborne pathogens. Moore-Neibel et al. (2012) demonstrated the efficacy of 0.1%, 0.3%, and 0.5% lemongrass oil against S. Newport on organic leafy greens, including romaine and iceberg lettuces and mature and baby spinach, in a concentration and storage time-dependent manner. This study also established that the plant essential oils showed residual activity and retained their antimicrobial activity upon storage at refrigeration temperatures. Jaroni and Ravishankar (2012) evaluated the effects of hibiscus extracts against E. coli O157:H7, S. enterica, and L. monocytogenes in vitro. No survivors were detected at 24 h on lettuce, alfalfa sprouts, or in the extract itself for E. coli O157:H7 and S. enterica, whereas reductions were seen in the population of L. monocytogenes ( Jaroni and Ravishankar, 2012). Even though plant compounds have several benefits in comparison to synthetic/chemical additives, one major issue faced by the produce industry from their application could be the adverse effects on the organoleptic properties of treated produce due to the pungency of some of the compounds such as essential oils or their active components (Rada et al., 2016). To overcome this issue, a combination application may be a viable option, where an aromatic essential oil or an active component of essential oil can be combined with a nonaromatic plant extract, both at lower concentrations. Use of lower concentrations of these compounds could help alleviate the adverse effects on the sensory properties of treated produce. The efficacy of 0.1% cinnamon or oregano essential oils in combination with 3% olive extract against S. enterica serovar Newport on organic romaine and iceberg lettuces and baby and mature spinaches was investigated (Rada et al., 2016). These combination treatments induced reductions in Salmonella population of up to 3.5–4 log and 3–4.4 log CFU/g on organic baby spinach and romaine lettuce, respectively, which were better than the reductions obtained when individual treatments were used (Rada et al., 2016). Cinnamon oil alone at 0.1% induced a reduction of less than 1 log, oregano oil alone at 0.1%, a reduction of 1 log, and olive extract alone at 3% resulted in 2.3 log CFU/g reduction, when compared to the PBS control for organic leafy greens after 3 days of storage (Todd et al., 2013; Moore-Neibel et al., 2013). Spinach leaves were inoculated with S. Typhimurium and treated with a combination of 3% grape seed extract and 2% malic acid using an electrostatic spray system (Ganesh et al., 2010). Reductions in Salmonella population ranged from 2.6 to 3.3 log CFU/g after 14 days of storage, and the combination treatment yielded higher reductions in comparison to the individual spray treatment using 3% grape seed extract (Ganesh et al., 2010).

4.6 Edible Films Edible films are made using the pulp of various fruits, vegetables, and other edible plant parts such as the stem, leaves, and roots as well as flowers. The antimicrobial of chosen concentration is added to the pulp and edible films are produced in various shapes and sizes, based on the application. Antimicrobial edible films represent a unique way of applying antimicrobials such as essential oils onto food products. Edible films can also be made from other natural substrates such as algin, chitosan, casein, or whey proteins (Lam and Nickerson, 2013). Edible films can either be used as wrappings on food products or added as ingredients in packages such as salad bags.

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Edible films can have several benefits such as: reducing the microbial load of foods; preventing cross-contamination; preventing browning in some fruits and vegetables; preventing lipid oxidation in foods; preventing loss of moisture; preventing foreign odor pick up by the food product; preventing loss of volatile flavors from foods (Gennadios et al., 1997); and addition of unique flavors to foods from the essential oils in the films. Edible films and coatings can serve as carriers for various food additives, including antimicrobials. The incorporation of antimicrobial compounds into edible films or coatings provides a novel way to control foodborne pathogen contamination (Cagri et al., 2004). Edible apple and tomato-based films containing low levels of plant essential oils (cinnamon, lemongrass, and oregano) and their major constituents (cinnamaldehyde, citral, and carvacrol) reduced populations of E. coli O157:H7, S. enterica, and C. jejuni in vitro (Rojas-Gra€ u et al., 2006; Rojas-Gra€ u et al., 2007; Du et al., 2008). Apple, carrot, and hibiscus-based edible films (Fig. 1) containing three concentrations (0.5%, 1.5%, and 3%) of carvacrol or cinnamaldehyde were added as ingredients in salad bags containing organic leafy greens, and their antimicrobial effectiveness against Salmonella Newport during storage at 4°C for 7 days was evaluated (Zhu et al., 2014). All three types of films containing 3% carvacrol reduced the population of Salmonella by 5 log CFU/g at day 0 and 1.5% carvacrol films reduced Salmonella population by 1–4 log CFU/g at day 7, whereas the films with 3% cinnamaldehyde showed 0.5–3 log reductions on different leafy greens by day 7 (Zhu et al., 2014). Lemongrass oil (1.0%–1.5%) and oregano oil (0.5%) containing apple puree-alginate edible coatings exhibited strong antimicrobial activity against Listeria innocua, reducing the bacterial

Apple film with 3% Carvacrol

Apple film with 3% cinnamaldehyde

Hibiscus film with 3% carvacrol

Hibiscus film with 3% cinnamaldehyde

Carrot film with 3% carvacrol

Carrot film with 3% cinnamaldehyde

FIG. 1 Apple, carrot, and hibiscus-based antimicrobial films that can be wrapped on meat products or added as ingredients in salad bags.

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population to below the limit of detection within 7 days (Rojas-Gra€ u et al., 2007). Films made of partially hydrolyzed sago starch and alginate mixture containing lemongrass oil inhibited E. coli O157:H7 (Maizura et al., 2007). Garlic oil containing chitosan films showed antimicrobial activity against E. coli, Staphylococcus aureus, S. typhimurium, L. monocytogenes, and Bacillus cereus (Pranoto et al., 2005). Oregano oil at 2% in whey protein films was effective against E. coli O157:H7, S. aureus, S. Enteritidis, L. monocytogenes, and Lactobacillus plantarum (Seydim and Sarikus, 2006). The use of 1.5%–2.0% chitosan in the methyl cellulose coating of fresh-cut cantaloupe reduced the growth of mesophilic aerobes, psychrotrophs, lactic acid bacteria, and total coliforms by 3–4 log CFU/g (Krasaekoopt and Mabumrung, 2008). The sensory properties of organic iceberg lettuce and spinach treated with essential oils, their active components, plant extracts, and combinations of essential oils with plant extracts were evaluated and the overall acceptability of iceberg lettuce and spinach treated with cinnamon oil was ranked the highest by the panelists ( Joshi et al., 2016). The effects of antimicrobial edible films (apple, carrot, and hibiscus-based films containing various concentrations of carvacrol and cinnamaldehyde) on the sensory properties of bagged organic spinach were evaluated ( Joshi, 2016), and it was found that the films containing cinnamaldehyde had the highest preference liking and were most likely to be purchased by panelists ( Joshi, 2016). Romaine lettuce treated with apple films had a higher likelihood of being purchased in comparison to other films. The lettuce treated with carrot films had a higher acceptance rating as compared to other films (Rao, 2017).

5 CONCLUSION Many recent produce outbreaks have indicated that control of the possible routes of contamination in the preharvest stages is nearly impossible. Hence, postharvest sanitization of produce becomes a very critical step in inactivating pathogens that could have contaminated them during production, to prevent any outbreaks or recalls. While choosing or designing a sanitizer as well as its mode of application, it is crucial to keep in mind that it should be effective against a wide range of pathogenic and spoilage microorganisms, is environmentally and user friendly, is derived from natural sources, has residual activity, can enable recycling of wash water, and is economical and readily available. With the differences in pre- and postharvest practices, sanitizers for the organic industry need to be evaluated for their efficacy in the presence of heavy organic load. The organic industry has strict regulations that allow for stipulated amounts of artificial chemicals to be used, resulting in possibly higher numbers of microorganisms. Minimal processing is a highly practiced principle in the organic produce industry in which sanitizing is the only kill step, especially for salad vegetables, that are consumed raw. Research is critically needed in this area for fresh and fresh-cut produce that are consumed raw or with minimal processing. An effective sanitizer can help improve microbiological safety of fresh produce and ensure safe and continuous supply of healthy produce.

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Further Reading https://agrochemicals.iupac.org/index.php?option¼com_sobi2&sobi2Task¼sobi2Details&catid¼3&sobi2Id¼31. Naik, M.I., Fomda, B.A., Jaykumar, E., Bhat, J.A., 2010. Antibacterial activity of lemongrass (Cymbopogon citratus) oil against some selected pathogenic bacterias. Asian Pac J Trop Med 3 (7), 535–538. Tzortzakis, N.G., 2009. Impact of cinnamon oil-enrichment on microbial spoilage of fresh produce. Innov. Food Sci. Emerg. Technol. 10 (1), 97–102.

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The Plant Microbiome: Diversity, Dynamics, and Role in Food Safety Sarah M. Allard*, Shirley A. Micallef†,‡ *

Maryland Institute for Applied Environmental Health, School of Public Health, University of Maryland, College Park, MD, United States †Department of Plant Science and Landscape Architecture, University of Maryland, College Park, MD, United States ‡Centre for Food Safety and Security Systems, University of Maryland, College Park, MD, United States

O U T L I N E 1 Introduction

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2 The Phyllosphere and Rhizosphere

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3 Constituents of the Plant Microbiome 3.1 Commensal Plant-Microbe Associations 3.2 Plant Pathogens 3.3 Human Pathogens

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4 Drivers of Microbial Community Structure 4.1 Plant Genotype 4.2 Plant Organ 4.3 Plant Microsite 4.4 Season and Development 4.5 Environment 4.6 Agricultural Management

Amplicon Sequencing (16s/18s/ITS) Metagenomics Metatranscriptomics/Metaproteomics Challenges Associated With Next-Generation Sequencing Methods 5.6 Culture-Based and Alternative Molecular Methods

232 233 233 234 234 235 236 237 237 238

5 Microbial Community Characterization 239 5.1 Culture-Independent Methods 239

Safety and Practice for Organic Food https://doi.org/10.1016/B978-0-12-812060-6.00011-8

5.2 5.3 5.4 5.5

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6 Harnessing the Power of Microbes in Agriculture 243 6.1 Biological Control 243 6.2 Disease-Suppressive Soils 244 6.3 Plant Growth Promotion 245 6.4 Environmental Health 245 6.5 Food Safety 246 7 Conclusions

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1 INTRODUCTION Microorganisms, including bacteria, fungi, oomycetes, and viruses, contribute to many processes important to human health and economic well-being. Microorganisms heavily influence global nutrient cycling, plant and animal health, and the phytoremediation of toxic chemicals (Furnkranz et al., 2008; Ali et al., 2012). Increasingly, studies focused on human medical conditions include a microbial component, as researchers turn toward the microbiome to explain differences in human health outcomes (Turnbaugh et al., 2007; Clemente et al., 2012; Ley et al., 2005; Gevers et al., 2014). Microbes make up a substantial portion of our own biomass and play an important role in human disease incidence, obesity, and behavior (Turnbaugh et al., 2009; Flint et al., 2012; Sampson and Mazmanian, 2015). Similarly, plants support numerous and diverse microbial communities that are intimately connected to their health and function (Lindow and Brandl, 2003; Vorholt, 2012; Lakshmanan et al., 2014; Philippot et al., 2013; Berendsen et al., 2012; Bulgarelli et al., 2013). The large collective genome of microbes associated with plants is often termed the plant’s “second genome” (Berendsen et al., 2012) due to the importance of microbes in plant growth and response to stress. In the context of crop production, plant-associated microbial communities influence growth, yield, nutritional quality, disease management, and safety. Worldwide, microbial plant pathogen infection leads to crop destruction and subsequent loss of income (Oerke and Dehne, 2004; Savary et al., 2017). Human pathogens occurring on crops can lead to illness and death among consumers, as well as to economic consequences for farmers of implicated commodities (Brandl, 2006). On the other hand, the majority of microbes associated with plants are commensal, and beneficial microbes can enhance root architecture, improve efficiency of nutrient uptake, and confer protection from pathogens (Berendsen et al., 2012; Pieterse et al., 2014; Zamioudis and Pieterse, 2012; Mantelin and Touraine, 2004). Study of the agricultural plant microbiome is therefore relevant to consumers, farmers, and health officials due to its influence on human and economic health. Of increasing concern in the agricultural environment is the presence of foodborne pathogens, such as Salmonella enterica, pathogenic Escherichia coli, and Listeria monocytogenes (Olaimat and Holley, 2012; Brandl, 2006). Unlike plant pathogens, which often decrease crop yield and quality (Oerke, 2006), human pathogens are unlikely to cause visible symptoms while the crop is growing, making detection in the field difficult. Enteric pathogens are capable of survival through harvest and processing (Bennett et al., 2015; Toma´s-Callejas et al., 2011; Harris et al., 2003), and once established on the plant surface, they are difficult to eliminate (Parish et al., 2003; Goodburn and Wallace, 2013), posing a serious threat to consumers of fresh-cut produce. In the United States alone, the CDC estimates that 1 in 6 people (48 million total) become sick from foodborne illness every year, and 3000 of those cases result in death (Scallan et al., 2011a,b). Fresh produce is implicated in 46% of foodborne illnesses (Painter et al., 2013). Efforts to reduce foodborne disease from fresh produce increasingly focus on prevention of contamination of fruits and vegetables, both pre- and postharvest. Good Agricultural Practices have been established to give farmers recommendations on cropping practices that strengthen on-farm food safety risk mitigation by reducing opportunities for contamination through microbiological water quality monitoring, effective animal waste processing, wildlife management, and worker education and training (FDA et al., 1998). The recent implementation of the Produce Safety Rule, part of the US Food and Drug Administration (FDA) Food Safety

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Modernization Act, similarly emphasizes prevention, by requiring the adoption of safe on-farm pre- and postharvest practices (PSR, 21 CFR 112). Direct interactions between plant hosts and foodborne pathogens are important in understanding on-farm food safety, but fluctuations in these interactions highlight the necessity for further research that identifies external influences. A holistic approach that considers agricultural and environmental conditions in relation to the plant microbiome as contributors to human pathogen-plant interactions will lead to a more complete understanding of the phytobiome. Such knowledge would inform efforts to reduce the risk of foodborne pathogen contamination of produce. Recent advances in molecular technology have changed the state of plant microbiome research, allowing for replicated high-throughput studies under manipulated conditions (Guttman et al., 2014). These advances have allowed scientists to characterize microbiota and interpret functional importance for diverse habitats. Environmental and human-driven factors in agriculture likely influence the crop microbiome in a way relevant to food safety and security, but the application of these methods to fresh produce safety is still in the early stages, and there are many basic questions that need to be answered for the field to move forward. This chapter examines current and classic research on the plant microbiome, with a focus on microbial dynamics of the phyllosphere and rhizosphere in relation to agriculture and produce safety.

2 THE PHYLLOSPHERE AND RHIZOSPHERE The interactions between plants and their associated microbes are complex and varied. The coined phrase, “Microbes wear their guts on the outside” ( Janzen, 1985) emphasizes the importance of microbes in plant growth and defense, and the intimate relationship that exists between the two. Research into the community structure and function of epiphytic bacteria, fungi, and archaea associated with plants is most often divided into two plant regions. The phyllosphere constitutes the aboveground surfaces of the plant, mostly composed of the leaves but also including blossoms, fruit, and stems (Vorholt, 2012), whereas the “rhizosphere” describes the area immediately surrounding and under the influence of plant roots (Lynch and Leij, 1990). Differences in nutrient availability and environmental pressures between the two plant regions contribute to their distinct microbial community diversity and structure. Although unique, both the phyllosphere and the rhizosphere support complex microbial assemblages (Ottesen et al., 2013; Bodenhausen et al., 2013; Micallef et al., 2009b). Bacteria are the most numerous inhabitants of the phyllosphere and rhizosphere (Vorholt, 2012; Bulgarelli et al., 2013), although filamentous fungi and yeasts are also present (Andrews and Harris, 2000; Ina´cio et al., 2002). Bacterial volume is estimated at up to 1011 cells per gram in the rhizosphere and up to 108 cells per gram in the phyllosphere (Berendsen et al., 2012; Lindow and Brandl, 2003). Roots provide a surface area for bacterial attachment, as well as a source of nutrients from root exudation and sloughed-off cells (Hawes et al., 2002; Micallef et al., 2009b). The phyllosphere may be a more ephemeral environment; seasonal changes in foliage or differences in an annual versus perennial existence can lead to drastic habitat changes for microbiota (Vorholt, 2012). Phyllosphere microorganisms must contend with rapid changes in host plant development and even senescence and death. The harshness of the phyllosphere habitat is

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characterized by substantial fluctuations in nutrients, water availability, and temperature, as well as constant exposure to damaging ultraviolet radiation and plant-derived reactive oxygen species (Vorholt, 2012; Lindow and Brandl, 2003; Muller and Ruppel, 2014). Despite these challenging conditions, many microorganisms have adapted to survive in the phyllosphere, on the leaf surface, in the leaf apoplast, or on the surface of flowers and fruit (Rastogi et al., 2013). The phyllosphere provides an enormous surface area for microbial colonization, comprising one of the largest microbial habitats on Earth (Vorholt, 2012; Bulgarelli et al., 2013). A better understanding of the complex mechanisms by which human enteric pathogens attach to and persist within crop plants in the rhizosphere and phyllosphere may lead to the development of targeted prevention strategies and suggestions to farmers on best practices for prevention of foodborne contamination originating in their fields. Furthermore, an understanding of how the diverse microbial communities associating with plant hosts may influence human enteric pathogen colonization and survival will be essential to fully characterizing these interactions and may eventually be used for risk assessments and interventions.

