Microbial Safety of Fresh Produce E-Book

• Herausgeber: John Wiley & Sons
• Kategorie: Fachliteratur
• Serie: Institute of Food Technologists Series
• Sprache: Englisch

Seitenzahl: 961

Veröffentlichungsjahr: 2013

Beschreibung

Microbial Safety of Fresh Produce covers all aspects of produce safety including pathogen ecology, agro-management, pre-harvest and post-harvest interventions, and adverse economic impacts of outbreaks. This most recent edition to the IFT Press book series examines the current state of the problems associated with fresh produce by reviewing the recent, high-profile outbreaks associated with fresh-produce, including the possible internalization of pathogens by plant tissues, and understanding how human pathogens survive and multiply in water, soils, and fresh fruits and vegetables.

Leseprobe

Contents

Contributors

Preface

Section I Microbial Contamination of Fresh Produce

1 Enteric Human Pathogens Associated with Fresh Produce: Sources, Transport, and Ecology

Introduction

Outbreaks Associated with Selected Fresh Produce Commodities

Incidence of Human Pathogens on Fresh Produce

Incidence of Generic E. coli on Produce

Animal Sources of Enteric Foodborne Pathogens Relevant to Produce Contamination

High-level Shedding of E. coli O157:H7 and Salmonella by Some Animals

Incidence of Potential Pathogens in Municipal and Agricultural Watersheds

Fate and Transport of Human Pathogens in the Environment

Source-Tracking Pathogens and Fecal Indicators of Contamination in Watersheds

How Do Pathogens Get onto Preharvest Produce and Survive?

Conclusions

Acknowledgments

References

2 The Origin and Spread of Human Pathogens in Fruit Production Systems

Introduction

Role of Fresh Fruit in Foodborne Illness

Preharvest Contamination of Crops

Contamination at Harvest

A Case Study: Dissemination of Enteric Bacteria in Sweet Cherry Orchards

Conclusions

References

3 Internalization of Pathogens in Produce

Introduction

Bacterial Endophytes

Sources of Human Endophytic Pathogens

Bacterial Attachment and Colonization

Impact of Plant Stress on Internalization

Portals of Entry

Bacterial Movement in Plants

Methods for Examining Bacterial Internalization

Labeling of Endophytic Bacteria

Methods for Introducing Endophytic Bacteria into Plants

Foodborne Pathogen Interactions with Plant and Soil Microflora

Evidence for Internalization of Foodborne Pathogens in Produce

References

Section II Preharvest Strategies

4 Produce Safety in Organic vs. Conventional Crops

Introduction

Organic Foods

Safety Issues Associated with Organic Fresh Produce

Pathogen Survival in Manure, Compost, and Soil

Bacterial Prevalence in Organic and Conventional Produce

Escherichia coli Contamination in Fresh Fruits and Vegetables

Evaluation of Organic Practices That Could Be Linked to Produce Contamination

Epidemiology of Foodborne Disease Linked to Organic Produce

Summary

References

5 The Role of Good Agricultural Practices in Produce Safety

Introduction

The Nature of Pathogen Contamination

The Economic Impact of Produce Outbreaks

The Development and Implementation of Good Agricultural Practices (GAPs)

Components of GAPs

Advancing GAPs Implementation

References

6 Effectively Managing through a Crisis

Introduction

Defining the Incident Management Plan

The Incident Management Team

Developing the Incident Management Plan

Implementing the Plan during a Crisis

The Seven R’s of a Response

Conclusions

7 The Role of Water and Water Testing in Produce Safety

Introduction

Occurrence of Foodborne Pathogens in Water

Survival in Water

Water Testing

Standards and Criteria for Indicators

Irrigation Waters

Standards for Irrigation Water Quality

Process Waters

Conclusions

References

8 The Role of Manure and Compost in Produce Safety

Introduction

Fresh Produce Outbreaks Due to Fecal Contamination of Produce in the Field

Human Pathogens Associated with Animal Wastes

Persistence of Enteric Pathogens in Preharvest Environment

Control of Pathogens in Animal Manure by Composting

Education on Safe Use of Raw Manure and Compost

Conclusion

References

Section III Postharvest Interventions

9 Aqueous Antimicrobial Treatments to Improve Fresh and Fresh-Cut Produce Safety

Introduction

Factors That Influence Antimicrobial Activity in Produce Washing

Aqueous Antimicrobial Treatments

Conclusion

References

10 Irradiation Enhances Quality and Microbial Safety of Fresh and Fresh-Cut Fruits and Vegetables

Introduction

Quality of Irradiated Produce

Microbial Safety of Irradiated Produce

Irradiation: Not a “Silver Bullet” but a “High Hurdle”

Summary

Acknowledgments

References

11 Biological Control of Human Pathogens on Produce

Introduction

Biocontrol Technologies

Conclusions

References

12 Extension of Shelf Life and Control of Human Pathogens in Produce by Antimicrobial Edible Films and Coatings

Biopolymers Used for Edible Films and Coatings

Edible Coatings for Fresh Fruits and Vegetables

Edible Films for Fresh Fruits and Vegetables

Fruit and Vegetable-Based Edible Films

Edible Film Casting Methods

Antimicrobial Plant Essential Oils in Edible Films

Physical Properties of Edible Films Containing Plant Essential Oils

Evaluation of Antimicrobial Activity of Volatile Components

Methods to Measure the Antimicrobial Activity of Edible Films

Use of Edible Films and Coatings on Fresh Fruits and Vegetables

Summary

References

13 Improving Microbial Safety of Fresh Produce Using Thermal Treatment

Introduction

Thermal Treatment Fundamentals

Hot-Water Treatment

Microwave, RF, and Infrared

Conclusion

References

14 Enhanced Safety and Extended Shelf Life of Fresh Produce for the Military

Introduction

Bacterial Spore Resistance to and Inactivation by Chemical Agents

Novel Chlorine Dioxide Technologies for Eliminating Microbial Hazards from Fresh Produce and Food-Handling Environments

Modified Atmosphere Packaging (MAP)

Acknowledgments

References

Section IV Produce Safety during Processing and Handling

15 Consumer and Food-Service Handling of Fresh Produce

Introduction

Selecting Produce

Consumer Perception of Produce Safety

Consumer Handling Practices

Food-Service Workers Handling Practices That Affect Produce Safety

Staying Healthy, Eating Healthy

Safe Handling of Fruits and Vegetables

16 Plant Sanitation and Good Manufacturing Practices for Optimum Food Safety in Fresh-Cut Produce

Introduction

Product Risk Assessment

Worker Hygiene

Process Controls

Facility and Equipment Sanitation

Monitoring

Verification

Summary

References

17 Third-Party Audit Programs for the Fresh-Produce Industry

Introduction

Current Issues

Internal Audits and Third-Party Audits

Conclusions

References

18 Applications of Immunomagnetic Beads and Biosensors for Pathogen Detection in Produce

Introduction

Biosensors for Pathogen Detection

Biosensor Processes Involving the Use of IMB for Pathogen Detection

Conclusions

Disclaimer

References

Section V Public, Legal, and Economic Perspectives

19 Public Response to the 2006 Recall of Contaminated Spinach

Introduction

Methods

Results

Discussion and Conclusions

Acknowledgment

References

20 Produce in Public: Spinach, Safety, and Public Policy

Introduction

Research on North American Outbreaks

Industry Efforts/Regulation

Spinach

Summary

References

21 Contaminated Fresh Produce and Product Liability: A Law-in-Action Perspective

Introduction

Legal Responsibility for Foodborne Illness

Understanding the Origins of Product Liability

The Modern Rule of Strict Liability

Traceability and Product Liability

The Persistent Role of Negligence in Product Liability

Reducing Liability by Spreading the Blame

The Sustainability and Local Food Movements and Their Potential Effects on the Future of Product Liability

