Microbiology of fruits and vegetables

Activeareas of research include incidence of human pathogen contamination, sources of microbial contamination, microbial attachment to produce surfaces, able spoilage problems, efficacy

Vegetables

A CRC title, part of the Taylor & Francis imprint, a member of the Taylor & Francis Group, the academic division of T&F Informa plc.

Edited by

Gerald M Sapers

James R Gorny Ahmed E Yousef

Fruits and Vegetables

Boca Raton London New York

Published in 2006 by

CRC Press

Taylor & Francis Group

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© 2006 by Taylor & Francis Group, LLC

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Microbiology of fruits and vegetables / edited by Gerald M Sapers, James R Gorny, Ahmed E Yousef.

Taylor & Francis Group

is the Academic Division of T&F Informa plc.

Fruits and vegetables represent an important part of the human diet, providingessential vitamins, minerals, and fiber, and adding variety to the diet In theirFood Guide Pyramid, the U.S Department of Agriculture encourages con-sumption of 3–5 servings of vegetable items, and 2–4 servings of fruit items perday In today’s global economy, fresh fruits and vegetables are available yearround

In the U.S and other technologically advanced countries, high-quality freshand processed fruits and vegetables are widely available Fresh-cut fruitsand vegetables represent a large and rapidly growing segment of the freshproduce industry These commodities have an excellent safety record withrespect to incidence of foodborne illness Nevertheless, surveillance statisticscompiled by the U.S Centers for Disease Control and Prevention indicate thatsignificant and increasing numbers of outbreaks have been associated withfresh fruits and vegetables, or their products The presence of human patho-gens in fresh produce is borne out by U.S Food and Drug Administrationproduct recall data, and by microbiological surveys of domestically producedand imported commodities Increased recognition of a food safety problemwith produce may reflect greater consumption of fruits and vegetables,more frequent eating out, greater reliance on imports of out-of-season fruitsand vegetables from ‘‘third world’’ producers, and improved surveillance andreporting methods by public health agencies

In addition to safety concerns, microbial spoilage of fresh produce sents a source of waste for consumers, and an economic loss to growers,packers, and retailers Post-harvest decay, bacterial soft rot, and microbialspoilage of fresh-cuts and processed juices are continuing problems

repre-In recent years, extensive research has been conducted on microbiologicalproblems relating to the safety and spoilage of fruits and vegetables Activeareas of research include incidence of human pathogen contamination, sources

of microbial contamination, microbial attachment to produce surfaces, able spoilage problems, efficacy of sanitizing treatments for fresh produce,novel interventions for produce disinfection, and methodologies for micro-biological evaluation of fruits and vegetables

intract-In this book, we have attempted a comprehensive examination of thesetopics, focusing on issues, rather than attempting an encyclopedic compilation

of information about all commodities, classes of microorganisms, or categories

of spoilage We have not included certain topics, such as preharvest diseases ofproduce or production of fermented vegetables, which are adequately covered

elsewhere We have selected chapter authors who are active researchers in theirrespective fields, and thus bring a working knowledge of current issues,industry practices, and advances in technology.

The book is divided into five sections: (I) Contamination and State ofMicroflora on Fruits and Vegetables; (II) Microbial Spoilage of Fruits andVegetables; (III) Food Safety Issues; (IV) Interventions to Reduce Spoilageand Risk of Foodborne Illness; and (V) Microbiological Evaluation of Fruitsand Vegetables Within each section we have grouped chapters that coverspecific issues related to the overall topic For example, Section I containschapters on sources of microbial contamination, attachment of microorgan-isms to fresh produce, internalization and infiltration of microorganisms inproduce, and stress adaptation by microorganisms and safety of produce

I wish to thank the individual chapter authors for the authoritativeand comprehensive coverage of their respective topics, and my co-editors,

Dr James R Gorny and Dr Ahmed E Yousef, for their assistance indeveloping the concept and organizational structure of the book, identifyingsuitable chapter authors, reviewing the completed chapters, and helping meassemble the manuscripts into a form suitable for publication I also thankSusan Lee, Food Science Editor at Dekker/CRC Press and her editorial stafffor their guidance, invaluable help, and patience in working with us on thisproject I thank my employer, the USDA Agricultural Research Service’sEastern Regional Research Center, for allowing me the time, and providingthe resources, that enabled me to participate in this project Finally, I mustthank my wife for her unlimited patience and understanding during themany long hours when I was attached to the computer and unavailable to meether needs

Gerald M Sapers

Gerald M Sapers received his Ph.D in food technology from MIT in 1961 Hejoined the USDA’s Eastern Regional Research Center (ERRC) in 1968, after 2years at the U.S Army Natick Laboratories, and 6 years in private industry