3 CONSTITUENTS OF THE PLANT MICROBIOME 3.1 Commensal Plant-Microbe Associations Symbiotic relationships such as mutualism, parasitism, and commensalism drive the dynamic between plants and their associated microbial communities. The vast majority of microbes in the phyllosphere and rhizosphere are commensal, exerting no negative influence on plant growth and development and, in fact, often conferring a positive effect (Bulgarelli et al., 2013). Many microbes profit from associating with plants, receiving a habitat for colonization and exuded phytocompounds for metabolism. Plants may benefit from more efficient nutrient acquisition, increased growth, protection from plant pathogens, and enhanced response to biotic and abiotic stress factors (Berg, 2009). In the rhizosphere, nitrogen fixation has been well documented (Berg, 2009; Bulgarelli et al., 2013; Chaparro et al., 2012; Esperschuetz et al., 2007). Rhizobia in the root nodules of legumes and free-living bacteria and archaea fix atmospheric nitrogen to a form usable by plants, receiving carbon exudates and habitat in exchange for providing this service (Philippot et al., 2013). Nitrogen fixation has also been described in the phyllosphere, although not nearly as extensively (Freiberg, 1998; Furnkranz et al., 2008). In the soil, microbes also contribute to enhanced soil stability, which helps increase water retention and uptake. Bacteria, fungi, and yeasts have all shown an ability to release indole-3-acetic acid, an auxin hormone that can stimulate root growth in plants (Berendsen et al., 2012). By stimulating root growth, these microbes increase the available colonizable surface area in the rhizosphere and root exudate volume, allowing for expansion of their own populations. In the rhizosphere, these characteristics have been extensively studied and are now being applied in the field (Ahemad and Kibret, 2014; Timmusk et al., 2017). In the phyllosphere, plant growth promotion has not been investigated in depth and represents an avenue for future research. Induced systemic resistance (ISR) occurs through colonization of plant roots by plant growth-promoting rhizobacteria (PGPR), which confer resistance to a variety of phytopathogens to noncolonized plant structures (Beneduzi et al., 2012; Somers et al., 2004;

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Pieterse et al., 2014). The priming of plant defenses by ISR has been well characterized (Bulgarelli et al., 2013; Haas and Defago, 2005; Shoresh et al., 2010; Yogev et al., 2010; Zamioudis and Pieterse, 2012). In the phyllosphere, microbial assemblages may reduce pathogen establishment or successful infection by acting as a barrier between the plant surface and the environment, through competitive exclusion and biocontrol. Some commensals may be more adapted to scavenging nutrients from the phyllosphere and may secrete toxic metabolites that reduce pathogen viability. Studies have shown that axenic (sterile) plants are more susceptible to disease compared to naturally colonized plants (Innerebner et al., 2011). Although the mechanisms are not yet well characterized, phyllosphere microbiota clearly can play a role in reducing pathogen infection in host plants.

3.2 Plant Pathogens Pathogenic bacteria and fungi in the phyllosphere and rhizosphere can pose a threat to plant productivity and food security (Savary et al., 2012). Although these pathogenic organisms make up only a small part of the phyllosphere and rhizosphere communities, they can have an enormous impact on crop yield, as well as local and global economies. In the US, approximately 10% of crops are lost to plant pathogens each year, resulting in a multibillion dollar economic loss (Arora et al., 2012). These pathogens may reduce marketable yield by decreasing growth, distorting crop shape, infecting fruit with toxins, or decreasing shelf life. Furthermore, the coexistence of human and plant pathogens in the field can facilitate survival of enteric pathogens. For example, Xanthomonas perforans, causal agent of tomato bacterial spot, suppresses pathogen-associated molecular pattern triggered immunity; when Salmonella is present during X. perforans infection, survival is increased tenfold (Potnis et al., 2014). The dynamics of plant pathogens and the host immune system have been extensively reviewed ( Jones and Dangl, 2006; Dodds and Rathjen, 2010; Glazebrook, 2005) and will not be discussed in detail here.

3.3 Human Pathogens Although crop losses due to plant pathogen infection are important to human health in terms of food security (Savary et al., 2017), occurrence of human pathogens results in unsafe food that poses a tremendous public health burden through gastrointestinal disease, economic losses, and damage to the implicated industry (Scharff, 2012; Scallan et al., 2015). Enteric pathogens are not typically pathogenic to the plant itself but can cause serious disease or even death in humans. Human enteric pathogens including S. enterica and E. coli O157:H7 have been identified as the disease-causing agent in many recent gastroenteritis outbreaks linked to the consumption of fresh produce such as tomatoes, leafy greens, and cucurbits (Teplitski et al., 2011; Greene et al., 2008). Although enteric pathogens are adapted to colonize and infect gastrointestinal tracts of animal hosts, several of the most virulent microbes have evolved an ability to, at least temporarily, also colonize plants (Teplitski et al., 2011; Zheng et al., 2013) and persist in the environment (Bell et al., 2015; Martinez-Urtaza et al., 2004; Silva et al., 2014; Strawn et al., 2013a).

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Seasonality is one of the strongest predictors of foodborne pathogen contamination risk, but certain agricultural management factors may also play a part (Pagadala et al., 2015; Marine et al., 2015; Strawn et al., 2013b; Park et al., 2012). It is becoming increasing clear that foodborne pathogens such as S. enterica may be able to survive long term in the environment, as observed in surface water and sediment (Bell et al., 2015; Micallef et al., 2012). These enteric pathogens have shown an ability to internalize into plant tissues and may persist if introduced to the environment through contaminated irrigation water or soil (Guo et al., 2001; Zheng et al., 2013; Barak et al., 2011), or through flower inoculation (Shi et al., 2009). Some enteric pathogens influence phyllosphere and rhizosphere dynamics, becoming an integral and influential part of the plant’s microbiome (Barak and Schroeder, 2012; Teplitski et al., 2011). Flower contamination with enteric pathogens has been linked to changes in microbial communities associated with developing fruit, showing that pathogens can play an important role in shaping phyllosphere community structure (Shi et al., 2009). Salmonella colonization of tomato plants is both cultivar-dependent (Barak et al., 2011) and organdependent (Zheng et al., 2013). Damage to tomato roots has been shown to increase internalization rates, and certain serovars differentially colonize the flowers, leaves, and roots (Zheng et al., 2013; Han and Micallef, 2014). Type III secretion systems (TTSS), essential for plant pathogen establishment, are evolutionarily conserved between plant and animal pathogens (Galan and Collmer, 1999), and studies have shown that TTSS can enhance survival of human pathogens on plants (Barak and Schroeder, 2012). Lipopolysaccharide was also needed for Salmonella colonization of tomato fruit, representing another shared mechanism between plants and animals (de Moraes et al., 2017). On the other hand, the AgfD gene, a master regulator of aggregative behavior in S. enterica, allowed for enhanced leaf attachment (Romling et al., 2000), although this gene does not enhance virulence in animal hosts. The identification of genes uniquely needed for survival on plants shows that the ability of enteric pathogens to colonize the phyllosphere is not purely due to conserved mechanisms between plant and animal pathogenicity. As research continues to explore the dynamics between human pathogen-plant interactions, it is becoming clearer that some foodborne pathogens have evolved specific adaptations for the agricultural environment, gaining a competitive advantage by utilizing plants as vectors to their next hosts (Barak and Schroeder, 2012; Fletcher et al., 2013).

4 DRIVERS OF MICROBIAL COMMUNITY STRUCTURE Microbial life associated with plants differs across multiple scales, from landscape to plant genotype to plant organ microsite. Many studies have sought to establish a hierarchy of importance for potential factors influencing bacterial community structure in the phyllosphere and rhizosphere, however results have differed across different host plants, locations, and environmental factors. Similarly, risk factors for human pathogen incidence on plants differs across these scales and in response to the same factors.

4.1 Plant Genotype Plant genotype has a documented influence on microbial community structure in multiple systems (Whipps et al., 2008; van Overbeek and van Elsas, 2008; Micallef et al., 2009a,b). In the C. RECOMMENDATIONS AND INTERVENTION FOR IMPROVING SAFETY

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rhizosphere, root exudates and root morphology differ across plant species and cultivars, shaping the structure and function of rhizosphere microbial communities in conjunction with soil type (Berg and Smalla, 2009). Root exudates, including nutrients and secondary metabolites, may enhance or decrease survival of certain microbial constituents of the rhizosphere (Micallef and Colo´n-Carmona, 2013). Rhizodeposits used as carbon sources, including sugars, mucilage, root border cells, and dead root cap cells, vary in composition and volume depending on plant genotype and environment ( Jones et al., 2009), as do antimicrobial and growth-promoting secondary metabolites (Wink, 2003). Although soil type has been described as a dominant driver (Bulgarelli et al., 2012), from the pool of highly diverse microorganisms in the soil environment, plants may recruit certain organisms suited to the rhizosphere and beneficial for plant growth and protection, allowing these organisms to increase in abundance and activity (Philippot et al., 2013; Micallef et al., 2009b; Berendsen et al., 2012; Kim et al., 2011), and are modulated as plants develop (Micallef et al., 2009a). Field history may also play an important role, as indicated by a study reporting differences in tomato rhizosphere communities attributed to previous cover crop systems (Han and Micallef, 2014). Plant-regulated recruitment extends to the phyllosphere as well. On the microbiome scale, different cultivars of the same plant species host distinct phyllosphere communities both epiphytically and endophytically (Correa et al., 2007; Rasche et al., 2006; Sessitsch et al., 2002). In fact, the effect of plant genotype on plant microbiomes has often been identified as stronger than other factors, and differences in interactions between specific microorganisms and plants may influence plant exudation that further drives microbial activity and community structure (Ryffel et al., 2016). Geographic location has been identified as a driving factor in many studies profiling phyllosphere communities (Perazzolli et al., 2014; Rastogi et al., 2012; Belisle et al., 2012; Finkel et al., 2011), however other studies have found limited influence of geographic location on phyllosphere communities of plants with the same genotype (Redford et al., 2010). Studies have shown that different plant species growing close together in the same soil harbor diverse phyllosphere microbial communities (Delmotte et al., 2009; Knief et al., 2010), indicating that plant genotype may be a stronger driver of microbial community structure than geographic location. Even at the cultivar level, differences in leaf and fruit exudate profiles may lead to differential success for specific bacteria, including enteric pathogens. On tomato plants, S. enterica growth and survival vary across leaves and fruit of different plant cultivars (Han and Micallef, 2014). These differences in survival correlate with differences in surface metabolite profiles (Han and Micallef, 2016), some of which individually restrict Salmonella growth on fruit (Dev Kumar and Micallef, 2017). Inside the fruit, S. enterica survival similarly fluctuates based on tomato cultivar (Noel et al., 2010).

4.2 Plant Organ Within a specific plant, microbial abundance and diversity differ between the phyllosphere and rhizosphere in general, but differences are clear at even finer scales. On tomato plants, microbial diversity has been shown to decrease as distance from the soil increases, and surface-dwelling microbial communities differ between lower, upper, and middle leaves, as well as between blossoms, fruit, and roots (Ottesen et al., 2013; Allard et al., 2016). C. RECOMMENDATIONS AND INTERVENTION FOR IMPROVING SAFETY

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Furthermore, survival of specific Salmonella serovars vary based on plant organ, suggesting niche fitness at the subspecies level (Zheng et al., 2013). Several dominant phyla, including Proteobacteria, Actinobacteria, Bacteriodetes, and Firmicutes, are consistently part of a core microbiome on the leaf surface (Bulgarelli et al., 2013; Whipps et al., 2008; Rastogi et al., 2013). Flower-associated microbial communities also may support a fairly consistent core microbiome, which contains several of the same bacterial taxa as well as additional fungal constituents across different plant types (Aleklett et al., 2014). Fruit and vegetable surfaces support common taxa as well, but diversity and community structure vary by plant type; tree fruits such as apples and peaches share similar community structure, as do tomatoes and peppers (Leff and Fierer, 2013). At the family level, many produce types support a high abundance of Enterobacteriaceae, often in conjunction with a relatively low species richness (Leff and Fierer, 2013). This has relevance for food safety, as several foodborne pathogens commonly associated with fresh produce outbreaks are classified as Enterobacteriaceae, a family apparently well adapted to the phyllosphere. Although plant anatomy drives much of the difference between plant-associated microbial communities, environmental factors can also play a significant role. Rhizosphere communities of tomato shifted in response to gradients of clay content across a field, whereas tomato phyllosphere communities were influenced by factors correlated to distance from the road (Allard et al., 2016). This study indicates that, although plant organ is a dominant driver of microbial communities, differences in microbial diversity in the surrounding microbial reservoirs may ultimately determine the pool from which plant organs can recruit.

4.3 Plant Microsite At even finer spatial levels, such as between the trichomes and stomata of leaves, or between the stigma and style of flowers, microbial communities may be distinct, with some microbes being preferentially attracted to certain exudates and characteristics specific to those microsites (Leveau and Lindow, 2001; Miller et al., 2001; Aleklett et al., 2014). In fact, individual microbial species may use different strategies to survive on diverse microsite habitats. Transcriptional studies have shown that Pseudomonas syringae, a common constituent of the phyllosphere, exhibits motility on the leaf surface but not in the apoplast, instead expressing genes that enhance resistance to plant defense response in the apoplast (Yu et al., 2013). Similarly, Methylobacterium extorquens expression differs between epiphytic leaves, roots, and synthetic growth medium, producing more abundant proteins related to stress response and alternative substrate utilization in the phyllosphere (Gourion et al., 2006). In flowers, yeast species differ significantly between inner and outer corolla, as well as between floral rewards (nectar and pollen) and the rest of the flower structure (Pozo et al., 2012). On tomato leaves, Salmonella preferentially colonizes trichomes on the leaf surface (Barak et al., 2011), and both Salmonella and E. coli may internalize through open stomata (Kroupitski et al., 2009; Deering et al., 2012; Shaw et al., 2008). On the tomato fruit, the porous and protective region of the stem scar has demonstrated enhanced host potential for Salmonella even after sanitation efforts (Guo et al., 2002; Wei et al., 1995). Microbial structure and function appears to be highly specialized to microsites within all plant organs, at even the smallest scale.

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4.4 Season and Development Microbial communities can be dynamic throughout the seasons or the life cycle of plant tissues, adding a temporal component to the study of the plant microbiome. Apple flowers host a diverse array of microbes, with community changes occurring consistently over time from before flower opening through flower senescence (Shade et al., 2013). Similarly, spinach leaves have shown that leaf-surface dwelling microbial communities become more complex and change in structure throughout the life of the leaves (Lopez-Velasco et al., 2013). In the rhizosphere of Arabidopsis thaliana, differences in abundance of certain phyla were observed between several developmental time points (Chaparro et al., 2014; Micallef et al., 2009a). Other studies, however, have found that leaf surface-dwelling microbes are fairly consistent over the development of the leaf (Delmotte et al., 2009). Taken together, these studies indicate that a bacterial succession occurs as plants develop, and microenvironments present on plant surfaces are variable enough to support significantly different communities on various temporal, developmental, and spatial scales. However, the relative importance of these factors, in relation to other factors, in shaping microbial community structure and diversity remains unclear. Clarification of the spatiotemporal dynamics of phyllosphere communities could help elucidate the when, where, and why of human pathogen colonization in plants.