Conclusion

References

22 The Economics of Food Safety: The 2006 Foodborne Illness Outbreak Linked to Spinach

Introduction

The U.S. Produce Industry

Government and Industry Response to Food Safety Problems

Economics of Adoption of GAPs and the LGMA

Economic Impacts of the Spinach Outbreak

Conclusions

Acknowledgments

References

Section VI Research Challenges and Directions

23 Research Needs and Future Directions

Prevention and Microbial Ecology

Containment

References

Index

The IFT Press series reflects the mission of the Institute of Food Technologists—to advance the science of food contributing to healthier people everywhere. Developed in partnership with Wiley-Blackwell, IFT Press books serve as leading-edge handbooks for industrial application and reference and as essential texts for academic programs. Crafted through rigorous peer review and meticulous research, IFT Press publications represent the latest, most significant resources available to food scientists and related agriculture professionals worldwide.

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Edition first published 2009

© 2009 Blackwell Publishing and the Institute of Food Technologists

Chapters 1, 5, 10, 12, 13, 14, 17, 18, and 22 remain with the U.S. Government.

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Library of Congress Cataloging-in-Publication Data

Microbial safety of fresh produce / editors, Xuetong Fan … [et al.].

p. cm. – (The IFT press series)

Includes bibliographical references and index.

ISBN 978-0-8138-0416-3 (hardback : alk. paper)

1. Fruit–Microbiology. 2. Vegetables–Microbiology. I. Fan, Xuetong.

QR122.M537 2009

363.19'29–dc22

2009009719

A catalog record for this book is available from the U.S. Library of Congress.

1 2009

Titles in the IFT Press series

Accelerating New Food Product Design and Development

(Jacqueline H. Beckley, Elizabeth J. Topp, M. Michele Foley, J.C. Huang, and Witoon Prinyawiwatkul)

Advances in Dairy Ingredients

(Geoffrey W. Smithers and Mary Ann Augustin)

Biofilms in the Food Environment

(Hans P. Blaschek, Hua H. Wang, and Meredith E. Agle)

Calorimetry and Food Process Design

(Gönül Kaletunç)

Nondigestible Carbohydrates and Digestive Health

(Teresa M. Paeschke and William R. Aimutis)

Food Ingredients for the Global Market

(Yao-Wen Huang and Claire L. Kruger)

Food Irradiation Research and Technology

(Christopher H. Sommers and Xuetong Fan)

Food Laws, Regulations and Labeling

(Joseph D. Eifert)

Food Risk and Crisis Communication

(Anthony O. Flood and Christine M. Bruhn)

Foodborne Pathogens in the Food Processing Environment: Sources, Detection and Control

(Sadhana Ravishankar and Vijay K. Juneja)

Functional Proteins and Peptides

(Yoshinori Mine, Richard K. Owusu-Apenten, and Bo Jiang)

High Pressure Processing of Foods

(Christopher J. Doona and Florence E. Feeherry)

Hydrocolloids in Food Processing

(Thomas R. Laaman)

Microbial Safety of Fresh Produce

(Xuetong Fan, Brendan A. Niemira, Christopher J. Doona, Florence E. Feeherry, and Robert B. Gravani)

Microbiology and Technology of Fermented Foods

(Robert W. Hutkins)

Multiphysics Simulation of Emerging Food Processing Technologies

(Kai Knoerzer, Pablo Juliano, Peter Roupas, and Cornelis Versteeg)

Multivariate and Probabilistic Analyses of Sensory Science Problems

(Jean-François Meullenet, Rui Xiong, and Christopher J. Findlay

Nondestructive Testing of Food Quality

(Joseph Irudayaraj and Christoph Reh)

Nanoscience and Nanotechnology in Food Systems

(Hongda Chen)

Nonthermal Processing Technologies for Food

(Howard Q. Zhang, Gustavo V. Barbosa-Cànovas, V.M. Balasubramaniam, Editors; C. Patrick Dunne, Daniel F. Farkas, and James T.C. Yuan, Associate Editors)

Nutraceuticals, Glycemic Health and Type 2 Diabetes

(Vijai K. Pasupuleti and James W. Anderson)

Packaging for Nonthermal Processing of Food

(J. H. Han)

Preharvest and Postharvest Food Safety: Contemporary Issues and Future Directions

(Ross C. Beier, Suresh D. Pillai, and Timothy D. Phillips, Editors; Richard L. Ziprin, Associate Editor)

Processing and Nutrition of Fats and Oils

(Ernesto M. Hernandez and Afaf Kamal-Eldin)

Processing Organic Foods for the Global Market

(Gwendolyn V. Wyard, Anne Plotto, Jessica Walden, and Kathryn Schuett)

Regulation of Functional Foods and Nutraceuticals: A Global Perspective

(Clare M. Hasler)

Sensory and Consumer Research in Food Product Design and Development

(Howard R. Moskowitz, Jacqueline H. Beckley, and Anna V.A. Resurreccion)

Sustainability in the Food Industry

(Cheryl J. Baldwin)

Water Activity in Foods: Fundamentals and Applications

(Gustavo V. Barbosa-Cànovas, Anthony J. Fontana Jr., Shelly J. Schmidt, and Theodore P. Labuza)

Whey Processing, Functionality and Health Benefits

(Charles I. Onwulata and Peter J. Huth)

Contributors

Bassam A. Annous, Chapter 13

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Roberto J. Avena-Bustillos, Chapter 12

USDA, Agricultural Research Service

Western Regional Research Center

800 Buchanan St.

Albany, CA 94710

Susan Bach, Chapter 2

Agriculture and Agri-Food Canada

Pacific Agri-Food Research Centre

4200 Highway 97 South

Summerland, British Columbia, V0H 1Z0 Canada

Craig Billington, Chapter 11

Food Safety Programme, ESR Ltd.

P. O. Box 29-181

Christchurch, New Zealand

Christine M. Bruhn, Chapter 15

Center for Consumer Research

Department of Food Science and Technology,

University of California, Davis

One Shields Ave.

Davis, CA 95616-8598

Linda Calvin, Chapter 22

USDA, Economic Research Service

Specialty Crops Branch, Rm 5040s

1800 M Street NW

Washington, D.C. 20036-5831

Shubham Chandra, Chapter 14

Chandra Associates, Milford, MA 01757

Present mailing address:

U.S. Army Natick Soldier Research, Development, and Engineering Center

Department of Defense Combat Feeding Directorate

Systems and Equipment Engineering Team

Natick, MA 01760-5018

Benjamin Chapman, Chapter 20

Department of Plant Agriculture

University of Guelph

Guelph, ON, N1G 2W1 Canada

Sarah C. Condry, Chapter 19

Food Policy Institute

Rutgers University

ASB III, 3 Rutgers Plaza

New Brunswick, NJ 08901

Cara L. Cuite, Chapter 19

Food Policy Institute

Rutgers University

ASB III, 3 Rutgers Plaza

New Brunswick, NJ 08901

Will Daniels, Chapter 6

Earthbound Farm

1721 San Juan Highway

San Juan Bautista, CA 95045

Pascal Delaquis, Chapter 2

Agriculture and Agri-Food Canada

Pacific Agri-Food Research Centre

4200 Highway 97 South

Summerland, British Columbia, V0H 1Z0, Canada

Jocilyn E. Dellava, Chapter 19

Department of Psychiatry, School of Medicine

University of North Carolina at Chapel Hill

101 Manning Drive CB #7160

Chapel Hill, NC 27599

Francisco Diez-Gonzalez, Chapter 4

Department of Food Science and Nutrition

University of Minnesota

1334 Eckles Avenue

St. Paul, MN 55108

Christopher J. Doona, Chapters 14, 23

U.S. Army Natick Soldier Research, Development, and Engineering Center

Department of Defense Combat Feeding Directorate

Food Safety and Defense Team

Natick, MA 01760-5018

Michael P. Doyle, Chapter 6

Center for Food Safety

Department of Food Science & Technology

University of Georgia

1109 Experiment St.

Griffin, GA 30223-1791

Wen-Xian Du, Chapter 12

USDA, Agricultural Research Service

Western Regional Research Center

800 Buchanan St.

Albany, CA 94710

Xuetong Fan, Chapters 10, 13, 23

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Florence E. Feeherry, Chapters 14, 23

U.S. Army Natick Soldier Research, Development, and Engineering Center

Department of Defense Combat Feeding Directorate

Food Safety and Defense Team

Natick, MA 01760-5018

Hao Feng, Chapter 9

Department of Food Science and Human Nutrition

University of Illinois at Urbana-Champaign

1304 W. Pennsylvania Avenue

Urbana, IL 61801

Edith H. Garrett, Chapter 16

Edith Garrett & Associates, Inc.

P. O. Box 1470

Arden, NC 28704

Andrew Gehring, Chapter 18

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Charles P. Gerba, Chapter 7

Department of Soil, Water and Environmental Science

University of Arizona

Tucson, AZ 85721

Robert B. Gravani, Chapters 5, 23

Department of Food Science

Cornell University

Ithaca, NY 14853

William K. Hallman, Chapter 19

Food Policy Institute

Rutgers University

ASB III, 3 Rutgers Plaza

New Brunswick, NJ 08901

Jianjun Hao, Chapter 3

Department of Plant Pathology

Michigan State University

East Lansing, MI 48824

Joy Herdt, Chapter 9

Ecolab Inc.

655 Lone Oak Drive

Eagan, MN 55121

Lihan Huang, Chapter 13

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

John Andrew Hudson, Chapter 11

Food Safety Programme, ESR Ltd.

P. O. Box, 29-181

Christchurch, New Zealand

Peter Irwin, Chapter 18

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Casey J. Jacob, Chapter 20

Department of Diagnostic Medicine/Pathobiology

Kansas State University

Manhattan, KS 66506

Helen H. Jensen, Chapter 22

Dept. of Economics

Iowa State University

Center for Agricultural & Rural Development

578 Heady Hall

Ames, IA 50011-1070

Xiuping Jiang, Chapter 8

Department of Food Science & Human Nutrition

Clemson University

217 Poole Ag. Center

Clemson, SC 29634

Kenneth Kustin, Chapter 14

Department of Chemistry Emeritus

Brandeis University

Waltham, MA 02254-9110

Present mailing address:

5210 Fiore Ter L-111

San Diego, CA, 92122-5686

Jing Liang, Chapter 22

Department of Economics

Iowa State University

Center for Agricultural & Rural Development

578 Heady Hall

Ames, IA 50011-1070

Robert E. Mandrell, Chapter 1

USDA, Agricultural Research Service

Western Regional Research Center

800 Buchanan St.

Albany, CA 94710

Tara H. McHugh, Chapter 12

USDA, Agricultural Research Service

Western Regional Research Center

800 Buchanan St.

Albany, CA 94710

Lynn McIntyre, Chapter 11

Food Safety Programme, ESR Ltd.

P. O. Box, 29-181

Christchurch, New Zealand

Avik Mukherjee, Chapter 4

Department of Food Technology

Haldia Institute of Technology

HIT/ICARE Campus, Hatiberia

Haldia, East Midnapur

West Bengal 721657 India

Brendan A. Niemira, Chapters 10, 23

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Mary L. Nucci, Chapter 19

Food Policy Institute

Rutgers University

ASB III, 3 Rutgers Plaza

New Brunswick, NJ 08901

Kenneth S. Petersen, Chapter 17

USDA, Agricultural Marketing Service

Fruit and Vegetable Programs

1400 Independence Avenue SW, Room 1661, Stop 0240

Washington, D.C. 20250-0240

Douglas A. Powell, Chapter 20

International Food Safety Network

Department of Diagnostic Medicine/Pathobiology

Kansas State University

Manhattan, KS, 66506

Elliot T. Ryser, Chapter 3

Department of Food Science and Human Nutrition

National Food Safety and Toxicology Center

Michigan State University

East Lansing, MI 48824

Peter Setlow, Chapter 14

Molecular, Microbial and Structural Biology

University of Connecticut Health Center

Farmington, CT 06030-3305

Marion Shepherd, Chapter 8

Department of Food Science & Human Nutrition

Clemson University

C233 Poole Ag. Center

Clemson, SC 29634

Deborah Sisson, Chapter 14

U.S. Army Natick Soldier Research,

Development, and Engineering Center

Department of Defense Combat Feeding Directorate

Systems and Equipment Engineering Team

Natick, MA 01760-5018

Denis W. Stearns, Chapter 21

Marler Clark LLP PS

6600 Bank of America Tower

701 Fifth Avenue

Seattle, WA, 98104

Shu-I Tu, Chapter 18

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Joseph Uknalis, Chapter 18

USDA, Agricultural Research Service

Eastern Regional Research Center

600 E. Mermaid Lane

Wyndmoor, PA 19038

Zhinong Yan, Chapter 3

Department of Food Science and Human Nutrition

National Food Safety and Toxicology Center

Michigan State University

East Lansing, MI 48824

Preface

Fresh and fresh-cut fruits and vegetables contain rich sources of many nutrients and provide numerous health benefits, so nutritionists and health professionals highly recommend increasing consumption of these important foods. However, fresh produce has also been the source of recent outbreaks of foodborne illnesses, which have caused sickness, hospitalizations, and deaths of consumers, as well as serious adverse economic impact on growers and processors. The intense media attention devoted to outbreaks of Escherichia coli O157:H7 in spinach and lettuce and Salmonella linked to hot peppers and tomatoes demonstrates the importance of food safety in the mind of the public. Whether diners at the table, growers on the farm, or military personnel on shipboard or in distant global deployments, the consumer trusts the innovations of science to lead the advances dedicated to ensuring the safety of fresh produce. The increasing outbreaks of foodborne diseases associated with consumption of fresh and fresh-cut produce underscore the urgent need for significantly improving the understanding of the ecology of pathogens and for developing improved farm-to-table strategies to ensure the safety of these foods.

Fresh fruits and vegetables risk contamination because they are generally grown in open fields with potential exposure to enteric pathogens from soil, irrigation water, manure, wildlife, workers, and/or other sources. Additionally, fresh produce is often eaten raw, without cooking or other treatments that could eliminate pathogens that may be present. Although the reasons for the recent increase in fresh produce–associated foodborne illnesses are not fully understood, many reasons have been suggested, including an increase in global trade, a longer and more complex food supply chain, centralized processing plants with wide distribution networks, genetic changes increasing the pathogenicity of microorganisms, and even an aging population that is more susceptible to foodborne illness.