4.5 Environment In conjunction with the plant habitat over different spatial and temporal scales, environmental factors contribute to bacterial community structure in the phyllosphere, both in the establishment of plant microbiomes and throughout the life of the plant. Inoculum for initial colonization of the phyllosphere may come from a variety of sources including air, water, seed, soil, or animal vectors (Bulgarelli et al., 2013; Vorholt, 2012; Ushio et al., 2015; Aizenberg-Gershtein et al., 2013; Rastogi et al., 2012; Lopez-Velasco et al., 2013). Within plant genotypes, specific organs of the phyllosphere have demonstrated core communities, with the same phyla—often plant species- and organ-specific—appearing year to year despite aging or newly established hosts (Knief et al., 2010). This indicates one or more environmental reservoirs of complex microbial inocula as well as stable or recurring plant characteristics that support the establishment of certain microbes on a consistent basis (Vorholt, 2012). One study comparing the microbiomes of artificial plastic and live tomato plants in the field showed that a combination of environmental factors are instrumental in shaping the plant microbiome; many taxa were shared on plastic and real plants (Ottesen et al., 2016b). Air, one potential source of microbiota, may be an important factor in early phytobiome establishment, but some studies have indicated that its influence may be specific to certain developmental time points or plant species (Vokou et al., 2012; Fahlgren et al., 2010; Maignien et al., 2014). Rainfall has been linked to changes in the prevalence of nonpathogenic indicators of fecal contamination in lettuce fields (Xu et al., 2016) and also larger scale bacterial community changes (Copeland et al., 2015; Allard, 2016). In most cases, soil and phyllosphere communities do not share many dominant phyla, indicating that soil is not a strong source of microbial inoculum for the phyllosphere (Kim et al., 2012; Bodenhausen et al., 2013; Knief et al., 2012), and functions in the soil and rhizosphere may be very different from those in the phyllosphere. The consistency of plant microbiome communities across seasons and generations could be

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partially explained by transmission from other nearby plants serving as microbial reservoirs (Vorholt, 2012). Vertical transmission from seed to plant represents another potential avenue of inoculum, sometimes termed the “maternal effect.” Lopez-Velasco et al. found that some core phyla, including Proteobacteria, Firmicutes, and Acidobacteria, are present both in seeds and at multiple stages of spinach plant development. The number of distinct OTUs (Operational Taxonomic Units at 97% identity) nearly tripled between the cotyledon and full-grown plant stages, however, indicating that any maternal effect was only a part of a greater picture, necessitating additional sources of inoculum (Lopez-Velasco et al., 2013). Microbial inoculum can travel between plants through pollinators and other animal visitors, however more research is need to clarify these relationships (Aleklett et al., 2014; Ushio et al., 2015; Pozo et al., 2012). Although insects have been identified as potential vectors of human pathogens (Olsen and Hammack, 2000; Pava-Ripoll et al., 2015), they also can carry and transmit a diverse array of beneficial microbes, which could exert a protective effect on floral or other plant surfaces. Diversity of pollinators is not influenced by organic versus conventional management practices when comparable wild plant diversity and habitat is available (Winfree et al., 2008), however increased habitat fragmentation associated with intensified agricultural production may lead to a decrease in pollinator diversity (Kremen et al., 2002). Whether a more diverse pollinator community will likely decrease or increase the risk of pathogen establishment remains unclear. The complexity of how numerous environmental sources of inoculum interact together with the plant to shape plant-associated microbial composition and structure makes plant microbiome source-tracking a rich and understudied avenue for continued research.

4.6 Agricultural Management The use of organic versus conventional management, encompassing a variety of differences in pest and nutrient management approaches, may lead to the maintenance of distinct phyllosphere (Ottesen et al., 2009) and rhizosphere bacterial communities (Bulluck et al., 2002; Esperschuetz et al., 2007). Long-term organic management may lead to increased microbial diversity in rhizosphere soils (Hartmann et al., 2015), possibly linked to differences in pH and water activity compared to conventionally managed soils (Chou et al., 2017). One of the most influential differences between conventional and organic management is choice and use of fertilizer. Biological soil amendments, used in organic agriculture as sources of plant nutrition, have shown some influence on rhizosphere communities (Esperschuetz et al., 2007; Jangid et al., 2008; Lavecchia et al., 2015; Peiffer et al., 2013; Das and Dhar, 2012; Ling et al., 2016; Hartmann et al., 2015), however in some cases the influence of soil properties and soil amendment application were inconsistent and unclear (Tian and Gao, 2014; Gao et al., 2015; Tatti et al., 2012; Allard et al., 2016). In the phyllosphere, the influence of soil amendment application and many other agricultural management practices is similarly unclear (Allard et al., 2016; Zarraonaindia et al., 2015; Badri et al., 2013). Pest management strategies typical of organic or conventional agriculture could also influence microbial communities. Biological and chemical pesticide application appears to have little influence on phyllosphere microbial community structure in grape systems (Perazzolli et al., 2014), whereas copper pesticide application had a weak but significant effect on tomato phytobiomes (Ottesen et al., 2015).

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The use of manure in agriculture is somewhat controversial in terms of food safety. Since organic growers use animal-derived fertilizer (fresh or composted manure) as a primary source of plant nutrition, it has been posited that organically grown produce will be associated with a higher risk of contamination with enteric human pathogens. Many consumers on the other hand assume that organically grown produce is “safer” than its conventional counterpart (Berlin et al., 2009; Williams and Hammitt, 2001). In actual fact, studies do not tend to support or refute this—many studies comparing the microbiological safety of conventional versus organic produce tend to show no differences in microbiological safety risk (Magkos et al., 2006; Bourn and Prescott, 2002; Diez-Gonzalez and Mukherjee, 2009; Marine et al., 2015; Pagadala et al., 2015). Many of these studies have used indicator bacteria, such as generic E. coli and fecal coliforms, to assess risk, however these indicators have been shown to have little to no correlation with the presence of pathogens (Wu et al., 2011; Pachepsky et al., 2014). The US FDA has acknowledged this research gap, deciding to delay the inclusion of manure use regulations in the Produce Rule of the Food Safety Modernization Act until sufficient research has been conducted. More indicative and comprehensive methods are needed to assess the relative risk of agricultural management practices, including use of manure, on produce safety. It is possible that fertilizer choice could lead to introduction of unwanted pathogens, although no shifts in the phyllosphere communities of tomato fruit and flowers were detected in a study comparing chemical fertilizer to poultry litter (Allard et al., 2016). Further research on a variety of crops is needed to assess whether any change in resident plant-associated microbial communities due to fertilization could in turn influence the opportunities for pathogen colonization in the phyllosphere.

5 MICROBIAL COMMUNITY CHARACTERIZATION 5.1 Culture-Independent Methods In light of the impressive influence that microbes have on plant life, it is clear that efforts to improve crop yield, disease resistance, and protection against human pathogens should consider microbial contributions to these processes. Historically much of the research designed to study microbial communities has been dependent upon culturing methods, however culturing selects for only those strains that are able to grow in a lab setting and can vastly underestimate the diversity and abundance of microbes in the environment (Rappe and Giovannoni, 2003). Today, culture-independent methods are becoming more widespread and accessible. Using next generation sequencing technology, it is possible to isolate and sequence DNA and RNA directly from environmental samples, providing a clearer picture of the actual and relative abundance of microbiota in the environment, as well as the functional activity of each community. Sequencing-based microbial characterization is a growing field, and it is somewhat unique in the realm of science today in that many studies using these methods are based on data mining rather than hypothesis testing (Wooley et al., 2010). Many studies begin by comparing two or more conditions, looking to see what differs between the two before forming hypotheses and designing follow-up experiments. Advances in technology and in the general body of knowledge of the plant microbiome are making replicated studies more possible and applicable, and hypothesis testing more feasible (Knight et al., 2012; Beattie, 2015).

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QUESTIONS TO ADDRESS WHEN CHARACTERIZING MICROBIAL COMMUNITIES INCLUDE: 1. 2. 3. 4. 5. 6. 7.

What is the community structure (identification and abundance of OTUs)? What functions can be carried out (what genes are present)? What functions are actively being carried out (what transcripts and/or proteins are present)? How are community (alpha diversity) and structure (beta diversity) related? How might structure and function change under different treatment conditions? What microbiota tend to co-occur? Are there keystone taxa that serve essential functions in complex communities?

5.2 Amplicon Sequencing (16S/18S/ITS) Ribosomal RNA may be used to characterize bacterial and fungal communities when identity and diversity of microbes is of primary interest to the study. This is often called amplicon sequencing, as a small region of microbial DNA is amplified from environmental samples using PCR, and sequences are compared to a database or assembled de novo to investigate microbial community structure and diversity (Mizrahi-Man et al., 2013; Muller and Ruppel, 2014). The 16S and 18S regions of the small ribosomal subunit of prokaryotic and eukaryotic organisms, respectively, contain both highly conserved and highly diverse sequences, making them ideal for constructing phylogenies and identifying microorganisms. The Internal Transcribed Spacer (ITS) region is increasingly used instead of 18S in amplicon sequencing of environmental fungi due to enhanced resolution across a broad range of species (Schoch et al., 2012). Amplicon sequencing may not be the most robust choice if the objective is to investigate functional diversity in microbial communities or activity on a short timescale. DNA may persist in the environment from dormant or dead microorganisms, and live organisms may contribute to function in an ecosystem disproportionately to their dominance (numerical abundance) (Kuczynski et al., 2010). Furthermore, differences in microbial community structure may not necessarily indicate differences in function; resilience and redundancy in function within communities may allow communities to maintain function under changing conditions (Allison and Martiny, 2008). Although this method is far from perfect, it is the most widely used for microbial characterization, and reference databases and data analysis pipelines are currently superior to those for other technologies.

5.3 Metagenomics Shotgun sequencing of total extracted community DNA can be used to link taxonomic information to function in an environmental sample (Wooley et al., 2010; Thomas et al., 2012). Gene characterization in a specific habitat, such as those needed for pathogenicity, antibiotic resistance, or hydrocarbon degradation, indicate what functions or ecosystem services may be possible within that environment. This method may also be used to identify specific taxa within a community. Accurate metagenomic characterization requires very deep sequencing,

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especially in highly complex matrices such as soil, and a solid reference database; it is not always adequate as a stand-alone technique to assess the diversity of an environmental sample (Fuhrman, 2012). Still, the method has potential in identifying organisms and genes with putative biotechnological or medical use, and its applicability and accuracy is constantly improving as databases become more robust and computational difficulties are smoothed out (Knight et al., 2012). Mitochondrial metagenomics is a growing field that provides unique opportunities in food safety, enabling source tracking of fecal contamination in the environment and in irrigation water sources (Kapoor et al., 2014; Crampton-Platt et al., 2016). By looking at mammalian species-specific mitochondrial markers, fecal contamination can be traced to potential sources (human, bovine, porcine, poultry, etc.) and linked to possible risk factors. Insights learned from metagenomic characterization of contaminated foods may lead to improvements in culture-based pathogen detection pipelines ( Jarvis et al., 2015; Ottesen et al., 2016a; Pettengill et al., 2012). Furthermore, pathogen detection directly from environmental samples and food matrices with little to no culturing component may be possible in the future using metagenomics (Forbes et al., 2017; Miller et al., 2013).

5.4 Metatranscriptomics/Metaproteomics Metatranscriptomics examines the activity of microbial communities, often in response to environmental changes at a highly responsive timescale. Total messenger RNA (mRNA) is isolated from the whole community, sequenced, and a profile of transcribed genes identified through database searches (Carvalhais et al., 2012). This method is challenging due to mRNA being unstable and difficult to extract, and due to the incomplete nature of available databases. Furthermore, the disconnect between half-lives of proteins and mRNA molecules, coupled with the wide variation in protein half-lives, means that abundance of mRNA transcripts may not correspond to protein abundance (Moran et al., 2013). Protein abundance and diversity may be directly characterized by metaproteomics, another growing field that offers the opportunity to examine the functional diversity of complex environmental samples (Wilmes and Bond, 2006). This method is based on mass spectrometry rather than nucleotide sequencing and may be combined with metagenomics to link structure to function (Wilmes and Bond, 2006). There are many challenges to this method, including extraction inefficiency and identification difficulties (Wilmes and Bond, 2006), but it has potential to help fill in the broader picture of microbial life in the phyllosphere and rhizosphere, especially when combined with other techniques (Delmotte et al., 2009).

5.5 Challenges Associated With Next-Generation Sequencing Methods With all of these methods, the large volume of data produced presents challenges in terms of establishing computational infrastructure and standardizing data management for easier sharing across studies (Wooley et al., 2010). The technology for these methods is swiftly changing, and standard protocols for microbial community studies from sample collection through data interpretation are not yet established (Mizrahi-Man et al., 2013). Preparation steps, including extraction techniques and the use of PCR, may introduce bias within samples that is challenging to identify and control for (Aird et al., 2011; van Dijk et al., 2014;

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Wilmes and Bond, 2006). Errors in sequence generation on the machine itself (Illumina, 454, etc.) can lead to erroneous OTU assignments, potentially inflating diversity estimates and providing a skewed picture of the rare biosphere (Reeder and Knight, 2009), potentially masking treatment effects (Gomez-Alvarez et al., 2009). Quality filtering methods are essential for removing theses sources of error (Bokulich et al., 2013), and care must be taken to prevent introduction of any additional bias during the data analysis pipeline (Ross et al., 2013). To get a clear picture of the structure and function within a given microbial community and reduce artifacts introduced by various methods, tools can be combined to answer a multitude of questions (Rastogi et al., 2013). Furthermore, results from these characterizations can be correlated with specific biological, chemical, temporal, and physical factors to better elucidate causal effects (Raes et al., 2011). Although analysis of these large and complex datasets can be challenging and requires specialized training, more user-friendly interfaces are becoming increasingly common, making it easier for investigators without strong bioinformatics backgrounds to at least partially analyze their own data (McMurdie and Holmes, 2015; Afgan et al., 2016; Chelaru et al., 2014; Caporaso et al., 2010; Vazquez-Baeza et al., 2017).

5.6 Culture-Based and Alternative Molecular Methods Sequencing, although growing in accessibility and popularity, is not always the best choice for hypothesis testing. Other technologies may be more appropriate as a first step to look for broad-scale differences between treatments, followed by targeted sequencing where greater resolution is required. These technologies may also be useful as a supplement to sequencing data, providing another lens through which to assess microbial diversity and activity within environmental samples. The Biolog ecoplate tests general metabolic activity, measuring the use of between 31 and 95 carbon-based substrates within environmental samples (Stefanowicz, 2006). Although this method provides information only about the overall activity of culturable microorganisms in a sample, it can be helpful for studies that seek to determine the effects of soil amendments or environmental disturbances on broad scale metabolic activity. Phospholipid fatty acid analysis is an affordable, reproducible, straightforward technique that can be used to characterize the diversity of microbial communities based on cell membrane composition (Ruess and Chamberlain, 2010). Quantitative real-time PCR (qPCR) can be used to identify the presence and abundance of certain genes of interest in the environment (Orr et al., 2011). When the main objective of a study is to investigate the role of microbial communities in specific processes, such as nitrogen fixation, qPCR may be the most efficient way to address the question. Denaturing gel gradient electrophoresis, automatic ribosomal intergenic spacer analysis, and terminal restriction fragment length polymorphism (t-RFLP) are examples of fingerprinting methods that may be used when sequencing is inaccessible or as a preliminary step to justify the enhanced resolution required by sequencing. Although they do not provide a comprehensive estimation of the total species richness of a niche, culturing methods can be useful when investigating specific plant-microbe interactions; culturing is still the easiest way to obtain large amounts of DNA from a clonal population for functional studies. P. syringae and Methylobacterium, for example, have been extensively studied as model epiphytes, providing valuable information about mobility, attachment, biofilm

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formation, substrate use, and pathogenicity. Results from experiments using these bacteria can be helpful in extrapolating behavior of other microorganisms in the phyllosphere and rhizosphere (Gourion et al., 2006; Knief et al., 2010; Chen and Beattie, 2008; Freeman et al., 2010; Hirano et al., 1999; Leveau and Lindow, 2001). Culture methods may also be used to isolate specific plant or human pathogens; once isolated, these cultures can be used for pathogenicity or inoculation studies, or isolates may be sequenced for enhanced understanding of specific genetic adaptations to the plant environment.

6 HARNESSING THE POWER OF MICROBES IN AGRICULTURE Just as pharmaceutical companies are investigating the power of microbes as alternative medicine to treat human disease (Reardon, 2014), interest in manipulating plant-associated microbial communities is growing in terms of agricultural biotechnology (Berg, 2009). Microbial dynamics of the rhizosphere have been studied much more extensively compared to those of the phyllosphere, and as a result, rhizosphere research has moved forward more substantially from description to application in the field (Wu et al., 2008; Termorshuizen et al., 2006; Liu et al., 2007; Bossio et al., 1998). This robust characterization has led to a greater understanding of how microbes can be used to enhance agricultural production and environmental sustainability (Berg, 2009; Bakker et al., 2012; Chaparro et al., 2012). Further research into the basic dynamics of the phyllosphere in response to varied agricultural practices will lead to similar advances in practical application.