This book evolved from several Symposia we organized at the 2007 Institute of Food Technologists (IFT) Annual Meeting in Chicago. It provides information on all aspects of produce safety, including pathogen ecology, good agricultural and manufacturing practices, preharvest and postharvest interventions, third-party audits, economic concerns, consumer perceptions, education, legal concerns, and policy issues. The contributors of this book are nationally and internationally renowned experts in the field of produce safety who have shared their perspectives on a variety of important issues. Given the importance of produce safety to the country and the world, research in this area is extremely active, involving scientists from industry, government, and academia. New and novel intervention technologies and strategies will be developed to further minimize the risk of pathogen contamination and increase consumer confidence in fresh produce.

This book reviews the challenges of the recent, high-profile outbreaks associated with fresh produce, including the possible internalization of pathogens by plant tissues, and explains how human pathogens survive and multiply in water, in soils, and on fresh fruits and vegetables. Understanding the ecology of human pathogens will help scientists develop effective intervention strategies to enhance produce safety. Several authors discuss the latest proactive measures and strategies that the industry is taking to improve the safety of produce. With the latest advances in scientific research, all sectors of the produce industry may be able to develop and adopt integrative practices that are specific, measurable, and verifiable to assure the farm-to-table safety of produce. To minimize the risk of human pathogens on fresh produce, emphasis on preharvest strategies such as the implementation of good agricultural practices (GAPs) and a risk analysis of irrigation waters and supply lines are discussed. Postharvest interventions—from current industry practices using chemical sanitizers, to promising innovative technologies such as irradiation and biological controls—are also presented. In addition, authors address the impact of foodborne outbreaks on public health and the fresh produce industry in terms of economic impact, consumer acceptance, and legal considerations. This book offers readers comprehensive reviews of the many challenges associated with produce safety and provides strategies to minimize the risk associated with consumption of fresh produce.

This text is a useful reference for all who are interested in produce safety, from consumers to university professors, students, government scientists, produce industry personnel, agricultural advisors and policy makers, consultants, equipment suppliers, third-party auditors, food retailers, and workers in the food-service industry, and it is replete with references to original source materials.

Our deepest appreciation and thanks go to the chapter authors who contributed significant amounts of their time, talents, knowledge, and expertise to bring this book to life from concept to hardcover in the pursuit of increased produce safety. We are indebted to them for the excellence of their contributions, without which this book would never have been published. We are also grateful to the thoughtful guidance, helpful advice, and dedicated assistance that Ms. Susan Engelken and Mr. Mark Barrett at Wiley-Blackwell have given in the preparation and completion of this book.

We dedicate this book to all those individuals who work diligently devoting their talents and efforts to reducing the microbial risks and hazards in the production, harvesting, packing, transporting, and merchandising of fresh fruits and vegetables and who value the importance of keeping these important foods safe for the benefit and well-being of all consumers.

Xuetong Fan Brendan A. Niemira Christopher J. Doona Florence E. Feeherry Robert B. Gravani

Section I

Microbial Contamination of Fresh Produce

1

Enteric Human Pathogens Associated with Fresh Produce: Sources, Transport, and Ecology

Robert E. Mandrell

Introduction

Now in the cold parts of the country, don’t you think people get to wanting perishable things in the winter—like peas and lettuce and cauliflower? In a big part of the country they don’t have those things for months and months. And right here in Salinas valley we can raise them all the year round. … Do you know we could ship lettuce right to the east coast in the middle of winter?”

John Steinbeck

In 1952, John Steinbeck through his character Adam Trask in “East of Eden” commented on the desirability of fresh produce and the uniqueness of the climate and soil conditions of the Salinas Valley of California for providing leafy greens and other vegetables year-round to the rest of the nation. The development of this region on the central coast of California, known as the “Salad Bowl of America,” is linked closely to the growth of fresh produce consumption in the U.S. as a result of increased seasonal availability, new varieties of domestic and imported produce, and increased interest in the nutritional and health benefits of fresh produce (Clemens 2004). The growing global economy has continued demand for fresh produce and involves shipping produce long distances rapidly. Increased mechanization and efficiency of production, new and improved cultivars, and new chemicals to treat plant disease and new products have been developed to meet this demand. Minimally processed, bagged produce is a relatively recent new product to help meet the growing demand for fresh produce (USDA-ERS 2001).

An unintended consequence of increased consumption of fresh and bagged produce, however, is an increase in illnesses and outbreaks, including some multistate and multicountry outbreaks. Some of the higher profile outbreaks have been caused by E. coli O157:H7–contaminated leafy vegetables, in addition to outbreaks caused by Salmonella-contaminated tomatoes, cantaloupe, and other produce items. Investigations of some of these outbreaks have led some to conclude that contamination occurred probably in the field, i.e., preharvest contamination (CalFERT 2007a,b, 2008; Hedberg and others 1999; Gupta and others 2007; Greene and others 2008; Castillo and others 2004).

The leafy green outbreaks appear not to be associated simply with an increase in consumption. Leafy green consumption between 1996 and 2005 increased 9% compared to the previous decade, but outbreaks associated with leafy greens increased 38.6%, with a majority of them caused by E. coli O157:H7 (Herman and others 2008). Outbreaks associated with these commodities occurring since 2000 have led to proposals and active studies to identify the risk factors that may enhance preharvest contamination of produce. However, no single risk factor can explain these multiple outbreaks associated with different production environments, processes, produce items, and pathogens. Rather, it is probable that a convergence of multiple dynamic events involving more than one factor are required to cause major, noticeable outbreaks. Each outbreak may be caused by one or more events different from other outbreaks, even though some common factors are suspected, such as the probable source (e.g., livestock, wild animal) and mechanisms of transport from a source to a field (e.g., watersheds, animal intrusions, aerosols). However, the mechanisms of survival of pathogens in complex environments, and locations and conditions where amplification of their numbers might occur, have not been well documented.

Reviews describing the sources, fate, and transport of pathogens as potential risk factors relevant to preharvest contamination have been published previously; they provide background and specific details that will be summarized in this review. Studies of the incidence and fitness of E. coli O157:H7 and Salmonella in the produce production environment associated with leafy vegetables, tomatoes, and cantaloupes will be emphasized since they have been associated with multiple outbreaks suspected of being caused by preharvest contamination in the U.S. and Mexico. However, the same environmental factors described for these two pathogens and implicated commodities will apply generally to other pathogens associated with produce contamination, except for specific fitness characteristics that might be linked to a specific commodity. Information related to the incidence and survival of bacterial pathogens and fecal indicators in the production environment, and potential transport processes and risk factors associated with growing fresh produce in dynamic, agricultural regions are presented.

Outbreaks Associated with Selected Fresh Produce Commodities

An unintended consequence of the increased production and consumption of fresh produce is an increase in the number of outbreaks of foodborne illness (CSPI 2007; Sewell and Farber 2001; Sivapalasingam and others 2004). The produce items and types of pathogens associated most frequently with outbreaks in the U.S. (Sivapalasingam and others 2003) and other industrialized countries (Sewell and Farber 2001) have been reported previously, and documented in previous review articles about this subject (Nguyen and Carlin 1994; Beuchat 1996, 2006; Seymour and Appleton 2001; Harris and others 2003; Mandrell and Brandl 2004; Johnston and others 2006b). However, selected data related to outbreaks linked with fresh leafy vegetables and tomatoes will be emphasized in this review in support of the theory that multiple recent outbreaks have resulted from preharvest contamination, especially large multistate or multicountry outbreaks (Table 1.1).

The total number of cases of foodborne illness in the United States has been estimated to be approximately 76 million illnesses per year, associated with 325,000 hospitalizations and 5000 deaths (Mead and others 1999). In a recent review of outbreaks associated specifically with fresh produce, the U.S. Centers for Disease Control and Prevention (CDC) analyzing data from the CDC Foodborne Outbreak Surveillance System for 1973–1997, identified 190 outbreaks associated with produce, 16,058 illnesses, 598 hospitalizations and 8 deaths (Sivapalasingam and others 2003). An updated review by CDC of outbreaks associated specifically with leafy greens between 1973 and 2006 determined that 502 outbreaks, >18,000 illnesses, and 15 deaths occurred, with 30 of the outbreaks caused by E. coli O157:H7, 35 by Salmonella, and 196 by Norovirus (Herman and others 2008). Comparison of the numbers in these two studies reflects the fact that produce-associated outbreaks linked with a known food item increased from 0.7% of all foodborne outbreaks in the 1970s to 6% in the 1990s and has increased further to the present.

Table 1.1. Selected outbreaks associated with enteric human pathogens and fresh producea

The bacterial, viral, and protozoal pathogens associated with fresh produce outbreaks (number of outbreaks) in the U.S. between 1973 and 1997 include the following: Salmonella (30 outbreaks), E. coli O157:H7 (13), non-O157 E. coli (2), Shigella (10), Campylobacter (4), Bacillus cereus (1), Yersinia enterocolitica (1), Staphylococcus aureus (1), Hepatitis A (12), Norovirus (9), Cyclospora cayetanensis (8), Giardia lamblia (5), and Cryptosporidium parvum (3); an additional 87 outbreaks were documented without any etiology identified (Sivapalasingam and others 2003). The produce items implicated most frequently in outbreaks are “salad” lettuce, seed sprout, melon and cantaloupe (Sivapalasingam and others 2003).

Multiple sprout outbreaks of S. enterica and E. coli O157:H7 illness occurring worldwide have been associated usually with sprouts (e.g., alfalfa, mung bean, radish) grown from contaminated seed (Michino and others 1999; Breuer and others 2001; Mahon and others 1997; Proctor and others 2001; Mohle-Boetani and others 2009). The seeds are harvested in different parts of the world (e.g., U.S., Australia, China) under agricultural conditions that in many cases are not controlled well for microbial safety, considering the eventual ready-to-eat product to be produced. The sprouting process involves ideal conditions for enriching even a small concentration of pathogen that may contaminate even a small proportion of the seeds. These conditions emphasize again the importance of the quality of the preharvest environment to produce production at every step of the production cycle, including seed and transplant production, harvesting, and the fields prior to and following harvest (water, fertilizers, crop debris, human and animal visits). Contaminated seeds are not a major risk factor probably in the nonsprout outbreaks to be documented further here; however, seeds should be appreciated as an early preharvest control point in fresh produce production.

Preharvest contamination is suspected in numerous outbreaks associated with leafy vegetables (lettuce and spinach), tomatoes, cantaloupes, and possibly other commodities (e.g., jalapeño peppers, April–July, 2008). For U.S.-grown leafy vegetables alone, there have been more than 20 foodborne outbreaks since 1995 linked to contamination by E. coli O157:H7, resulting in at least 600 reported illnesses and 5 deaths. Since 2000, at least 12 outbreaks have been linked to Salmonella contaminated tomatoes (>1600 cases) and 3 outbreaks linked to Salmonella contaminated cantaloupes (72 cases) (Table 1.1). It is worth noting that, during the final preparation of this review, a major ongoing outbreak of Salmonella in St. Paul is associated with jalapeño peppers grown in Mexico and distributed by a company in Texas occurred (CDC 2008b). This was the first reported outbreak associated with this food item; however, additional details will be required to determine whether the contamination occurred on the farm or postharvest (packinghouse). Several outbreaks suspected of being associated with preharvest contamination of tomatoes, lettuce, and carrots by Shigella and Yersinia species also occurred (Table 1.1). These outbreaks have been listed to emphasize some emerging produce-pathogen issues of concern: preharvest contamination, pathogen persistence and/or fitness in the environment, and diversity of pathogens implicated depending upon local growing conditions (Table 1.1; e.g., leafy vegetables—Western U.S./Sweden/Italy, tomatoes—Eastern U.S., cantaloupe—Mexico, Yersinia—Finland).

Previous epidemiological studies of fresh produce outbreaks often lacked definitive evidence of the source of contamination and a step within the food production and processing chain where contamination could have occurred. However, traceback investigations of E. coli O157:H7–leafy vegetable outbreaks determined that 12 of them were linked probably to commodity grown on farms in the Salinas Valley, a region located on the Central Coast of California, and the major supplier of fresh produce to the U.S. market (Table 1.1; see references for additional details). Indeed, baby spinach linked to a large multistate outbreak of E. coli O157:H7 in the late spring of 2006 was grown in a valley adjacent to the Salinas Valley (CalFERT 2007b; Cooley and others 2007). Similarly, recurrent outbreaks associated with tomatoes were suspected of being grown on farms in Virginia and Florida, and outbreaks with cantaloupes on farms in Mexico (Table 1.1).

Produce outbreaks linked to a region where a large amount of fresh produce is grown is logical; however, a number of factors revealed by recent outbreak investigations are relevant to concepts of where, when, and how contamination occurs. As noted, outbreaks have been associated with commodities grown in the same region and with preharvest contamination rather than later in the distribution chain (e.g., transport or restaurant). Also, pathogen strains of the same serovar could be isolated from watersheds in the vicinity of implicated fields, and for the first time in recent outbreak investigations, E. coli O157:H7 and Salmonella strains indistinguishable from the clinical outbreak strains were isolated from environmental samples (CalFERT 2007b, 2007c, 2008; Cooley and others 2007; Greene and others 2008). Therefore, accurate information about the fate and transport processes relevant to contamination processes and the fitness of pathogens near, on, or in produce plants in the field is critical for developing strategies for minimizing preharvest contamination of produce.

Incidence of Human Pathogens on Fresh Produce

How often are produce items contaminated with pathogens? The incidence is very low generally, but any amount may be too much considering the low infectious dose for some of the pathogens, especially E. coli O157:H7 on raw produce. The incidence of major foodborne pathogens on different items of fresh produce and in animal hosts has been reported in numerous studies, in addition to data relevant for assessing the survival and fitness of pathogens in agricultural environments such as manure, water, and soil. These data are relevant to consider also for identifying potential point sources and transport processes of pathogens in production environments linked to outbreaks.

Beuchat published in 1996 one of the first and best reviews of reported incidence of common foodborne pathogens on ready-to-eat vegetables, and the potential sources of the pathogens and mechanisms of contamination (Beuchat 1996). The incidence, growth, and survival of foodborne pathogens in fresh and processed produce has been reported also in comprehensive reviews by Nguyen-the and Carlin (Nguyen-the and Carlin 2000) and Harris and others (see Tables I-1 to I-7 in Harris and others 2003), and other recent reviews (Johnston and others 2006b; Beuchat 2006; Mandrell and Brandl 2004). Although distinctions between pre- and postharvest contamination are not provided generally, these reviews provide useful summaries of the different methods for isolating pathogens—for example, Salmonella, Listeria, Yersinia, Campylobacter species, E. coli O157:H7, and generic E. coli—from multiple types of produce items that were grown in different regions of the world.