6.1 Biological Control Bacterial and fungal biocontrol agents are becoming an important part of agricultural management, and demand for them is steadily increasing (Berg, 2009). The natural tendency of some microbes to enhance plant responses to abiotic and biotic stresses may be exploited by isolating and applying these beneficial microbes in higher-than-endemic concentrations in the field. Some microbes have been investigated as potential biocontrol agents for foodborne pathogen infection (Allard et al., 2014), however biocontrol organisms used to control plant pathogens are much more widely studied (Hermosa et al., 2012; Berendsen et al., 2012). Microbial biocontrol agents use diverse mechanisms to suppress the growth of pathogens and promote plant growth. Often direct competition for space and nutrients with the target pathogen is a factor, although this is difficult to measure, as the advantage conferred by their strategy will likely give them a growth advantage, whereas other species are impaired. Some microbes release antibiotics that harm or kill pathogenic organisms in a process called antibiosis (Arora et al., 2012; Mukherjee et al., 2012). For example, Pantoea agglomerans acts through antibiosis to combat fire blight in apple blossoms, targeting the causative agent Erwinia amylovora, with a specific and unique antibiotic (Pusey et al., 2011). Other biocontrol microbes break down toxins released by the pathogenic microbes or damage the pathogens directly. Foliar application of Paenibacillus lentimorbus B-30488 has been shown to reduce the incidence of early blight disease in tomatoes by 45% (Khan et al., 2012). Khan et al. (2012)

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concluded that a combination of factors is responsible for this reduction, including the release of hydrolytic enzymes that degrade fungal hyphae of the blight-causing pathogen Alternaria solani. In addition to direct interactions between biocontrol organisms and pathogens, some rhizosphere inhabitants, known as PGPR, boost host plants’ defenses by priming them for stronger and faster defense responses while promoting growth. These microbes jumpstart the plant immune system, causing changes in jasmonic acid and ethylene signaling pathways tied to plant defense and induce an increase in the synthesis of pathogenesis-related (PR) proteins (Shoresh et al., 2010). Several strains within the genus Paenibacillus have shown promise as biological control agents and/or PGPR, enhancing plant defense against pathogens through competition, antibiosis, and ISR (von der Weid et al., 2003; Anandaraj et al., 2009; McSpadden Gardener, 2004; Allard et al., 2014). Biological control agents, like all plant-associated microbes, have complex relationships with host plants and other environmental microorganisms, making their activity variable and at times unpredictable (Harman, 2000). Nextgeneration sequencing technologies provide an opportunity to elucidate the interplay between these factors in an effort to discover and implement more effective biocontrol agents (Droby et al., 2016). Network analysis of microbiome data has been demonstrated as an effective tool for identification of biological control agents (Poudel et al., 2016), and the future is bright for the development of agricultural biocontrol approaches from microbiome datasets (Berg et al., 2017).

6.2 Disease-Suppressive Soils Central to plant pathology is the disease triangle, a model showing the interactions between host, pathogen, and environment that lead to disease (Scholthof, 2007). For disease to occur, conditions for all of these components must be optimal. Disease-suppressive soils manipulate the environment, reducing conduciveness to disease despite the presence of a pathogen and susceptible host (Hadar and Papadopoulou, 2012). Once established, disease suppressiveness persists in the long term, even with repeated reintroduction of a pathogen (Cook et al., 1995). Composts with suppressive qualities include vermicompost, green waste, straw, animal manure, and soil amendments used in organic agriculture. Sterilization studies have shown that the disease-suppressive qualities of compost can be attributed primarily to microbial communities (Liu et al., 2007). Microbes with known pathogen-suppressing potential, such as members of Xylariaceae, Lactobacillaceae, and Bacillus, are more abundant in disease-suppressive soils than nonsuppressive soils (Wu et al., 2008; Klein et al., 2013; Penton et al., 2014; Mendes et al., 2011). Microbial communities associated with disease suppression may act through general or specific mechanisms. The general suppression effect is attributed to competition for nutrients and/or space as well as release of antibiotic compounds and toxins carried out by a large metabolically active community (Hadar and Papadopoulou, 2012). Specific interactions between compost-dwelling microbes and pathogens, including parasitism and predation, also lead to disease suppression. Suppressive composts may enhance plant defense through ISR (Yogev et al., 2010; Zhang et al., 1998) and supporting plant growth and general health. In contrast to the application of a single biocontrol organism, suppressive composts contain a diverse community of microorganisms that may combine several of the strategies described to achieve C. RECOMMENDATIONS AND INTERVENTION FOR IMPROVING SAFETY

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disease suppression. The effectiveness of disease-suppressive soils may be enhanced by inoculation with biocontrol agents such as Trichoderma hamatum or Bacillus subtilis (Nakasaki et al., 1998; Kwok et al., 1987; Hadar and Papadopoulou, 2012). Although disease suppression in amended soils has been observed in many different contexts, it is not easy to reproduce in the field (Bonanomi et al., 2010; Termorshuizen et al., 2006). Due to the complexity and specificity of plant-pathogen-environment interactions, use of disease-suppressive soils will be most effective if tailored specifically based on host, pathogen, and environment in including consideration of interplay with the plant microbiome. With these concerns addressed, disease-suppressive composts have potential as an environmentally friendly, safe, and effective approach to disease control for organic agriculture.

6.3 Plant Growth Promotion As microbes associated with plants frequently exhibit multiple plant growth and healthpromoting characteristics, a more holistic approach to the use of microorganisms in agriculture could be adopted with the use of “plant probiotics” (Berlec, 2012). In the same way that “rhizoengineering” has been suggested, “phylloengineering” could be utilized at the interface between the environment and the above-ground plant surface. Using this approach, a plant’s microbiome would be considered as significantly as the plant’s own genotype and phenotype. Microorganisms may be specifically formulated and applied to the field due to their growth-promoting effects, decreasing nutrient-deficiency-based stress and increasing crop yield. Alternatively, the added benefits associated with biocontrol agents and diseasesuppressive soil application may be explored; in addition to disease suppression these often support enhanced nutrient uptake by host plants (Berg, 2009). In fields with low nitrogen content, seeds treated with fungal biocontrol Trichoderma strain T-22 reached their yield plateau with 38% less supplemental nitrogen than nontreated seeds (Harman, 2000). Many rhizosphere microbes release organic acids into the soil, increasing the solubility and the availability of several additional micro- and macronutrients to host plants. Potassium, a macronutrient instrumental for stomatal closure and establishment of osmotic potentials in plants, can be difficult for plants to access, and stress conditions reduce its uptake. Plant-associated microbes in the rhizosphere, such as Trichoderma, have shown an ability to increase potassium content of plants (Shoresh et al., 2010). Some soil-dwelling biocontrol microbes oxidize sulfate and solubilize iron, activities that benefit plant growth while simultaneously removing nutrients from the soil that could be used by damaging plant pathogens (Berg, 2009). Strains of the bacteria Pseudomonas secrete siderophores into the rhizosphere, solubilizing iron so that the plant increases its iron uptake, and plant pathogens in the soil have reduced iron access (Harman, 2000). Due to these effects, the introduction of single biological control agents or the use of suppressive soils could contribute to plant growth promotion in addition to pathogen control.

6.4 Environmental Health The potential for phyllosphere microorganisms to reduce the negative environmental impacts of agricultural production is an exciting avenue for future research. The use of plant C. RECOMMENDATIONS AND INTERVENTION FOR IMPROVING SAFETY

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growth promoting microorganisms could lead to reduced use of synthetic fertilizers, which in turn would lead to decreased runoff and eutrophication of waterways. Harnessing the ability of microorganisms to stimulate plant defense and antagonize pathogens could lead to reduced use of pesticides and an associated decrease in human health risks associated with exposure to these chemicals. Perhaps microbial communities could even be employed to enhance the medicinal properties or nutritional content of plants; research has shown that phytotherapeutic compounds attributed to medicinal plants are often in fact produced by their associated microbial communities (Koeberl et al., 2013). Furthermore, plant-breeding efforts could focus on those plants that actively recruit microbes efficient in phytoremediation (Ali et al., 2012), helping to alleviate the environmental effects of pollution.

6.5 Food Safety Microbial characterization of plants commonly implicated in food safety incidents may assist with the prevention of foodborne outbreaks, as well as increase the speed of contamination traceback in the event of a foodborne illness outbreak. Characterization of microbial communities associated with plants naturally contaminated with enteric pathogens will provide insights into the microbial ecology and dynamics that allow for the introduction and survival of these pathogens. Shifts in microbial communities in response to external factors may signal an interval during which new taxa can become introduced in an established microbiome. Indicator species may be identified as precursors to establishment of human pathogens such as S. enterica or plant pathogens such as Ralstonia solanacearum. If these indicator species are present in larger amounts than the contaminant or if they are easier to detect in field labs, they could be valuable resources for prevention and detection of foodborne disease. Examination of the interaction between plant genotypes and their environments could be helpful in establishing best practices for agriculture to reduce risks of foodborne pathogen colonization. Tomatoes have frequently been associated with Salmonella outbreaks, and at least twice in the past 11 years the outbreak strain has been traced back to on-site irrigation ponds (Greene et al., 2008). California is another major tomato-producing state, and yet out of the 17 multistate outbreaks of Salmonella in tomatoes in the United States over the past 13 years, only one originated in California (Ottesen et al., 2013). Analysis of the microbial communities across these geographical areas may provide clues as to the biological factors that cause the disparity between east coast and west coast food safety risks for specific human pathogen-plant commodity pairs. Another potential benefit of characterization of microbes associated with at-risk food crops is the discovery of biocontrol organisms. If some organisms are highly enriched in healthy, disease-free plants and deficient in infected plants, these could be investigated for commercial potential as microbial inoculants to encourage plant growth and prevent pathogen colonization. Biocontrols for plant pathogens do not appear to have lasting effects on phyllosphere and rhizosphere microbial communities, and could represent an environmentally sound approach to foodborne pathogen control in the field (Perazzolli et al., 2014; Sylla et al., 2013).

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7 CONCLUSIONS Plants host a large diversity of microbial species in both the rhizosphere and phyllosphere; these influence nutrient uptake, growth, and response to biotic and abiotic stresses in diverse ways. The intricacy of plant-microbe interactions makes understanding the mechanisms by which plants may become colonized by, and maintain populations of, pathogenic microorganisms complex. Molecular characterization of plant-associated microbial communities provides opportunities to identify risk factors for pathogen infection, discover indicator organisms that can act as a “canary in the coal mine” before pathogen infection, and investigate how choices in agricultural management may influence plant-associated microbial communities, as well as human, plant, and environmental health. Next-generation sequencing technology, which has become increasingly affordable and accurate, has allowed the field of phyllosphere ecology to grow, but there are still many basic questions that need to be answered for the field to move forward. An enhanced understanding of the balance between plants, their associated microorganisms, and the environment will lead to a richer understanding of the influence of agricultural management choices, potentially leading to innovations in produce safety, plant pathogen management, and sustainability. In today’s world, agriculture faces formidable challenges. Global climate change may lead to increased dispersal of pathogens, plant stress, and crop loss (Scholthof, 2007). The world population continues to grow, as does world hunger and demands on potable water and fresh produce. Foodborne disease outbreaks linked to fresh produce are common worldwide. Once a basic understanding of plant-associated microbial community dynamics is established, manipulation of microbial communities to maximize plant growth, defense against human and plant pathogens, and nutrient uptake efficiency may be possible, allowing more efficient use of limited resources, reduced side effects of agricultural inputs, and enhanced produce safety.

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Vorholt, J.A., 2012. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10 (12), 828–840. Wei, C.I., Huang, T.S., Kim, J.M., Lin, W.F., Tamplin, M.L., Bartz, J.A., 1995. Growth and survival of salmonellamontevideo on tomatoes and disinfection with chlorinated water. J. Food Prot. 58 (8), 829–836. Whipps, J.M., Hand, P., Pink, D., Bending, G.D., 2008. Phyllosphere microbiology with special reference to diversity and plant genotype. J. Appl. Microbiol. 105 (6), 1744–1755. Williams, P.R.D., Hammitt, J.K., 2001. Perceived risks of conventional and organic produce: pesticides, pathogens, and natural toxins. Risk Anal. 21 (2), 319–330. Wilmes, P., Bond, P., 2006. Metaproteomics: studying the functional gene expression in microbial ecosystems. Trends Microbiol. 14 (2), 92–97. Winfree, R., Williams, N.M., Gaines, H., Ascher, J.S., Kremen, C., 2008. Wild bee pollinators provide the majority of crop visitation across land-use gradients in New Jersey and Pennsylvania, USA. J. Appl. Ecol. 45 (3), 793–802. Wink, M., 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64 (1), 3–19. Wooley, J.C., Godzik, A., Friedberg, I., 2010. A primer on metagenomics. PLoS Comput. Biol. 6(2), e1000667. Wu, T., Chellemi, D.O., Graham, J.H., Martin, K.J., Rosskopf, E.N., 2008. Comparison of soil bacterial communities under diverse agricultural land management and crop production practices. Microb. Ecol. 55 (2), 293–310. Wu, J., Long, S.C., Das, D., Dorner, S.M., 2011. Are microbial indicators and pathogens correlated? A statistical analysis of 40 years of research. J. Water Health 9 (2), 265–278. Xu, A., Buchanan, R.L., Micallef, S.A., 2016. Impact of mulches and growing season on indicator bacteria survival during lettuce cultivation. Int. J. Food Microbiol. 224, 28–39. Yogev, A., Raviv, M., Hadar, Y., Cohen, R., Wolf, S., Gil, L., Katan, J., 2010. Induced resistance as a putative component of compost suppressiveness. Biol. Control 54 (1), 46–51. Yu, X.L., Lund, S.P., Scott, R.A., Greenwald, J.W., Records, A.H., Nettleton, D., Lindow, S.E., Gross, D.C., Beattie, G.A., 2013. Transcriptional responses of Pseudomonas syringae to growth in epiphytic versus apoplastic leaf sites. Proc. Natl. Acad. Sci. U. S. A. 110 (5), E425–E434. Zamioudis, C., Pieterse, C.M., 2012. Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25 (2), 139–150. Zarraonaindia, I., Owens, S.M., Weisenhorn, P., West, K., Hampton-Marcell, J., Lax, S., Bokulich, N.A., Mills, D.A., Martin, G., Taghavi, S., van der Lelie, D., Gilbert, J.A., 2015. The soil microbiome influences grapevine-associated microbiota. MBio. 6 (2). e02527-14. Zhang, W., Han, D.Y., Dick, W.A., Davis, K.R., Hoitink, H.A.J., 1998. Compost and compost water extract-induced systemic acquired resistance in cucumber and arabidopsis. Phytopathology 88 (5), 450–455. Zheng, J., Allard, S., Reynolds, S., Millner, P., Arce, G., Blodgett, R.J., Brown, E.W., 2013. Colonization and internalization of Salmonella enterica in tomato plants. Appl. Environ. Microbiol. 79 (8), 2494–2502.

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Control Strategies for Postharvest Microbiological Safety of Produce During Processing, Marketing, and Quality Measures Luis J. Bastarrachea*, Solmaz Alborzi†, Rohan V. Tikekar† *

Department of Nutrition, Dietetics and Food Sciences, Utah State University, Logan, UT, United States †Department of Nutrition and Food Science, University of Maryland, College Park, MD, United States

O U T L I N E 1 Introduction 1.1 Postharvest Washing and Handling of Organic Produce

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3 Emerging Sanitizers 3.1 Organic Acids 3.2 Electrolyzed Water

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1 INTRODUCTION One of the most important food safety challenges is contamination of fresh produce, which has caused numerous foodborne outbreaks and the greatest number of illnesses per outbreak in recent years (Hussain and Gooneratne, 2017). Foodborne outbreaks not only affect public

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health but also can represent a heavy impact on the economics of the food industry (Hussain and Dawson, 2013). The hazards found on fresh produce can be classified into physical, chemical, and biological. Physical hazards can be caused by contamination of dust, sand, wood, and metal pieces. Chemical hazards can be caused by contamination with chemicals, such as those found in packaging, or with pesticides. Biological hazards can be caused by pathogenic bacteria such as Escherichia coli, Salmonella, Listeria monocytogenes, or other pathogenic bacteria found in soil (Mahajan et al., 2014; Hussain and Gooneratne, 2017). Growth of antimicrobial resistant bacteria strains in fresh produce is another challenge to food scientists and food processors, which makes it important to minimize their occurrence in fresh produce by knowing their pathways through contamination (Hussain and Gooneratne, 2017). Consuming fruits and vegetables is considered to be a requirement of a balanced diet to help achieve and maintain a healthy body weight. Therefore it is important to prevent microbial contamination of fresh produce at all steps from farm to table, which includes growing, harvesting, packaging, transportation, distribution, and home processing (Qadri et al., 2015). The greatest risk takes place when unwashed vegetables and fruits are used, which makes washing an imperative step (Hussain and Gooneratne, 2017). Washing with water is an essential step in fresh and fresh-cut produce processing to remove the debris and soils, maintaining quality and shelf life of the final products (Simons, 2000). Because washing with water alone could play a major role as a mediator for pathogenic cross-contamination, addition of sanitizers to water is by far the most effective preventive approach to decrease the microbial population. Chlorine is the most widely utilized sanitizer in the fresh produce industry due to its low cost and rapid bacterial inactivation at relatively low doses (Toma´s-Callejas et al., 2012; Gomez-Lopez and Lannoo, 2014). However, the efficacy of chlorine can also be substantially affected by various physicochemical factors (Toma´sCallejas et al., 2012; Gomez-Lopez and Lannoo, 2014). For example, the efficiency of chlorine as a sanitizer for fresh produce could be affected by increased organic load that reduces the concentration of free chlorine (Fuzawa et al., 2016). There are several other choices, such as ozone or other gas treatments, UV-irradiation, organic acids, essential oils, and other treatments, such as steaming or pasteurization. Each of these methods has some advantages and disadvantages (Johannessen, 2007).