The incidence of pathogens reported in these separate studies often was between 0 and <10% of all samples tested, with an occasional incidence of >20% reported (Nguyen-the and Carlin 1994; Harris and others 2003; Mandrell and Brandl 2004). Moreover, in the few studies reporting the concentration of pathogen per gram of produce, the levels were low in most studies, even for generic E. coli, as a measure of possible fecal contamination. For example, the percentages of positives out of 774 total samples tested for Salmonella on leafy vegetables or salad in eight separate studies were 0 (0/151), 0 (0/63), 0.6 (1/159), 0.9 (1/116), 3.5 (2/57), 6.3 (5/80), 7.1 (2/28), and 68% (82/120) (Harris and others 2003). In contrast, all 214 samples of lettuce or salad mix tested for E. coli O157:H7 in large U.K. and U.S. studies were negative (Harris and others 2003). Of >3,800 ready-to-eat salad vegetables from retail markets sold in the U.K., only 0.2% were positive for Salmonella; an additional 0.5% were considered of poor quality due to contamination with E. coli or L. monocytogenes at >100 CFU per g of product (Sagoo and others 2003). A survey of “minimally processed ” vegetables in Brazil determined that 4 of 181 samples (2.2%) were contaminated with Salmonella (Froder and others 2007). Similarly, 180 fresh vegetable samples surveyed in South Africa identified 4 (2.2%) contaminated with E. coli O157:H7, and reported levels of E. coli O157:H7 as high as 1,600,000 CFU/g of spinach (Abong’o and others 2008). These results reflect the tremendous diversity of produce quality depending upon spatial and temporal factors, and possibly methodological factors.

Multiple outbreaks of Salmonella illness associated with tomatoes have occurred recently, but surveys of tomatoes for the incidence of pathogens have been limited. Of 123 samples of domestic (U.S.) tomatoes tested by the U.S. FDA-CFSAN starting in May, 2001, none were positive for Salmonella or E. coli O157:H7 (FDA-CFSAN 2001b); also, 0/20 imported tomato samples collected starting in March, 1999 were negative for both pathogens (FDA-CFSAN 2001a). However, 11 of 151 imported and 4 of 115 domestic cantaloupe samples in the same surveys were positive for Salmonella or Shigella. These results appear consistent with the fact that multiple outbreaks occurred in 1997, 2000, 2001, and 2002 due to Salmonella-contaminated cantaloupe imported from Mexico (Table 1.1). A large survey of cantaloupe and environmental samples from six farms and packing plants in South Texas and three farms in Mexico resulted in 5/950 and 1/300 cantaloupes positive for Salmonella, respectively (Castillo and others 2004). Irrigation-related samples of cantaloupe production (e.g., water source, tank, in field) revealed a higher incidence of Salmonella for both Texas and Mexico farms: 13/140 (9.2%) and 10/45 (22.2%), respectively, compared to the commodity. Moreover, generic E. coli was isolated at significant levels from some of the samples of Texas and Mexico cantaloupe (3.9%, 25.7%) and Texas and Mexico irrigation water (22.8% and 31.1%, respectively) (Castillo and others 2004). It is noteworthy that none of the 150 field and prewash cantaloupes from Mexico were positive for E. coli, compared to 39/75 (52%) and 38/75 (51%) positive samples for the postwash and packed cantaloupe, respectively. Although the concentrations of Salmonella and generic E. coli in these samples were not reported, these results reflect a prevalence of fecal contamination of water sources (well, river, aquifer, canal, dam), suggesting they may be sources of both pre- and postharvest contamination. Fecal contamination of postharvest processing water is an obvious potential source of cross-contamination of cantaloupes (Castillo and others 2004).

The fitness characteristics of pathogens in the environment are important for their long-term survival and exposure to produce. The long-term persistence in the environment of some foodborne pathogen strains is exemplified by a strain of S. Enteritidis implicated in at least one major outbreak, and possibly a minor outbreak, associated with raw almonds in 2000/01 (Isaacs and others 2005) and 2005/06 (Ledet Muller and others 2007), respectively. The S. Enteritidis outbreak strain, subtyped as phage type 30, was isolated from a suspect orchard at multiple times over at least a 5-year period, and with increasing frequency in samples collected during and following harvests (Aug–Dec) and following rain events (Uesugi and others 2007). Salmonella strains isolated during the 5-year study were all phage type 30 and indistinguishable from the clinical outbreak strains (or one band difference) by two-enzyme pulsed field gel electrophoresis (PFGE) analysis. Although it was probable that almonds became contaminated by pathogens present in soil/dust where almonds were dropped and then harvested by sweepers, the original source of the outbreak-related strain was never identified, nor were any suspect practices (Uesugi and others 2007).

The extended persistence of any pathogens in an agricultural environment, especially strains that have the potential to cause an outbreak, raises questions relevant to other produce-related outbreaks. Is contamination periodic and cumulative or due to major isolated contamination events? Do persistent strains reflect selection and evolution of special fitness characteristics in a specific environment (e.g., orchard environment; almond, leafy vegetable, tomato surface)? Is the incidence or concentration of pathogens greater now than in the past? Does pathogen survival at low concentrations in harsh soil conditions (dry, high UV) with subsequent resuscitation/amplification (rain/moisture, low UV) relate to virulence? Do certain wildlife species (e.g., mammalian, avian, amphibian) become colonized and high shedders of pathogen and associated with persistent contamination? These and other questions stimulated by recent outbreaks are difficult to answer, but they assist in focusing on areas for further research.

Incidence of Generic E. coli on Produce

Increased concerns in the U.S. and other countries about produce-associated outbreaks (Table 1.1) have stimulated initiation of multiple surveys of fresh produce for selected pathogens, and also surveys of the incidence of generic E. coli as an indicator of fecal, and potential pathogen, contamination. The results from some of these studies, including recent surveys, are presented to indicate the general microbiological quality of different types of produce grown in different regions conventionally or organically, and tested at different stages of the pre- and postharvest cycle.

A survey of produce items (e.g., arugula, cantaloupe, cilantro, parsley, spinach) collected between November 2000 to May 2002 from 13 farms in the southeastern U.S. revealed E. coli levels ranging from 0.7 to 1.5 log CFU/g for field or packing-shed produce (Johnston and others 2005). All samples were negative for L. monocytogenes and E. coli O157:H7; however, 3 of 398 samples tested for Salmonella were positive (0.7%). A similar survey by the same investigators comparing produce grown in the southern U.S. and Mexico involved testing 466 produce items obtained from packing sheds between November 2002 and December 2003. Levels of E. coli ranged between 0.7–1.9 and 0.7–4.0 log CFU/g for Mexican and southeastern U.S. produce, respectively (Johnston and others 2006a). All samples were negative for E. coli O157:H7, Salmonella, and Shigella; however, three domestic cabbage samples were positive for L. monocytogenes (0.6% of total produce samples; 7% of cabbage samples).

A variety of fresh produce items grown conventionally or organically on farms in Minnesota were picked between May and September 2002 and surveyed for microbiological quality (Mukherjee and others 2004). E. coli incidence was 4.3, 11.4, and 1.6% for 117 certified organic, 359 noncertified organic, and 129 conventional produce items, respectively, and the average E. coli counts for the positive samples was reported as 3.1 log MPN/g. The E. coli incidence was sixfold higher on organic versus conventional produce and 2.4-fold higher on produce from farms using cattle manure compared to farms using other types of manure. Noncertified organic lettuce had the highest incidence (12/39, 30.8%) for any item with more than 10 samples tested (Mukherjee and others 2004).

The microbiological quality of ready-to-eat produce has been surveyed in other parts of the world. In a study of leafy salads collected from retail markets in Brazil, >85% of 181 samples were reported to have >4 logs Enterobacteriaceae per g (Froder and others 2007). Leafy vegetable salads collected postpreparation from 16 university restaurants in Spain yielded 26% positive for E. coli (Soriano and others 2001). In contrast, only one (lettuce) of 50 produce items collected from retail and farmers markets in Washington, D.C. was positive for E. coli (Thunberg and others 2002). These results suggest major diversity in E. coli incidence depending upon the size, time, and location of the study, and possibly differences in the sensitivity of methods.

A study initiated by the USDA Agricultural Marketing Service in 2002 and coordinated with state and other federal agencies to survey the microbial quality of fresh produce items available at terminal markets and wholesale distribution centers continues as of 2008 (USDA-AMS-MDP 2008). The cumulative results over 6 years, with approximately 65,000 samples analyzed to date, provides a significant data set for analyzing spatial, temporal, and other factors related to produce contamination using E. coli incidence as the measure of fecal contamination. Multiple commodities, both domestic and imported, have been tested during the program (e.g., cantaloupe, leaf and romaine lettuce, tomatoes, green onions, and alfalfa sprouts) for generic E. coli, E. coli “with pathogenic potential” (including E. coli O157:H7), and Salmonella. The results from tests of >59,000 samples from 2002–2007 indicate that low levels of generic E. coli are common on produce items collected at the distribution stage of the postharvest production cycle compared to levels on produce in the field (Table 1.2); however, only 1.5 to 2.7% of the samples by year were positive for E. coli at concentrations >10 MPN/ml (USDA-AMS-MDP 2008). Moreover, E. coli with pathogenic potential based on PCR results for various virulence factors, including shigatoxin 1 and 2 (Stx 1 and 2), ranged from 0.1 to 0.4% of all samples tested each year. Examples of individual produce items having a high percentage of samples positive for E. coli were cantaloupe (2004 and 2005, 26–32%), leaf and/or romaine lettuce (2004 and 2005, 25–44%), cilantro (2004 and 2005, 66–71%), and parsley (2004 and 2005, 72%) (USDA-AMS-MDP 2008); data not shown.

Table 1.2. Incidence of E. coli on selected fresh produce items obtained and tested in years 2002–2007, as part of the USDA, Agricultural Marketing Service, Microbial Data Program (USDA-AMS-MDP 2008)

A similar survey for E. coli on 1,183 produce items grown in Ontario, Canada, in 2004 resulted in a 0, 1.3, 6.5, 11.6, 4.9, and 13.4% reported incidence for tomato, cantaloupe, conventional leaf lettuce, organic leaf lettuce, cilantro, and parsley, respectively (Arthur and others 2007a). However, the concentrations of E. coli ranged from >5 to 290 CFU/g for leaf lettuce, to <5 to 7,600 and 16,000 CFU/g for cilantro and parsley, respectively. Only two samples yielded a potential pathogen: S. Schwarzengrund in a sample each of Roma tomato and organic leaf lettuce (Table 1.2) (Arthur and others 2007a).

Finally, a recent study of 100 domestic bagged cut spinach and lettuce mixes (conventional and organic) for total bacterial, coliform, and E. coli counts reported means of 7.0 to 7.7 log CFU/g, <0.5 to >4.0 log MPN/g and 3 to 9.2 MPN/g (16% of samples), respectively, depending upon the product; 12.1% conventional and 16.6% organic spinach and 23.1% conventional and 6.3% organic lettuce mix samples were positive for E. coli (Valentin-Bon and others 2008). These results for bagged leafy greens from retail markets are consistent with surveys of ready-to-eat produce in the U.S. and other countries noted above, and other surveys reporting relatively high incidences of E. coli in specific produce items such as lettuces, parsley, and cilantro (Soriano and others 2001; Froder and others 2007; USDA-AMS-MDP 2008).

Significant correlations between the levels of E. coli contamination of produce and incidences of major bacterial enteric pathogens are lacking. Thus, E. coli incidence can be considered simply an indicator of potential minor or major preharvest contamination, and a risk factor for additional postharvest contamination, cross-contamination during washing, or amplification of bacteria (pathogen) during transport and storage. E. coli incidence serves as a moderately effective measure of changes in fecal microbial flora during the produce production and processing cycle, and for assessing the potential for pathogenic strains, if they were to be present, to survive under the same produce processing conditions. The concentration of E. coli may be a more relevant indicator of the risks associated with human consumption of a contaminated produce item.

Evidence of fecal contamination as high as 50–70% on some produce items does not correlate necessarily to a higher incidence of illness, unless undetected sporadic illness is occurring. Although major outbreaks are of concern, it should be emphasized that relative to the number of consumptions of ready-to-eat produce (and tree nuts) (many billions), outbreaks are not frequent, causing an extremely low number of known total cases per total consumptions; however, some cases are sporadic probably and never linked to a food source. Nevertheless, vigilance and research are important to identify what is probably a rare convergence of events and/or specific circumstances that result in a major outbreak of disease, some of it severe, and thus, a noticeable event. The relatively low incidence of pathogens on produce measured in surveys seems consistent with the speculation that incidence is very rare and occurs only after multiple unusual circumstances that result also in an outbreak. Surveys of produce are informative because they provide a measure of the background incidence of indicators of fecal contamination and pathogens related to dynamic spatial, temporal, and geographic factors. Incidence in the absence of illness or outbreaks also is informative.

Animal Sources of Enteric Foodborne Pathogens Relevant to Produce Contamination

Carriage of pathogens by food animals is a critical factor relevant to many outbreaks associated with produce, meat, milk, and other food products. Evidence for the colonization of cattle (Elder and others 2000; Hussein and Bollinger 2005; Fegan and others 2005; Low and others 2005; Dargatz and others 2003), swine (Chapman and others 1997; Jay and others 2007), sheep (Ogden and others 2005), poultry (Chapman and others 1997; Rose and others 2002; Foley and others 2008; McCrea and others 2006), and multiple species of wild animals (Ejidokun and others 2006; Hernandez and others 2003; Kirk and others 2002; Sargeant and others 1999; Pritchard and others 2001; Wetzel and LeJeune 2006) by E. coli O157:H7, S. enterica, and C. jejuni (Miller and Mandrell 2006) has been documented. Pathogen colonization of livestock and wild animals is a dynamic process depending upon how and when pathogens are encountered in the environment (food, grass, water), pathogen fitness in the environment and animal GI tracts (viability, dose), animal contact/commingling and movement, immunity, and fecal shedding. In addition, there are unknown factors that might enhance or diminish pathogens in particular environments, for example, weather conditions, feed, predation, or antimicrobials. One or more of these factors may be important in initiating or contributing to the size of an outbreak.

Studies documenting the incidence of E. coli O157:H7 and Salmonella in animals are summarized in Table 1.3. Details regarding the methods, periods, locations, and samples studied can be obtained from the original papers cited.

E. coli O157:H7 and Non-O157 STEC

Cattle are major carriers of E. coli O157, non-O157 shigatoxin-positive E. coli (STEC), S. enterica and C. jejuni strains (Table 1.3). Strains of the same serovars as those associated with produce outbreaks have been isolated frequently from cattle. Similarly, sheep, pigs, chickens, and turkeys are common or intermittent carriers of these pathogens, and a variety of wildlife species carry these pathogens or related pathogens (Tables 1.1 and 1.3). For example, E. coli O157:H7 and nonO157 STEC strains have been isolated from deer (Keene and others 1997; Sargeant and others 1999; Fischer and others 2001; Dunn and others 2004; Renter and others 2006), feral swine (Jay and others 2007), pigeons (Morabito and others 2001), seagulls (Makino and others 2000), starlings, horses, dogs (Hancock and others 1998), barn flies (Keen and others 2006), and slugs (Sproston and others 2006). Salmonella has been isolated from deer (Branham and others 2005; Renter and others 2006), badgers (Nielsen and others 1981), wild mice (Tablante and Lane 1989), wild turtles and tortoises (Hidalgo-Vila and others 2007), and a variety of wild birds (Fenlon 1981; Wahlstrom and others 2003; Hughes and others 2008). The concentration of pathogen in wildlife samples is not well documented; thus, the shedding status of wildlife compared to livestock is unclear. Moreover, the quantity of feces shed by different species of wildlife per animal or for a population in a region is unknown, so data relevant to the total amount of pathogen disseminated by a species in any spatial and temporal context also are unknown. The amount of pathogen shed by an animal is extremely relevant epidemiologically for identifying potential sources of pathogen and relevant risk factors for contamination of produce (Chase-Topping and others 2007).