1.1 Postharvest Washing and Handling of Organic Produce Postharvest handling, cleaning, and storage for both conventional and organic products include the same operations. However, the cleaning agents used may differ (Suslow, 2000). The most important way to maintain postharvest quality is removing field heat as rapidly as possible in postharvest storage, because heat can accelerate the rate of respiration, which leads to quality loss. Therefore proper cooling protects quality and extends both the sensory and nutritional attributes of produce. Unloading commodities from harvest bins, washing, and precooling are other postharvest issues, which also need to be evaluated for adherence to organic standards (Suslow, 2000). In general, most vegetables and fruits are chilled after harvest to lower their respiration rates. Among the different techniques used to remove field heat from fruits and vegetables, “icing” is probably most frequently used; other options include cooling down by quick transport to a properly sized refrigeration unit and some are hydrocooled (Bubl, 2007).

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To clean the produce, liquid sodium hypochlorite is the most common agent for both organic and conventional operations. However, in the case of organic products, the residual chlorine level should not exceed 4 ppm. The optimum antimicrobial activity of chlorine can be obtained at a pH level of 6.5–7.5 (Suslow, 2000). During the washing process of fresh produce, chlorine dissolves in water to form HClO, an efficient oxidizer for pathogen inactivation. Maintaining a stable HClO form during the washing process can be a challenge because HClO can dissociate into hypochlorite ions (OCl ) at high pH or into Cl2 at low pH. Soil and debris in the washing process can increase organic load, which can reduce the amount of available chlorine. If the level of chlorine is excessive to counteract the organic load in the washing water, toxic byproducts such as trihalomethanes and haloacetic acids can be formed (Deborde and von Gunten, 2008; Banach et al., 2015). To adjust the pH, products must be chosen from natural sources such as citric acid, sodium bicarbonate, or acetic acid. But there are some limitations in adding hypochlorite to clear, clean water as a disinfectant (Suslow, 2000). Acetic acid, ethyl alcohol, ammonium sanitizers, hydrogen peroxide, ozone, and peroxyacetic acid are other sanitizers that can be used in the case of organic fresh produce (Suslow, 2000). Coating of fresh produce is an additional step that diminishes water loss during handling and storage, and also adds sheen to the produce. Waxes are generally not used on organic fruits, although natural waxes such as carnauba or wood-extracted wax are allowed. Products coated with approved wax must be included on the label (WSU, 2011). The next important step to protect fresh produce from bruising and other injuries is packing. An effective shipping container must be strong to tolerate the weight of stacked containers during shipping and at the same time provide adequate ventilation for cooling. Some fresh produce such as tomato and summer squash should be dried before packing to reduce decay. Other produce such as leafy vegetables can be packed wet, but they have to be quickly cooled with sanitized water. There are several options for shipping containers for organic growers. Dry vegetables can be packed into corrugated fiberboard cartons to remove any surface moisture (Sargent and Treadwell, 2009). Finally, the containers should be transferred to a storage area. In the storage area, the amount of field heat must be removed and the temperature maintained. It has been shown that for every 20°F reduction in pulp temperature, the shelf life increases two- or three-fold. It should be noted that temperature fluctuations quickly reduce quality and promotes decay. Therefore after reduction of temperature, the crop must be kept cool (Sargent and Treadwell, 2009). At the end, organic rousts could be blended with nonorganic products, although the mixed products cannot be sold as 100% organic product anymore. Based on this scenario, four categories of organic products can exist: 100% organic, 95% organic, made with organic ingredients (70%–95% organic), and nonorganic (>70% nonorganic) (Perkins-Veazie and Lester, 2008).

2 DISINFECTANTS ALLOWED FOR ORGANIC PRODUCE According to the National Organic Program established by the United States Department of Agriculture (USDA), certain categories of chemical sanitizers and disinfectants can be used as long as it is demonstrated that, during the different operations involved in the crop’s production process, there is no cross-contamination or direct contact between these substances

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and the produce (CFR, 2000). Additionally, it should be demonstrated that these chemical agents do not contaminate the soil and the water used for cultivation and irrigation. The allowed substances relevant for food processing facilities include alcohols (ethanol and isopropanol), chlorine materials (calcium hypochlorite, chlorine dioxide, and sodium hypochlorite), copper sulfate, hydrogen peroxide, ozone gas, and peracetic acid. In the following paragraphs, information will be provided on the mode of action, antimicrobial power, and general limitations of these disinfectants.

2.1 Alcohols Alcohols represent a group of solvents that possess affinity toward a wide variety of organic compounds. For this reason, they are able to inactivate microorganisms through the solubilization of proteins and lipids, which constitute the building blocks of enzymes and cell membrane components (Martı´nez, 2009). More specifically, alcohols’ antimicrobial effect is a result of cell membrane disruption (by affecting fatty acid composition), inhibition of protein synthesis, change of cytoplasmic pH, and alteration of membrane potential (Fried and Novick, 1973; Terracciano and Kashket, 1986; Chiou et al., 2004; Silveira et al., 2004; Cincarova et al., 2016). Ethanol and isopropanol are the most widely used alcohols as disinfectants. Normally, alcohol aqueous solutions are used at a 50%–70% volumetric concentration (Todd et al., 2010). Previous works have demonstrated the effectiveness of alcohols to reduce the microbial load from food contact surfaces. In a recent study, in >4 logarithmic cycles (>99.99%), alcohol-based sanitizers were able to reduce the population of gram-positive (Staphylococcus aureus) and gram-negative (E. coli O157:H7) bacteria from contaminated stainless steel. However, alcohols have some limitations. Given their nature as solvents, residual organic matter may reduce or deplete their antimicrobial effect, and they may not be effective against biofilms (Martı´nez, 2009). Some studies have found that, when exposed to ethanol or isopropanol, some species of Escherichia and Salmonella experience oxidative stress, resulting in the production of neutralizing enzymes, which function to prevent cell damage and repair any detrimental effects on the genetic material (Demple and Harrison, 1994). In addition, sublethal levels of ethanol are able to induce biofilm formation, as it was found in a recent study in which concentrations of ethanol as low as 1.25%–2.50% were able to induce S. aureus biofilm formation (Cincarova et al., 2016).

2.2 Chlorine Materials Chlorine materials include a variety of chlorine-based compounds. The most widely employed are liquid chlorine, hypochlorites, organic and inorganic chloramines, and chlorine dioxide. They have shown to be biocidal when exposed to vegetative cells, yeasts, molds, spores, and viruses. The antimicrobial activity of chlorine materials is based on their ability to denature proteins (in particular with an oxidizing effect on the sulfhydryl groups), alter membrane activities (such as oxidative phosphorylation), interfere in protein synthesis, degrade genetic material (depleting cell reproduction), and disrupt metabolic functions (Martı´nez, 2009; Ray and Bhunia, 2014). The maximum level of free chlorine allowed for disinfection in food processing facilities is 200 ppm (Rutala and Weber, 2008). However, in >4

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logarithmic cycles (>99.99%), concentrations as low as 8 ppm of free chlorine are able to reduce the population of vegetative cells within minutes of exposure in the absence of organic matter (Bastarrachea et al., 2013). Some studies have reported >5 logarithmic reductions (>99.999%) within 30 s of exposure with concentrations as low as 0.5–1.0 ppm (Luo et al., 2011; Van Haute et al., 2013; Shen et al., 2013). Even though chlorine-based materials represent the most widely used type of sanitizer (due to their availability, low cost, and ease of use), they also exhibit some limitations. Given their ability to react with organic matter, its presence can substantially reduce (or completely eliminate) their antimicrobial activity (Martı´nez, 2009; Ray and Bhunia, 2014; Zhou et al., 2015; Bastarrachea and Goddard, 2016). Their effectiveness is also limited by level of temperature, pH, and salinity (Ray and Bhunia, 2014). In addition, some studies have reported that resistance toward chlorine may be developed by microorganisms at different growth phases (Cherchi and Gu, 2011) and by biofilms (Ryu and Beuchat, 2005). 2.2.1 Copper Sulphate Copper is a micronutrient necessary for the survival of microorganisms. It serves as a cofactor of enzymes and proteins. If its concentration is high, it may alter cell membrane integrity, denature proteins, and promote the formation of free radicals (Meireles et al., 2016). Copper sulphate has demonstrated to be effective against algae due to its ability to aggregate genetic material and disrupt chloroplasts (Qian et al., 2010), and for this reason it has been applied in the seafood industries (Gr€ aslund and Bengtsson, 2001) and in water treatment (Halpern et al., 1999). It has also been demonstrated to be effective against bacteria (Flemming and Trevors, 1989; Prasad et al., 1993). The effectiveness of copper sulfate can be substantially lower compared to other disinfectants, and its biocidal effect can also be diminished (if not depleted) in the presence of organic matter. In one study conducted to evaluate the effectiveness of copper sulfate as a disinfectant to reduce the coliform population from sewage sludge, 2–3 logarithmic reductions were obtained after 24 h of exposure with copper sulfate concentrations in the 30–40 mg/g range. In contrast, when the concentrations were low (1–3 mg/g), the coliform population increased. In another study, copper sulphate was challenged with other disinfectants against different pathogenic bacteria frequently found in fish (Kim et al., 2008). In the cited work, even at the highest concentrations tested (3200 ppm), copper sulphate couldn’t reduce in >90% the populations of Vibrio, Edwardsiella tarda, Streptococcus and Staphylococcus. These findings may explain why this compound has been used as a supplement for animal feed for pathogen control in animals for human consumption (Aarestrup and Hasman, 2004). An additional problem this compound exhibits is its toxicity toward aquatic life (St-Laurent et al., 1992; Gr€ aslund and Bengtsson, 2001).

2.3 Hydrogen Peroxide Hydrogen peroxide is an antimicrobial agent of natural origin, able to inactivate microorganisms (bacteria, molds, and viruses) by oxidizing essential cell components such as lipids, proteins, and genetic material. It is the product of a defense mechanism exhibited by lactic acid bacteria, which are able to synthesize hydrogen peroxide inside the cell and release it

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to its surroundings (Martı´nez, 2009; Ray and Bhunia, 2014). It has been used in raw milk and raw liquid eggs at levels of 25 ppm to inhibit pathogens and spoilage microorganisms (Ray and Bhunia, 2014). The main advantages hydrogen peroxide offers relate to its “generally recognized as safe” status (GRAS) and to its small impact to the environment by converting into oxygen and water through the action of catalases. Its main limitations deal with its low stability and slow bactericidal effect (Meireles et al., 2016). This may be the main reason behind the small levels of inactivation achieved when it is applied to produce at high concentrations. In one study, 1–2 logarithmic reductions occurred against E. coli O157:H7 in baby spinach at a concentration of 30,000 ppm within 5 min (Huang et al., 2012). In another study, up to 3.5 logarithmic reductions occurred against L. monocytogenes on melon after 2 min of exposure to 50,000 ppm (Ukuku and Fett, 2002). In addition to the high dosage required to achieve an antimicrobial effect, some bacteria (from Bacillus and Pseudomonas species) have been shown to develop resistance toward hydrogen peroxide through antioxidant mechanisms (Hartford and Dowds, 1994; Elkins et al., 1999; Martı´nez, 2009).

2.4 Ozone Ozone is a potent oxidizing agent. Subjecting molecular oxygen to an electric current can form ozone. It exhibits good solubility in water, and concentrations as low as 1–5 ppm are enough to impart an antimicrobial effect. However, in the gaseous form, its antimicrobial effect can be diminished substantially due to its interactions with water vapor (Clark, 2004; Meireles et al., 2016). Probably the main advantage of ozone relates to its ability to impart an antimicrobial effect without generating toxic residues, as it decomposes into oxygen; compared to chlorine compounds, it is less affected by the presence of organic matter (Clark, 2004). However, the levels of inactivation that can be reached with ozone can in some cases be substantially lower than those provided by chlorine materials. In one study, 1–2 logarithmic reductions of Shigella sonnei in lettuce were obtained when it was applied dissolved in water at a concentration of 5 ppm (Selma et al., 2007). Comparable levels of inactivation were obtained in another study in which ozone in the gaseous form was applied onto spinach leaves contaminated with E. coli O157:H7 (Vurma et al., 2009). In a different study, ozone dissolved in water at 5 ppm was able to reduce the microbial load of E. coli O157:H7 and L. monocytogenes in lettuce by 1.09 and 0.94 logarithmic cycles, respectively (Yuk et al., 2006). In another work, involving the same microorganisms, it was possible to reduce the E. coli O157:H7 and L. monocytogenes populations in produce by >5 logarithmic cycles using aqueous solutions with only 3 ppm of ozone (Rodgers et al., 2004). Similarly, in a previous work, >7 logarithmic cycles in reduction were obtained by applying aqueous solutions with 5.9 ppm of ozone on stainless steel contaminated with Bacillus subtilis (Khadre and Yousef, 2001). In addition to the wide variability in the antimicrobial efficacy of ozone (which seems to be dictated by the type of food and microorganism), it possesses other disadvantages such as the fact that it has to be generated where it is going to be used (due to its lack of stability), its detrimental effect on the organoleptic properties of produce, and its corrosive behavior on equipment (Meireles et al., 2016).

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2.5 Peracetic Acid Peracetic acid results from the combination of acetic acid and hydrogen peroxide (Kitis, 2004). It possesses a high oxidizing potential that has shown biocidal efficacy against bacteria, molds, and viruses (Martı´n-Espada et al., 2014). It is an environmentally friendly compound that degrades into acetic acid and active oxygen (Meireles et al., 2016). An additional advantage of peracetic acid is the low concentrations required to impart an antimicrobial effect compared to hydrogen peroxide. However, it is also unstable compared to hydrogen peroxide, and its stability reduces with decreasing concentrations in aqueous solutions, which has a direct impact on its antimicrobial effectiveness as concentrations higher than 15% (w/w) represent a hazard of reactivity and explosiveness (Kitis, 2004). One relevant feature peracetic acid has shown is its ability to keep its biocidal efficacy even in the presence of organic matter. In a recent study (Davidson et al., 2017), peracetic acid at 50 ppm was challenged at different levels of organic matter (0%, 2.5%, 5%, or 10% w/v) against E. coli O157:H7 on lettuce, and it was found that the presence of organic matter didn’t have a statistically significant impact on microbial efficacy, which could be >5 logarithmic cycles. Another work (Baert et al., 2009) is in agreement with this interpretation, in which sodium hypochlorite and peracetic acid were challenged against E. coli O157:H7 and L. monocytogenes inoculated in iceberg lettuce. In the mentioned study, the presence of organic matter affected the antimicrobial effect of sodium hypochlorite (at concentrations of 20 and 200 ppm) but didn’t substantially influence the efficacy of peracetic acid (used at 80 and 250 ppm). However, another study (Kalchayanand et al., 2016) that confirmed the antimicrobial effectiveness of peracetic acid (200 ppm) in aqueous solutions against Salmonella and Shiga toxin-producing E. coli (with >5 logarithmic cycles in reduction) also found that its efficacy can be affected by the presence of organic matter. In that same study, lactic acid was more effective than peracetic acid in the presence of organic matter. Peracetic acid has also been demonstrated to be effective against some types of biofilms. In one study that evaluated the efficacy of peracetic acid against Pseudomonas aeruginosa (Martı´nEspada et al., 2014), biofilm formation was possible to inhibit below detection levels. In a more recent work (Shi et al., 2016) peracetic acid (200 ppm) was able to decrease the biofilm level of different strains of Salmonella on a plastic surface by 1–3 logarithmic reductions.

3 EMERGING SANITIZERS Although they may not be specifically permitted for organic produce, several emerging sanitizers have the potential to reduce the risk of microbial cross-contamination. This section briefly descries these emerging technologies. Additional regulatory approval is necessary before some of these sanitizers can be used for organic produce.

3.1 Organic Acids Organic acids represent a group of compounds of natural origin with diverse applications in the food industry, mainly as food ingredients (in the form of preservatives and antioxidants). However, due to their status as GRAS given by the FDA, their potential use as

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disinfectants or antimicrobials has been evaluated in a variety of applications. Organic acids are weak acids able to inactivate microorganisms by disruption of the transmembrane pH gradient, the internal cell pH, and the proton gradient, which results in energy depletion and cell death (Ray and Bhunia, 2014). Some of the organic acids that have been studied in the form of disinfectants include acetic acid, oxalic acid, cinnamic acid, sorbic acid, decanoic acid, citric acid, malic acid, tartaric acid, formic acid, and propionic acid (Feliziani et al., 2016). They have also been studied as a means to inhibit biofilm formation. In a recent work (Akbas and Cag, 2016), the efficacies of citric, malic, and gallic acid were evaluated against B. subtilis biofilms at concentrations of 1%–2% (w/v) on microtitration plates and on stainless steel coupons; it was found that citric acid exhibited a level of efficacy to prevent biofilm formation comparable to chlorine at levels of 200 ppm. However, it should be noted that the concentrations of each disinfectant in that study are not at the same magnitude. The organic acid concentrations used were up to 100 orders of magnitude higher than the chlorine concentrations used. This example reflects the main disadvantage of organic acids as disinfectants. Substantially high concentrations may be necessary to achieve the same results given by other disinfectants at much lower concentrations, and as a result organic acids may have a detrimental effect on equipment and food contact surfaces due to corrosion (Sagong et al., 2011; Meireles et al., 2016). The latter reasons have possibly motivated the evaluation of the effectiveness of organic acids in combination with other antimicrobial agents. In a recent study (Cossu et al., 2016), the synergistic effect between gallic acid and UV light in the UV-A range (365 nm) was evaluated to inhibit E. coli O157:H7 biofilms. The combination of the both antimicrobial agents was also tested in the presence of organic matter (2000 mg O2/L COD). In the cited study, it was confirmed that gallic acid is an approved food ingredient with no intrinsic antimicrobial activity, but its combination with UV-A light was able to provide >5 logarithmic reductions in suspension, and 3 logarithmic reductions in the presence of organic matter. The combination was also able to reduce the metabolic activity of the E. coli O157:H7 biofilm by 80%. Moreover, the gallic acid solution could be recycled to be used for up to 3 cycles of inactivation with no loss of antimicrobial efficacy. It was also confirmed that the combination of UV-A light and gallic acid was able to produce reactive oxygen species (specifically hydrogen peroxide) as part of the reason behind the antimicrobial effect. In another recent work (Wang et al., 2017), the mechanisms behind the synergistic action between gallic acid and UV-A light (365 nm) were elucidated, and it was found that UV-A light is able to induce uptake of gallic acid by E. coli O157:H7, inducing intracellular generation of reactive oxygen species, inhibition of superoxide dismutase activity (disturbing cellular redox balance), and disruption of cell morphology. A different approach may consist in combining organic acids with surfactants. In one study (Webb et al., 2013), levulinic acid was combined with sodium dodecyl sulphate to inactivate Salmonella enterica serovar Poona inoculated on cantaloupes (at different locations), at two different combinations: 1% levulinic acid with 0.1% sodium dodecyl sulphate, and 2% levulinic acid with 0.2% sodium dodecyl sulphate. Chlorine at 120 ppm was used as a positive control. The disinfectants were applied either by immersion or brushing. Both combinations of levulinic acid and sodium dodecyl sulphate were more effective than chlorine, resulting in up to 4.47 logarithmic reductions from the highest concentrations of levulinic acid and sodium dodecyl sulphate. In contrast, the maximum level of inactivation achieved by chlorine was 1.59 logarithmic cycles. The use of the surfactants

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may enhance removal of bacteria attached on surfaces. It is also possible that these compounds are able to loosen the cell membranes, thereby enhancing the uptake of other antimicrobial compounds used in combination.

3.2 Electrolyzed Water Electrolyzed water is a relatively new concept that has attracted attention in recent years. To produce electrolyzed water, a sodium chloride solution (although potassium chloride may also be used) has to be passed through an electrolysis chamber. The dissociation of anions and cations results in the formation of a variety of chemical species such as hypochlorous acid, chlorine gas, hypochlorite ion, and hydrochloric acid at the anode’s side (Gil et al., 2015; Meireles et al., 2016). These chemical species individually possess a powerful antimicrobial character, mainly as oxidants but also as acids, so in combination they can create an effective disinfectant. The main motivation behind the development of this concept derives from the problems related to the storage and handling of commonly used chlorine solutions (mainly in the form of sodium hypochlorite), such as toxicity and lack of stability (Gil et al., 2015). Electrolyzed water also offers several advantages such as its environmentally friendly character, lack of detrimental effect on surfaces (compared to chlorine compounds), lack of deleterious effect on the organoleptic properties of foods, and an approved status by the FDA to be used as a disinfectant at maximum concentrations of 200 ppm (FDA, 2014; Meireles et al., 2016). In a recent work (Navarro-Rico et al., 2014), neutral and acidic neutralized water (at both concentrations, 70 or 100 ppm) was challenged against mesophilic bacteria, psychrophilic bacteria, enterobacteria, yeasts, and molds in broccoli. The produce was washed and stored for up to 20 days at 5°C. Sodium hypochlorite at 100 ppm was used as a positive control. Both modes of electrolyzed water proved to be more effective than the chlorine treatment in reducing microbial loads. Moreover, the phenolic contents of the broccoli were less affected by the electrolyzed water treatments. In another study (Abadias et al., 2008), neutralized electrolyzed water was challenged against E. coli O157:H7, L. monocytogenes, Salmonella, and Erwinia carotovora inoculated in lettuce. The biocidal efficacy of neutralized electrolyzed water with a chlorine content of 50 ppm was comparable to the effect given by sodium hypochlorite at 120 ppm (1–2 logarithmic cycles). In addition, no difference in the antimicrobial efficacy was found between different inoculation levels (5–7 log (CFU/mL)). According to a 2015 memorandum from USDA, electrolyzed water is a type of chlorine material allowed in organic production and handling.

4 CONCLUSION This chapter highlights that diverse sanitizers are available to address food safety challenges associated with handling of fresh produce. It is important that the user understands the mode of action and limitations of these sanitizers to make effective use of these compounds to lower food safety risk.

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References Aarestrup, F.M., Hasman, H., 2004. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet. Microbiol. 100, 83–89. Abadias, M., Usall, J., Oliveira, M., Alegre, I., Vin˜as, I., 2008. Efficacy of neutral electrolyzed water (NEW) for reducing microbial contamination on minimally-processed vegetables. Int. J. Food Microbiol. 123, 151–158. Akbas, M.Y., Cag, S., 2016. Use of organic acids for prevention and removal of Bacillus subtilis biofilms on food contact surfaces. Food Sci. Technol. Int. 22, 587–597. Baert, L., Vandekinderen, I., Devlieghere, F., Van Coillie, E., Debevere, J., Uyttendaele, M., 2009. Efficacy of sodium hypochlorite and peroxyacetic acid to reduce murine norovirus 1, B40-8, Listeria monocytogenes, and Escherichia coli O157:H7 on shredded iceberg lettuce and in residual wash water. J. Food Prot. 72, 1047–1054. Banach, J.L., Sampers, I., Haute, S.V., van der Fels-Klerx, H.J., 2015. Effect of disinfectants on preventing the crosscontamination of pathogens in fresh produce washing water. Int. J. Environ. Res. Public Health 12, 8658–8677. Bastarrachea, L.J., Goddard, J.M., 2016. Self-healing antimicrobial polymer coating with efficacy in the presence of organic matter. Appl. Surf. Sci. 378, 479–488. Bastarrachea, L.J., Peleg, M., McLandsborough, L.A., Goddard, J.M., 2013. Inactivation of Listeria monocytogenes on a polyethylene surface modified by layer-by-layer deposition of the antimicrobial N-halamine. J. Food Eng. 117, 52–58. Bubl, C., 2007. Introduction to Post-Harvest Food Handling. Oregan State University II. CFR, 2000. Electronic Code of Federal Regulations: Part 205-National Organic Program. Cherchi, C., Gu, A., 2011. Effect of bacterial growth stage on resistance to chlorine disinfection. pdf. Water Sci. Technol. 64 (1), 7–13 Chiou, R.Y.-Y., Phillips, R.D., Zhao, P., Doyle, M.P., Beuchat, L.R., 2004. Ethanol-mediated variations in cellular fatty acid composition and protein profiles of two genotypically different strains of Escherichia coli O157:H7. Appl. Environ. Microbiol. 70, 2204–2210. Cincarova, L., Polansky, O., Babak, V., Kulich, P., Kralik, P., 2016. Changes in the expression of biofilm-associated surface proteins in Staphylococcus aureus food-environmental isolates subjected to sublethal concentrations of disinfectants. Biomed. Res. Int. 2016, 1–12. Clark, J.P., 2004. Ozone—cure for some sanitation problems. Food Technol. 58, 75–76. Cossu, A., Ercan, D., Wang, Q., Peer, W.A., Nitin, N., Tikekar, R.V., 2016. Antimicrobial effect of synergistic interaction between UV-A light and gallic acid against Escherichia coli O157:H7 in fresh produce wash water and biofilm. Innovative Food Sci. Emerg. Technol. 37, 44–52. Part A. Davidson, G.R., Kaminski-Davidson, C.N., Ryser, E.T., 2017. Persistence of Escherichia coli O157:H7 during pilot-scale processing of iceberg lettuce using flume water containing peroxyacetic acid-based sanitizers and various organic loads. Int. J. Food Microbiol. 248, 22–31. Deborde, M., von Gunten, U., 2008. Reactions of chlorine with inorganic and organic compounds during water treatment-kinetics and mechanisms: a critical review. Water Res. 42, 13–51. Demple, B., Harrison, L., 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63, 915–948. Elkins, J.G., Hassett, D.J., Stewart, P.S., Schweizer, H.P., McDermott, T.R., 1999. Protective role of catalase in Pseudomonas aeruginosa biofilm resistance to hydrogen peroxide. Appl. Environ. Microbiol. 65, 4594–4600. FDA, 2014. Food Additive Status List. U. S. Department of Health and Human Services. https://www.fda.gov/ Food/IngredientsPackagingLabeling/FoodAdditivesIngredients/ucm091048.htm. [(Accessed 1 August 2017)]. Feliziani, E., Lichter, A., Smilanick, J.L., Ippolito, A., 2016. Disinfecting agents for controlling fruit and vegetable diseases after harvest. Postharvest Biol. Technol. 122, 53–69. Flemming, C.A., Trevors, J.T., 1989. Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut. 44, 143–158. Fried, V., Novick, A., 1973. Organic solvents as probes for the structure and function of the bacterial membrane: effects of ethanol on the wild type and an ethanol-resistant mutant of Escherichia coli K-12. J. Bacteriol. 114, 239–248. Fuzawa, M., Ku, K.M., Palma-Salgado, S.P., Nagasaka, K., Feng, H., Juvik, J.A., Sano, D., Shisler, J.L., Nguyen, T.H., 2016. Effect of leaf surface chemical properties on efficacy of sanitizer for rotavirus inactivation. Appl. Environ. Microbiol. 82, 6214–6222. Gil, M.I., Go´mez-Lo´pez, V.M., Hung, Y.-C., Allende, A., 2015. Potential of electrolyzed water as an alternative disinfectant agent in the fresh-cut industry. Food Bioprocess Technol. 8, 1336–1348.

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Ryu, J., Beuchat, L.R., 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: effect of exopolysaccharide and Curli production on its resistance to chlorine. Appl. Environ. Microbiol. 71, 247–254. Sagong, H.-G., Lee, S.-Y., Chang, P.-S., Heu, S., Ryu, S., Choi, Y.-J., Kang, D.-H., 2011. Combined effect of ultrasound and organic acids to reduce Escherichia coli O157:H7, Salmonella typhimurium, and Listeria monocytogenes on organic fresh lettuce. Int. J. Food Microbiol. 145, 287–292. Sargent, S.A., Treadwell, D., 2009. Guide for Maintaining the Quality and Safety of Organic Vegetables and Melons During Harvest and Handling Operations. University of Florida Extension, Gainesville, FL. 1. 1–7 pages. Selma, M.V., Beltra´n, D., Allende, A., Chaco´n-Vera, E., Gil, M.I., 2007. Elimination by ozone of Shigella sonnei in shredded lettuce and water. Food Microbiol. 24, 492–499. Shen, C., Luo, Y., Nou, X., W, Q., Millner, P., 2013. Dynamic effects of free chlorine concentration, organic load, and exposure time on the inactivation of Salmonella, Escherichia coli O157:H7, and non-O157 Shiga toxin–producing E. coli. J. Food Prot. 76, 386–393. Shi, Z., Baker, C.A., Lee, S.I., Park, S.H., Kim, S.A., Ricke, S.C., 2016. Comparison of methods for quantitating Salmonella enterica Typhimurium and Heidelberg strain attachment to reusable plastic shipping container coupons and preliminary assessment of sanitizer efficacy. J. Environ. Sci. Health, Part B 51, 602–608. Silveira, M.G., Baumg€artner, M., Rombouts, F.M., Abee, T., 2004. Effect of adaptation to ethanol on cytoplasmic and membrane protein profiles of Oenococcus oeni. Appl. Environ. Microbiol. 70, 2748–2755. Simons, L., 2000. New Washing Treatments for Minimally Processed Vegetables. Lloyd Simons, et al. 144 Pages. Werribee, Australia. St-Laurent, D., Blaise, C., Macquarrie, P., Scroggins, R., Trottier, B., 1992. Comparative assessment of herbicide phytotoxicity to Selenastrum capricornutum using microplate and flask bioassay procedures. Environ. Toxicol. Water Qual. 7, 35–48. Suslow, T.V., 2000. Organic Farming Practices: Postharvest Handling. Regents of the University of California, Division of Agriculture and Natural Resources, Vegetable Research and Information Center, Organic Vegetable Production in California Series, pp. 1–10. Terracciano, J.S., Kashket, E.R., 1986. Intracellular conditions required for initiation of solvent production by Clostridium acetobutylicum. Appl. Environ. Microbiol. 52, 86–91. Todd, E.C., Michaels, B.S., Holah, J., Smith, D., Greig, J.D., Bartleson, C.A., 2010. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 10. Alcohol-based antiseptics for hand disinfection and a comparison of their effectiveness with soaps. J. Food Prot. 73, 2128–2140. Toma´s-Callejas, A., Lo´pez-Ga´lvez, F., Sbodio, A., Artes, F., Artes-Herna´ndez, F., Suslow, T.V., 2012. Chlorine dioxide and chlorine effectiveness to prevent Escherichia coli O157:H7 and Salmonella cross-contamination on fresh-cut red chard. Food Control 23, 325–332. Ukuku, D.O., Fett, W., 2002. Behavior of Listeria monocytogenes inoculated on cantaloupe surfaces and efficacy of washing treatments to reduce transfer from rind to fresh-cut pieces. J. Food Prot. 65, 924–930. Van Haute, S., Uyttendaele, M., Sampers, I., 2013. Organic acid based sanitizers and free chlorine to improve the microbial quality and shelf-life of sugar snaps. Int. J. Food Microbiol. 167, 161–169. Vurma, M., Pandit, R.B., Sastry, S.K., Yousef, A.E., 2009. Inactivation of Escherichia coli O157:H7 and natural microbiota on spinach leaves using gaseous ozone during vacuum cooling and simulated transportation. J. Food Prot. 72, 1538–1546. Wang, Q., de Oliveira, E.F., Alborzi, S., Bastarrachea, L.J., Tikekar, R.V., 2017. On mechanism behind UV-A light enhanced antibacterial activity of gallic acid and propyl gallate against Escherichia coli O157:H7. Sci. Rep. 7, 8325. Webb, C.C., Davey, L.E., Erickson, M.C., Doyle, M.P., 2013. Evaluation of levulinic acid and sodium dodecyl sulfate as a sanitizer for use in processing Georgia-grown cantaloupes. J. Food Prot. 76, 1767–1772. WSU, 2011. Postharvest information network. In: Postharvest Information Network. Washington State University. http://postharvest.tfrec.wsu.edu/pages/J3I4C. Yuk, H.-G., Yoo, M.-Y., Yoon, J.-W., Moon, K.-D., Marshall, D.L., Oh, D.-H., 2006. Effect of combined ozone and organic acid treatment for control of Escherichia coli O157:H7 and Listeria monocytogenes on lettuce. J. Food Sci. 71, M83–M87. Zhou, B., Luo, Y., Nou, X., Lyu, S., Wang, Q., 2015. Inactivation dynamics of Salmonella enterica, Listeria monocytogenes, and Escherichia coli O157:H7 in wash water during simulated chlorine depletion and replenishment processes. Food Microbiol. 50, 88–96.