Table 1.3. Selected studies reporting incidence of E. coli O157, S. enterica, and C. jejuni in livestock and wild animal feces

The incidence data listed in Table 1.3 are from selected recent studies; the data reflect the dynamic nature of the incidence associated with different animal hosts, spatial and temporal differences, and a variety of different methods. In a recent review by Hussein and Bollinger, 39 reported studies of the incidence of E. coli O157:H7 in thousands of cattle fecal samples from feedlots, pasture/range, and entering slaughter ranged from 0.2 to 28%, depending upon the study and the cattle feeding or production process (Hussein and Bollinger 2005). A previous review of some of the same studies involving animals in Asia, Australia, Europe, and North America (sampling periods between 1991–1999) reported incidence in fecal samples in the range of 0.1 to 62% (Duffy 2003). Indeed, the common occurrence of E. coli O157:H7 in cattle is consistent with numerous outbreaks of E. coli O157:H7 occurring as a result of direct human contact with animals, feces, or manures at fairs, farms, and other public settings (Duffy 2003; Durso and others 2005; Keen and others 2006, 2007). Similar studies of sheep in the U.K., U.S., and Spain, representing thousands of samples, reported an incidence of E. coli O157 that ranged from 0.7 to 7.3%, and for domestic pigs incidence ranged from 0.3 to 8.9% (Table 1.3).

In multiple studies of cattle feedlots and ranches, strains of E. coli O157:H7 persisted for up to 24 months at individual farms, and strains indistinguishable by molecu-lar typing methods were isolated from farms separated by up to 50 km (Rice and others 1999; LeJeune and others 2004; Wetzel and LeJeune 2006). Indeed, a link between livestock and human illness with E. coli O157:H7 and other STEC has been supported by a direct correlation reported between the density of livestock and amount of reported illness in a region of Ontario, Canada (Michel and others 1999).

Salmonella enterica

Strains of S. enterica were isolated from 1.4 to 9% of beef cow fecal samples (Australia, U.S., U.K.) reported in four studies (Table 1.3). In a recent study of 7,680 animal and environmental samples from a single U.S. dairy, 13–72% of the cattle samples (depending upon period of testing), and >50% of air, soil, water, insect, and bird feces samples yielded S. enterica (Pangloli and others 2008). Similarly, high incidences of S. enterica in pigs were reported in a U.K. study (23.4%), in poultry flocks (10.5 to 13%) in U.S. and Belgium studies, and in poultry production environmental samples (12 to 51%) in a U.S. study (Table 1.3). S. enterica has been isolated from 1 to 7% of deer samples in two studies reported and up to 3% of wild bird samples. A multidrug-resistant S. Newport strain was prevalent on two different farms for months and shed by a cow for at least 190 days (Cobbold and others 2006), and, as noted above, a strain of SE (PT30) has been isolated from almond orchard soil periodically for at least 5 years (Uesugi and others 2007).

Campylobacter Species

C. jejuni incidence in cattle, poultry, other farm animals, and wild animals has been reported and reviewed (Miller and Mandrell 2006). Although the incidence of C. jejuni reported in >20 studies is comparable or higher than those reported and listed for E. coli O157 and Salmonella in Table 1.3, few major outbreaks of C. jejuni associated with fresh produce have occurred (Mandrell and Brandl 2004). In agreement perhaps, is the absence of any isolation/detection of C. jejuni on >6,800 produce samples in recent studies reported (Sagoo and others 2001; Thunberg and others 2002; Moore and others 2002; Sagoo and others 2003), suggesting that C. jejuni may be of lesser fitness compared to E. coli O157 and Salmonella in environments relevant to fresh produce production and preharvest contamination (Brandl and others 2004). Nevertheless, high numbers of sporadic C. jejuni illnesses compared to E. coli O157 and Salmonella (MMWR 2005b, 2007b) suggest surveillance to identify food sources associated with C. jejuni illness, including produce, should be continued.

The results summarized in Table 1.3 confirm there are multiple livestock and wildlife sources of pathogens and suggest modes of transport of pathogens for contamination of fresh produce in fields or orchards. Livestock are located near produce production in many locations, but not close enough usually to be considered a major risk. However, resident wildlife species are potential sources of pathogens also, and commingle with livestock on ranches, dairies, or feedlots, thus increasing exposure of livestock and wildlife to pathogens. Wildlife colonized by pathogens will roam and potentially disseminate them to produce or other locations in the vicinity of produce (Jay and others 2007). This presents problems for controlling wildlife intrusion into fields depending upon the size and roaming capability of the species. Small mammals (e.g., squirrels, mice, raccoons), large mammals (feral swine, deer, elk), and birds illustrate the diversity of population sizes, barriers (fencing height, depth, gage), and habitat that are issues in considering interventions to control exposure of wildlife to fields. Therefore, only obvious risk factors can be addressed until definitive data are obtained about major sources of pathogen in an environment.

A few conclusions can be drawn from the selected livestock and wildlife incidence data. First, they reflect the dynamic fluctuations in the incidence of enteric pathogens that can occur and that relatively high incidence of certain pathogens may occur at specific times. Second, there appears to be a general trend in higher incidence of S. enterica strains in surveys of animal and environmental samples compared to E. coli O157:H7, a trend consistent with the general amount of illness reported for these pathogens in the U.S. and U.K. (MMWR 2005b, 2007b; CDR 2006). In contrast, the recurrent outbreaks of E. coli O157:H7, in the absence of any known Salmonella outbreaks, associated with leafy vegetables grown in the same region (Table 1.1) is inconsistent with this trend. Perhaps, a study of the incidence of Salmonella in the environment of leafy vegetable production would provide clues to explain this paradox.

High-level Shedding of E. coli O157:H7 and Salmonella by Some Animals

Measuring the prevalence of pathogens in animals and other environmental reservoirs relevant to produce production are informative, but the concentration and total amount of pathogen disseminated is perhaps more relevant to identifying potential risks in a produce production region. However, quantifying pathogen in complex samples is difficult due to the inability to survey livestock and wildlife populations comprehensively and to obtain accurate values with environmental samples containing low concentrations of pathogens in a complex microbial flora.

Cattle shedding high levels of E. coli O157:H7 in their feces have been identified in some surveys. The majority of cows positive for E. coli O157:H7 in a herd have <100 CFU/g of feces, and this usually is detectable only by preenrichment and immunomagnetic selection methods. However, high-level shedders (“super shedders”) have been identified that shed between 1,000 and 1,000,000 CFU/g of feces (Low and others 2005; Chase-Topping and others 2007). Similarly, mice shedding >108 CFU viable Salmonella cells per gram of feces have been identified in laboratory studies, and high-shedding status appeared linked directly to the health of the intestinal microflora and level of inflammation in the colon (Lawley and others 2008).