Further Reading U.S. Government Publishing Office, www.ecfr.gov. [(Accessed 20 July 2008)]. C. RECOMMENDATIONS AND INTERVENTION FOR IMPROVING SAFETY

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Control Strategy for Postharvest Microbiological Safety of Animal Products During Processing, Marketing, and Quality Measures Tagelsir Mohamed Raleigh District Office, Food Safety and Inspection Services, United States Department of Agriculture, Trenton, NJ, United States

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1 INTRODUCTION The United States Department of Agriculture (USDA) Food Safety and Inspection Service (FSIS) is the public health agency responsible for protecting the public’s health by ensuring the safety of the Nation’s commercial supply of meat, poultry, and processed egg products. The agency concentrates its efforts on pathogens with a major contribution to foodborne illness and adverse effects to the public health. Sofos (2008) identifies the bacterial pathogens of concern, meaning those that need to be controlled in fresh meat and poultry products, for example, Salmonella, Campylobacter, Escherichia coli including serotype O157:H7, and several other enteric pathogens. E. coli is a gram-negative, facultative anaerobic, rod-shaped bacterium commonly found in the lower intestine of warm-blooded organisms (endotherms). Most E. coli strains are harmless, but some serotypes can cause serious food poisoning in their hosts and are occasionally the reason for product recalls. For example, E. coli O157:H7 can produce large quantities of a potent toxin called shiga toxins, which cause severe damage to the lining of the intestine. Some strains of E. coli can colonize in the intestines of animals and ultimately contaminate meat products. E. coli O157:H7 is easily destroyed by thorough cooking. Salmonella is a genus of rod-shaped, gram-negative bacteria of the Enterobacteriaceae family. The two important species are Salmonella enterica and Salmonella bongori. S. enterica is divided into six subspecies including >2500 serotypes. Salmonella may be found in the intestinal tracts of livestock, poultry, and other warm-blooded animals. Cold temperature (freezing) doesn’t kill this microorganism, but it is destroyed by high temperature (thorough cooking). Staphylococcus is a genus of gram-positive bacteria. They appear round (cocci) and form grape-like clusters. The Staphylococcus genus includes at least 40 species. Of these, nine have two subspecies, one has three subspecies, and one has four subspecies. Although most are considered harmless and reside normally on the skin and mucous membranes of humans and animals, Staphylococcus aureus can be pathogenic. Most outbreaks are a result of contamination from food handlers and production of a heat-stable toxin in the food. Hygienic practices in food handling, proper cooking, and refrigeration can prevent staphylococcal foodborne illness. Listeria is a bacterium with 10 known species (until 1992), each containing two subspecies. As of 2014, another five species were identified. Listeria species are gram-positive, rod-shaped, and facultative anaerobe, and do not produce endospores. Among different species, Listeria monocytogenes is considered to be pathogenic, usually the causative agent of severe bacterial disease, listeriosis. The disease is of particular concern to pregnant women, newborns, adults with weakened immune systems, and the elderly. In the overt form, listeriosis has a case-fatality rate around 20%. The two main clinical manifestations are sepsis and meningitis. Meningitis is often complicated by encephalitis, when it is known as meningoencephalitis, a pathology unusual for most bacterial infections. Listeria ivanovii is another pathogen of mammals, specifically ruminants, and has rarely caused listeriosis in humans. L. monocytogenes is destroyed by cooking, but a cooked product can be recontaminated by poor handling practices and poor sanitation. FSIS has a zero tolerance for L. monocytogenes in cooked and ready-to-eat (RTE) products such as beef franks or lunchmeat.

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These bacteria can be managed with proper handling and thorough cooking. Meat must be adequately cooked to eliminate any disease-causing bacteria that may be present. Bacteria can be found on raw or undercooked chicken. Some bacteria associated with chicken are Salmonella enteritidis, S. aureus, Campylobacter jejuni, and L. monocytogenes. They multiply rapidly at temperatures between 40°F (4.4°C) and 140°F (60°C) out of refrigeration and before thorough cooking occurs. Pork must also be adequately cooked to eliminate disease-causing parasites and bacteria that may be present. Although the estimated prevalence of Trichinella in pork products greatly decreased by 1995, humans may contract trichinosis (caused by the parasite, Trichinella spiralis) by eating undercooked pork. Some other foodborne microorganisms that can be found in pork are E. coli, Salmonella, S. aureus, and L. monocytogenes. Proper handling and thorough cooking destroys them all. Salmonella spp. cause illness by means of infection, that is, the organism grows/multiples in the host’s body and becomes established in or on the cells or tissues of the host. Salmonella multiplies in the small intestine, colonizes, and subsequently may invade the intestinal tissues, produce enterotoxins, and cause inflammatory reaction and diarrhea. When Salmonella overcomes the natural defense systems of the host, the organisms can enter the blood stream and cause more severe illnesses. Symptoms usually develop 12–72 h after the consumption of contaminated foods. Acute symptoms may last for 1–2 days or may be prolonged depending on host factors, ingested dose, and strains ( Jay, 2000). Serious bloodstream infections can occur in the very young or elderly. The target populations susceptible to salmonellosis are the elderly and infants. The infective dose of Salmonella depends on host resistance, pathogen virulence, and food matrix. However, studies have reported that consumption of foods containing 102–109 cells of nontyphoid Salmonella can cause gastroenteritis in humans (Blaser and Newman, 1982). Food safety in general and control of zoonotic pathogen in meat and poultry must be managed by well-established systems. It is important to control fecal contamination of carcasses and product temperature in slaughterhouses. Public health is protected when FSIS verifies an establishment’s compliance with the pathogen reduction, sanitation, and Hazard Analysis and Critical Control Point (HACCP) regulations.

2 SANITATION Sanitation is vital to the food industry. The wholesomeness of products depends on the sanitary measures implemented during the food production process. Insanitary practices and equipment, poor food handling, and improper personal hygiene can create an environment leading to contamination of food products. Food production facilities include, but are not limited to, floors, drains, walls, doors and doorways, water supply, lighting, and refrigeration. Effective environmental sanitation and cleanliness with hygienic maintenance of equipment, proper personal hygiene, and proper food handling practices substantially reduce the risk of product contamination and are essential to the implementation of other food safety systems, such as HACCP.

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Establishments under inspection must adhere to Sanitation Standard Operating Procedures (SSOP) and the Sanitation Performance Standards (SPS). Following and complying with both is important to prevent product contamination. Under the SSOP requirements, each establishment must develop, implement, and maintain written protocols for the procedures it conducts daily, before and during operations, to prevent product from direct contamination and adulteration. Any deviations must be corrected, and proper records must be kept of all activities.

3 SANITATION PERFORMANCE STANDARD SPS requirements encompass the conditions in and around the establishment (e.g., ventilation, lighting, facility and equipment construction, and maintenance of the grounds). SPS requirements used in conjunction with SSOP requirements ensure that meat and poultry products are produced in a sanitary manner. The 9 Code of Federal Regulation (CFR) 416 deal with both SPS and SSOP; the parts dealing with SPS includes establishment grounds and facilities (416.2), equipment and utensils (416.3), sanitary operations (416.4), employee hygiene (416.5), and tagging insanitary equipment, utensils, rooms, or compartments (416.6) (CFR, 2018).

4 SANITATION STANDARD OPERATING PROCEDURE The SSOP is composed of preoperational and operational activities. There are two components to these activities: record review, review and observation of the SSOP task, or both. Red meat processing establishments receive beef and pork for further processing. These establishments cut, grind, and package meat for further processing. Establishments monitor sanitation steps and record the findings, as well as any corrective actions and preventive measures necessary. All records, data, checklists, and other information pertaining to the SSOP will be maintained on file and made available to the FSIS Consumer Safety Inspector. The establishment sanitation crew performs daily organoleptic sanitation inspection after preoperational equipment cleaning and sanitizing. The results will be recorded on a preoperational sanitation form. If it is found to be acceptable, the appropriate line will be checked. If corrective actions are needed, such actions will be documented. If the equipment does not pass organoleptic examination, the corrective actions will be implemented as stated on the establishment’s sanitation plan. The establishment personnel monitor the cleaning of the equipment and retrain employees, if necessary. The corrective actions must be designed to prevent direct product contamination or adulteration, and are recorded on the preoperational sanitation forms. The parts of 9 Code of Federal Regulation (CFR) 416 dealing with SSOP includes development of SSOPs (416.12), implementation of SSOPs (416.13), maintenance of SSOPs (416.14), corrective actions (416.15), and record-keeping requirements (416.16) (CFR, 2018). Establishments producing RTE products have a special responsibility for sanitation because of the high risk of foodborne illness due to postlethality contamination of RTE product.

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The main concern is the contamination of RTE products with L. monocytogenes. Establishments must focus on preventing contamination with L. monocytogenes, which can be introduced by contaminated food contact surfaces, employees, or the environment. Cross-contamination occurs when postlethality exposed RTE product directly contacts a surface that has been contaminated with bacteria. Establishments are to implement practices to prevent cross-contamination to ensure that sanitation is properly maintained, with special attention to areas where product is stored or handled after a lethality treatment has been applied to the product.

5 HAZARD ANALYSIS AND CRITICAL CONTROL POINTS The HACCP system is composed of seven steps designed to manage risks, often referred to as the HACCP principles: 1. Conduct hazard analysis: Hazard analysis is the initial step in designing the HACCP plan. Its purpose is to develop a list of hazards that are reasonably likely to cause injury or illness if not effectively controlled. If a hazard is justified as not reasonably likely to occur, then it may be controlled through a prerequisite program, such as Good Manufacturing Practices or SSOP. 2. Determine critical control points: Critical control points (CCPs) are those points in food processing at which the hazard can be prevented, eliminated, or reduced to acceptable levels. 3. Establishment of critical limits: Critical limits are the parameters that indicate whether the control measure at the CCP is in or out of control. It is a maximum or minimum value to which a biological, chemical, or physical parameter must be controlled to prevent, eliminate, or reduce a parameter to an acceptable level. 4. Establish monitoring procedure: This is a set of observations or measurements to assess whether a CCP is under control and to produce an accurate record for future use in verification. Every CCP in the HACCP plan must be monitored to ensure that the critical limits are consistently met and that the process is producing safe product. 5. Establish corrective actions and preventive measures: Corrective actions must be determined for each CCP in cases where the critical limit is not met. Corrective actions are required to prevent potentially hazardous foods from reaching consumers. The corrective actions consist of: a. Identifying and eliminating the cause of the deviation, b. Ensuring that the CCP is under control after the corrective action is taken, c. Ensuring that measures are established to prevent recurrence, and d. Ensuring that no product affected by the deviation is shipped. 6. Establish record-keeping and documentation procedures: All measurements taken at a CCP, and any corrective actions taken, should be documented and kept on file. These records can be used to trace the production history of a finished product. A review of records is to determine whether the product was produced in a safe manner according to the HACCP plan.

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7. Establish verification procedures: There are four processes involved in the verification of the establishment’s HACCP system. The establishment is responsible for the first three; FSIS is responsible for the fourth. a. Scientific and technical processes, known as validation, for determining that the CCP and associated critical limits are adequate and sufficient to control hazards that are reasonably likely to occur. b. To ensure, initially and on an ongoing basis, that the entire HACCP system functions properly. c. To conduct documented, periodic reassessment of the HACCP plan. d. Government verification (under the regulatory authority granted to FSIS) to ensure that the establishment’s HACCP system is functioning adequately.

6 PROCESS CATEGORY There are nine identified HACCP process categories: 1. Slaughter: Occurs in establishments where the livestock are slaughtered. This should adhere to the human handling procedures. 2. Raw nonintact: This applies when further process was used such as grinding and other processes. 3. Raw intact: This process is associated with the raw nonground products. 4. Thermally processed, commercially sterile: These finished products are products in cans or flexible containers. 5. Not heat-treated, shelf stable: This process mainly uses a curing, drying, or fermenting processing step to reach food safety. The products in this process are shelf stable, because it mainly depends on the water activity. This kind of product does not required to be frozen or refrigerated. 6. Heat-treated, shelf stable: Heat treatment in this process is used to achieve the safety of the food in addition to further process used such as drying step to achieve food safety. Hence, the product of this process is shelf stable. 7. Fully cooked, not shelf stable: Full lethality cooking heat step is used; it is also named as RTE products. The finished products are not shelf stable, and it should be frozen or refrigerated. 8. Heat-treated but not fully cooked, not shelf stable: In this category, the product is further processed from other processing categories such as not ready-to-eat products or raw otherwise processed products that are refrigerated or frozen throughout the product’s shelf life. 9. Products with secondary inhibitors: A curing processing step or other ingredients may be used to inhibit the growth of the bacteria. These products are generally refrigerated or frozen. To verify regulatory compliance for specific HACCP tasks in the Public Health Information System (PHIS; a web-based inspection application for recording FSIS inspection results), there are multiple components to consider. These include (1) record-keeping and review

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and observation, and (2) monitoring, verification, and corrective actions. Inspection staff uses either component or a combination of the components. Inspection staff needs to use the regulatory thought process when performing the HACCP inspection tasks and gather information, assess the situation, and determine if the information supports the findings. Inspection staff will either determine the HACCP system is effectively controlling the food safety hazards or the establishment has failed to meet one or more HACCP regulatory requirements. In case of failure, a noncompliance record should be issued to the establishment. This can be closed when the establishment provides the inspection staff functioning corrective action and preventive measures to prevent recurrence of the incident.

7 POULTRY PROCESSING Ante-mortem and Good Commercial Practices should be followed for poultry presented for slaughter. Inspection is performed on a lot basis. The establishment should designate the size of the lot. In general, a lot is made up of birds from a single house of poultry raised on a single farm, and also it might be as large as the whole number of chicken in a specific farm. The inspection team examines the birds before slaughter, and only accepts the birds capable of producing healthy and safe products. Generally, the purpose of ante-mortem inspection is to pass birds that are healthy, safe, and capable of being processed into wholesome product. Inspection of birds is for removal of diseased animals from the food supply prior to slaughter and to identify those requiring a more postmortem examination by FSIS inspectors. After bleeding, the birds are conveyed through a scalding tank. Scalding loosens the feathers and makes for easier plucking and pinfeather removal. Carcasses scalded in water of 138–140°F for 30–75 s are generally considered to be subscalded. Semiscalding, often called soft- or slack-scalding, is carried out at 123–130°F for 90–120 s. Scalding temperature is of greater importance than scalding time. The higher the temperature, the shorter the time required, but care must be taken to control time and temperature, because at higher temperatures there is a greater danger of removal of portions of skin in the defeathering machines. Optimum conditions must be established for the kind of bird being dressed. The USDA requires using a minimum of one quart of hot water per bird (Cason, et al., 2000). After scalding, the birds pass through the picking system. Picking machines consist of revolving drums with rubber fingers that remove the feathers. The neck of the bird also passes through a separate neck scalder. This helps to ensure all neck feathers have been removed. Finally, the carcasses are washed with a stream of water and simultaneously scrubbed with rubber fingers (Geornaras, et al., 1997; Wempe, et al., 1983). Evisceration and inspection generally take place in a conditioned room. Usually, an airhandling unit with cooling and heating coils is used to provide the required conditioning and ventilation. At this point, the inspection team will condemn either whole bird or partial carcass. The inspection team checks for synovitis (inflammation of the hock joint), inflammatory process, air sacculitis, tumors, leukosis, and sometimes cooked appearance, which indicates overscald, may be septicemia and toxemia (emaciation). Each of these diseases has its own regulation, which is part of Title 9 Code of Federal Regulations.

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Birds passing inspection are thoroughly washed, then rapidly chilled to about 30–35°F with cold water or ice slush, which always contain chlorine to preserve quality and to prevent spoilage. Chlorine is a widely distributed element not found in its free state but exists primarily in combination with sodium, calcium, potassium, and magnesium. Commercially, sodium and calcium are generally combined with chlorine to produce hypochlorite that is more convenient to use than other forms of chlorine, such as chlorine gas. With the emerging use of hypochlorites, chlorine and hypochlorite will be used as interchangeable terms; however, the most prevalent form of chlorine for food industry use is in the form of hypochlorite in water treatment systems. As disinfectants, chlorine and chlorine-based compounds gained widespread acceptance as effective sanitizers. Chlorinated water used in the food industry is usually at a concentration of 20–50 ppm (Kemp et al., 2000). During chilling, the birds absorb a small amount of moisture from the slush. After chilling, the birds are drained of excess moisture and are sized and graded for quality. The USDA requires a chilled water flow rate of about 2 gal per bird. After grading, the birds may pass through an antimicrobial spray cabinet or dip tank; these interventions help control Salmonella and other pathogens, and at this step the postchill samples for microbial analysis are collected. The graded poultry is packaged fresh in boxes surrounded by crushed ice. Birds must be kept below 40°F and rapidly moved to retail distributors because shelf life may be only a few days. To prolong storage life, poultry is often frozen. The birds are vacuum-packed in low-moisture and low-oxygen transmission bags or films, as the fat of chicken is highly susceptible to the growth of microorganisms.

8 MEAT PROCESSING The slaughtered animals like cattle, goat, swine, etc. should be healthy and physiologically normal. They should be rested, especially if they have traveled over long distances. Most food hazards originate with the live animals and are commonly found on the hides, hooves, and in the gastrointestinal tract. The microbial contamination can be reduced through effective sanitary dressing, which is a practice conducted by establishments to handle carcasses that produce safe products. Pigs are usually slaughtered on arrival as time and distances traveled are relatively short and holding in pens is considered to be stressful for them. Animals should be watered during holding and can be fed, if they stay >24 h. The holding period allows the animals to settle and become less agitated, and for sick animals to be isolated and quarantined. FSIS inspectors inspect livestock before slaughter for food consumption. Regulations require that the establishments present animals for ante-mortem inspection. Certain diseases can only be determined when the livestock are alive. FSIS inspectors examine the animals and makes determination for dispositions. The animals are either passed for normal slaughter, passed for slaughter but tagged as a “U.S. Suspect” animal, or condemned and tagged.

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The slaughter of livestock involves three distinct stages, preslaughter handling, stunning, and slaughtering. In the United States, the humane treatment of animals during each of these stages is required by the Humane Methods of Slaughter Act (HMSA). When ready for slaughter, animals should be moved to the stunning area in a quiet and orderly manner without noise. Movement can be facilitated using flat straps, rolled plastic, or paper. Animals are required under the HMSA to be treated humanely. They should be led in a single line into the stunning area where they can be held appropriately before the stunning. Also, it is very important that animals are properly restrained before stunning or bleeding. This is to ensure stability of the animal so that the stunning operation can be carried out accurately and properly. Types of restraint are dependent upon the species, for example, in case of cattle, a stunning box is used. The size of the box should be just wide enough to fit the animal and prevent it from turning around, to make the stunning process run smoothly. The floor of the box should be rough to prevent the animal from slips. Some stunning areas are equipped with device to fix the head and minimize opportunity for a missed shot. If the first shot is missed, the in-establishment inspection personnel should issue a noncompliance record, and require the establishment to provide corrective actions and preventive measures to ensure that the incident does not happen again. Missing the second shot could lead to an enforcement action, such as a Notice of Suspension or Notice of Intended Enforcement. There are certain steps that play an important role in controlling product contamination, which are bunging, where a cut is made around the rectum to free from the carcass, and rodding the weasand, in which the establishment uses a rod to free the esophagus from the trachea and surrounding tissues. These measures are important steps to take to ensure that fecal material and ingesta do not contaminate the carcass.

9 COMMINUTED MEAT PRODUCTS Comminution is the mechanical process of reducing raw materials to small particles. The degree of comminution differs among various processed products and is often a unique characteristic of a particular product range from very coarsely comminuted, to finely comminuted, to forming an emulsion. Machines for Comminuting: The range and quality of finished products prepared from comminuted meat depend on the skill of personnel and the equipment available. A minimum layout should include grinder, cutter, emulsion mill, and icemaker. Machines must be designed for easy cleaning. All surfaces in contact with products must be smooth, free from pits, crevices, and scales. Machines must be constructed either of stainless steel or heat-resistant, nontoxic plastic material. All machines and tools should be carefully cleaned several times during the working day. Manufacturer’s instructions about the use and the maintenance of the machines must be strictly followed. The grinder is usually the first machine used in the comminution. For non-emulsion-type products, grinding is often the only form of comminution. It is used to cut the raw material and thoroughly mix the ingredients. Meat is pushed along a worm screw and then through

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perforated plates. The holes of the grinder plates vary both in size (2–30 mm) and shape. If the plates and knives are not kept in good condition, and particularly if they are not sharp, meat will become overheated and greasy, and lose its binding ability. The cutter is the most important comminuting machine for simultaneous comminution and mixing. Meat revolves in a bowl and passes through a set of knives mounted on a high-speed rotating arbor in a fixed position. The meat is guided toward the knives by a plow fixed inside the bowl. There are usually two speeds each for the bowl and the knives. The knives can differ in size and shape from rectangular to round. There can also be a special device for charging and discharging the bowl. To eliminate heating of the batter caused by friction, ice water is added. This is better than ice flakes alone. To avoid excessive heating, properly sharpened knives must be used, and the clearance between the knives and the bowl should not exceed 0.7 mm. A thermometer is mounted on the cover of the bowl to monitor the temperature of the meat batter. Modern cutters can operate under vacuum, which improves the color and other properties of the finished meat products. Depending on the meat-particle size desired, it is possible to produce a satisfactory comminuted meat product using only the cutter. For very fine products, such as frankfurters or bologna, it is often preferable to pass the emulsion obtained in the cutter through an emulsion mill.

10 STRATEGIES FOR INACTIVATION OF BACTERIA Studies have been conducted to examine the population dynamics of a number of pathogenic and spoilage bacteria. The growth, survival, and inactivation of Salmonella spp. in broth, sterile chicken, and chicken with native microflora have been studied as a function of temperature and conditions encountered during processing, storage, and handling of chicken (Oscar 2005, 2006, 2007). Mohamed et al. (2015) studied the chlorine resistance among strains of Salmonella Kentucky isolated from chicken carcasses. Eight strains were exposed to 30 ppm of chlorine in 10% buffered peptone water (pH 7.4) for 0–10 min at 4°C and 150 rpm. The initial level (mean
SD) of S. Kentucky was 6.18
0.09 log CFU/mL and did not differ (P ˃ 0.05) among strains. A two-way analysis of variance indicated that the level of S. Kentucky in chlorinated water was affected (P < 0.05) by a time by strain interaction. Differences among strains increased as a function of chlorine exposure time. After 10 min of chlorine exposure, the most resistant strain was 5.63
0.54 log CFU/mL, whereas the least resistant strain was 3.07
0.29 log CFU/mL. Significant differences in chlorine resistance were observed for most strain comparisons. Death of S. Kentucky was nonlinear over time and fitted well to a power law model with a shape parameter of 0.34 (concave upward). Time (minutes) for a 1-log reduction of S. Kentucky differed (P < 0.05) among strains: >10 min for SK145, 6.0 min for SK254, 1.5 min for SK179, and 0.3–0.65 min for other strains. Results of the Mohamed et al. (2015) study indicate that strain is an important variable to include in models that predict changes in levels of S. Kentucky in chlorinated water.

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Leclair et al. (1994) investigated the inactivation of L. monocytogenes and Salmonella typhimurium in synthetic egg washwater under varying conditions, that is, temperature (38–46°C), egg solids (0%–2%), pH (9.5–10.5), and chlorine concentration (0–10 μg per mL) using a full factorial design. Inactivation was measured as the logarithm of the time required for a 4-log reduction in viable counts. Both pathogens were significantly affected by temperature and the presence of egg solids, whereas the survival of S. typhimurium was significantly reduced by pH and chlorine alone. Both pathogens were affected by second order interactions involving egg and either pH or chlorine. Egg was the most significant factor, reducing the survival of L. monocytogenes while promoting the survival of S. typhimurium. The effects of chlorine and pH on the bactericidal activity of electrolyzed water were examined by Park et al. (2004) against E. coli O157:H7 and L. monocytogenes. The residual chlorine concentration of the electrolyzed water ranged from 10 to 500 ppm, and the pH effect was examined at pH 3.0, 5.0, and 7.0. The bactericidal activity of the electrolyzed water increased with the residual chlorine concentration for both pathogens, and complete inactivation was achieved at residual chlorine levels equal to or higher than 10 ppm. The results showed that both pathogens are very sensitive to chlorine, and residual chlorine levels of electrolyzed water should be maintained at 100 ppm or higher for practical applications. For each residual chlorine level, bactericidal activity of electrolyzed water increased with decreasing pH for both pathogens. However, with sufficient residual chlorine (>200 ppm), electrolyzed water can be applied in a pH range between 2.6 (original pH of electrolyzed water) and 7.0 while still achieving complete inactivation of E. coli O157:H7 and L. monocytogenes. Kemp et al. (2000) investigated the acidified sodium chlorite (ASC) solution for its antimicrobial effects on broiler carcasses processed under conditions similar to those used in U.S. commercial poultry facilities. Of particular interest was the ability of the ASC solution to reduce natural bioburden in a prechill procedure. A number of parameters such as pretreatment washing of carcasses with water (no wash vs. water wash), ASC concentration (500, 850, and 1200 ppm), method of application (spray vs. dip), and method of acid activation (phosphoric acid vs. citric acid) were explored to evaluate disinfection conditions. ASC dip solutions (18.9 L) were freshly prepared for groups of five prechill eviscerated carcasses per treatment (n ¼ 10 carcasses). ASC treatment was shown to be an effective method for significantly reducing naturally occurring microbial contamination on carcasses. Reductions following immersion dipping were demonstrated at all disinfectant concentrations for total aerobes (82.9%–90.7%), E. coli (99.4%–99.6%), and total coliforms (86.1%–98.5%). Additionally, testing showed that ASC solutions maintained stable pH and minimal chlorite ion concentration deviations throughout each treatment. The results of the parameter evaluations indicated that maximal antimicrobial activity was achieved in carcasses that were prewashed and then exposed to a 5-s dip in a solution containing phosphoric acid or citric acid activated with ASC. At 1200 ppm ASC, a mild but transitory whitening of the skin was noted on dipped carcasses. The results support the methods currently approved by the USDA for the use of ASC solutions as a prechill antimicrobial intervention in U.S. poultry processing establishments. Acidic electrolyzed water has strong bactericidal activity against foodborne pathogens on fresh vegetables. However, soil or other organic materials present influence the efficacy of acidic electrolyzed water. Park et al. (2009) studied the bactericidal activity of acidic electrolyzed water in the presence of organic matter, in the form of bovine serum, against foodborne

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pathogens on the surfaces of green onion and tomatoes. Green onion and tomatoes were inoculated with a culture cocktail of E. coli O157:H7, S. typhimurium, and L. monocytogenes. Treatment of these organisms with acidic electrolyzed water containing bovine serum concentrations of 5, 10, 15, and 20 mL/L was performed for 15 and 30 s, and 1, 3, and 5 min. The total residual chlorine concentrations of acidic electrolyzed water decreased proportionally to the addition of serum. The bactericidal activity of acidic electrolyzed water also decreased with increasing bovine serum concentration, whereas unamended acidic electrolyzed water treatment reduced levels of cells to below the detection limit (0.7 log CFU/g) within 3 min (Park et al., 2009). Chlorine dioxide (ClO2) is a strong oxidizing agent that can be applied in solution as well as in the gaseous state. It has bactericidal, fungicidal, and viricidal properties. Several foodrelated microorganisms, including gram-negative and gram-positive bacteria, yeasts, mold spores, and Bacillus cereus spores were tested for their susceptibility to 0.08 mg/L gaseous ClO2 during 1 min at a relative humidity of 90%. In this screening, the resistance of the different groups of microorganisms toward gaseous ClO2 generally increased in the order gram-negative bacteria, gram-positive bacteria, yeasts, and mold and B. cereus spores. With this treatment, reductions of microbial numbers between 0.1 and 3.5 log CFU/cm2 were achieved. The effects of the food components starch, fat, protein, and NaCl on the antimicrobial activity of gaseous ClO2 were also evaluated. Soluble starch, corn oil, butter, whey protein isolate, and NaCl were added in incremental concentrations to portions of an agar medium, and then plates of the supplemented agars were inoculated with Leuconostoc mesenteroides at numbers of 4 log CFU/cm2 and subsequently treated with ClO2. Both soluble starch and sodium chloride did not have an effect on the antimicrobial efficacy of ClO2. However, butter, corn oil, or whey protein in the agar almost eliminated the antimicrobial effect of ClO2. In corn oil–water emulsions treated with gaseous ClO2, the peroxide value increased significantly, indicating the formation of primary oxidation products. Similarly, a treatment with ClO2 increased the protein carbonyl content and induced the transformation of SH-groups to dSdSgroups in whey protein. The findings suggest that gaseous ClO2 will be a highly effective decontaminating agent for carbohydrate-rich foods, but that it would be less effective for the decontamination of high-protein and fatty foods (Vandekinderen et al., 2009). Kim et al. (2008) also studied the inactivation of E. coli O157:H7, S. typhimurium, and L. monocytogenes in iceberg lettuce by aqueous chlorine dioxide (ClO2) treatment. For this study, iceberg lettuce samples were inoculated with approximately 7 log CFU/g of E. coli O157:H7, S. typhimurium, and L. monocytogenes and then samples were treated with 0, 5, 10, or 50 ppm ClO2 solution and stored at 4°C. Aqueous ClO2 treatment significantly decreased the populations of pathogenic bacteria on shredded lettuce (P < 0.05). In particular, 50 ppm ClO2 treatment reduced E. coli O157:H7, S. typhimurium, and L. monocytogenes by 1.44, 1.95, and 1.20 log CFU/g, respectively. Changes in aerobic plate counts (APC), total coliform counts (TCC), E. coli counts (ECC), and Salmonella incidences on poultry carcasses, parts, and in poultry processing water were evaluated at three processing establishments: (1) establishment A (New York wash, postevisceration wash, inside-outside bird washes 1 and 2, chlorine dioxide wash, chlorine dioxide wash plus chlorine chiller, chiller exit spray, and postchill wash); (2) establishment B (New York wash, inside-outside bird washes 1 and 2, trisodium phosphate wash, and chlorine chiller); and (3) establishment C (trisodium phosphate wash and chlorine chiller). The majority

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of individual interventions effectively or significantly (P < 0.05) reduced microbial populations on or in carcasses, carcass parts, and processing water. Reductions in APC, TCC, and ECC due to individual interventions ranged from 0 to 1.2, 0 to 1.2, and 0 to 0.8 log CFU/mL, respectively. Individual interventions reduced Salmonella incidence by 0% to 100% depending on the type of process and product. Multiple-sequential interventions resulted in significant reductions (P < 0.05) in APC, TCC, ECC, and Salmonella incidence of 2.4, 2.8, and 2.9 log CFU/mL and 79%, respectively, at establishment A; 1.8, 1.7, and 1.6 log CFU/mL and 91%, respectively, at establishment B; and 0.8, 1.1, and 0.9 log CFU/mL and 40%, respectively, at establishment C. These results enabled validation of in-establishment poultry processing interventions and provide a source of information to help the industry in its selection of antimicrobial strategies (Stopforth et al., 2007).

11 SAMPLING Verification activities serve to protect the consumers from foodborne hazards. A key component of FSIS inspection activity is the sampling of product to test for microbiological contaminants. A baseline study was conducted during the period from December 2005 to January 2007 by FSIS. Samples were collected from meat and poultry products to estimate the national prevalence and levels of bacteria of public health concern. Those samples are collected from federally inspected establishments and analyzed by the three federal laboratories in the United States. Beef trimmings were collected at establishments operating under federal inspection. Samples were analyzed to estimate the percent positive and levels of E. coli O157:H7, and Salmonella. The study found 0.68% and 1.28%, E. coli O157:H7 and Salmonella positive samples, respectively. FSIS conducted the Raw Chicken Parts Baseline Survey from January 2012 to August 2012. The survey generated 2496 valid samples of diverse chicken parts collected at the end of the production line. These samples were analyzed to determine the percent positive and pathogen levels for Salmonella and Campylobacter, as well as the levels for generic E. coli, APC, Enterobacteriaceae, and total coliforms. The Salmonella and Campylobacter positive rate for different chicken parts was 26.3% and 21.4%, respectively. The positive percentage for APC (35°C APC), Enterobacteriaceae, coliforms, and generic E. coli were 98.84%, 96.23%, 88.46%, and 62.6% respectively. Routine samples are categorized to follow-up on the quality of products, and primarily concentrate on collecting samples to verify compliance of the federally inspected establishments; those establishments are randomly selected each month. Also, routine samples are collected from retail stores through routine visits. In addition, follow-up samples are collected depending on the results of the samples collected from the randomly selected establishments and the routine samples. The follow-up samples include both sampling to verify corrective actions and sampling to help identify the source of the contamination. Table 1 shows the sampling results for FSIS-regulated products for the period from July 1, 2016, to June 30, 2017. The Raw Ground Beef was tested for E. coli O157:H7 and Salmonella spp. from 172 establishments; 552 samples were collected, resulting in one positive for E. coli O157:

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TABLE 1 Sampling Results for FSIS Regulated Products for the Period (July 1, 2016–June 30, 2017 Species

Product

Pathogen

Type of Calculation

Raw beef

Raw ground beef

E. coli O157:H7

Percent positive

172

552

1

0.18

Raw ground beef

Salmonella spp.

Percent positive

172

552

37

6.7

Bench trim

E. coli O157:H7

Percent positive

507

1200

1

0.08

Bench Trim

Salmonella spp.

Percent Positive

507

1200

15

1.25

Intact cuts

Salmonella spp.

Percent positive

190

952

137

12.61

Intact other

Salmonella spp.

Percent positive

83

458

116

26.53

Comminuted

Salmonella spp.

Percent positive

299

1328

309

30.93

Nonintact cuts

Salmonella spp.

Percent positive

51

268

24

12.79

Nonintact other

Salmonella spp.

Percent positive

49

222

31

22.97

Carcasses

Salmonella spp.

Prevalence

205

9108

520

5.42

Carcasses

Campylobacter spp.

Prevalence

204

8961

272

1.76

Parts—legs, breasts, wings

Salmonella spp.

Prevalence

420

7566

1148

14.16

Parts—legs, breasts, wings

Campylobacter spp.

Prevalence

419

7397

288

3.43

RTE meat/poultry

Salmonella spp.

Percent positive

2198

6148

2

0.02

RTE meat/poultry

L. monocytogenes

Percent positive

2198

6148

16

0.04

RTE meat/poultry

Salmonella spp.

Percent positive

1994

8265

4