He has conducted research on dehydrated potato stability, apple volatiles,safety of home canned tomatoes, utilization of natural pigments, pigmentation

of small fruits, cherry dyeing, control of enzymatic browning in minimallyprocessed fruits and vegetables, mushroom washing, and microbiologicalsafety of fresh produce, which is his current area of research He has been aLead Scientist at ERRC since 1991 Dr Sapers has published 110 scientificpapers, 3 book chapters and 5 patents He is an active member of the Institute

of Food Technologists’ Fruit and Vegetable Products Division, and theInternational Fresh-cut Produce Association

James R Gorny received his Ph.D in plant biology from the University ofCalifornia, Davis, and his M.S and B.S degrees in food science fromLouisiana State University in Baton Rouge He is currently vice president ofTechnology and Regulatory Affairs for the International Fresh-cut ProduceAssociation, and has been the author and editor of numerous scientificpublications including: Editor-In-Chief of the IFPA Food Safety Guidelinesfor the Fresh-cut Produce Industry and a contributor to the chapter on

‘‘Produce Food Safety’’ in the recently revised U.S Department of AgricultureHandbook 66 His research has focused on the effects of modified atmos-pheres on the quality and safety of whole and fresh-cut fruit produce Hehas been actively involved in the fresh-cut produce industry since 1986, andhas worked extensively as a consultant on food safety, packaging, qualityassurance, operations, and general management issues, both nationally andinternationally

Ahmed E Yousef received his Ph.D in food science from the University

of Wisconsin (UW)-Madison in 1984 Subsequently, he served as a doctoral researcher at the Department of Food Science and the Department

post-of Food Microbiology and Toxicology, UW Dr Yousef joined The OhioState University (OSU) as an assistant professor in 1991 At OSU, Dr Yousefinvestigated food biopreservation using bacteriocins, explored new applica-tions of ozone in food processing, and addressed the safety of foods processed

by novel technologies such as pulsed electric field, high pressure processingand ohmic heating He is currently a professor at the Department of Food

Science and Technology and the Department of Microbiology, teachingthe main food microbiology course at OSU Dr Yousef has published

2 books, 10 book chapters, and 70 scientific papers and review articles, and apatent He is an active member of the Institute of Food Technologists, theAmerican Society for Microbiology, and the International Association of FoodProtection

Bassam A Annous

Eastern Regional Research Center

Agricultural Research Service

U.S Department of Agriculture

Department of Food Science

Pennsylvania State University

University Park, Pennsylvania

Larry R Beuchat

Center for Food Safety

Department of Food Science and

Technology

University of Georgia

Griffin, Georgia

Maria T Brandl

Western Regional Research Center

Agricultural Research Service

U.S Department of Agriculture

Albany, California

F Breidt, Jr

Agricultural Research Service

U.S Department of Agriculture

and Department of Food Science

North Carolina State University

Raleigh, North Carolina

Naveen ChikthimmahDepartment of Food SciencePennsylvania State UniversityUniversity Park, PennsylvaniaPascal Delaquis

Food Safety and QualityAgriculture and Agri-Food CanadaSummerland, British Columbia,Canada

Mary Ann Dombrink-KurtzmanNational Center for AgriculturalUtilization Research

Agricultural Research ServiceU.S Department of AgriculturePeoria, Illinois

Elazar FallikDepartment of Postharvest Sciences

of Fresh ProduceARO-The Volcani CenterBet-Dagan, Israel

William F FettEastern Regional Research CenterAgricultural Research ServiceU.S Department of AgricultureWyndmoor, Pennsylvania

Daniel Y.C FungDepartment of Animal Sciences andIndustry

Kansas State UniversityManhattan, Kansas

Western Regional Research Center

Agricultural Research Service

U.S Department of Agriculture

U.S Food and DrugAdministrationSummit Argo, Illinois

Michael F KozempelEastern Regional Research CenterAgricultural Research ServiceU.S Department of AgricultureWyndmoor, Pennsylvania

Ching-Hsing LiaoEastern Regional Research CenterAgricultural Research ServiceU.S Department of AgricultureWyndmoor, Pennsylvania

Richard H LintonCenter for Food Safety EngineeringPurdue University

West Lafayette, Indiana

Robert E MandrellWestern Regional Research CenterAgricultural Research ServiceU.S Department of AgricultureAlbany, California

Pamela G MarroneAgraQuest, Inc

Davis, California

Julien MercierAgraQuest, Inc

Davis, California

Arthur J MillerU.S Food and DrugAdministrationCenter for Food Safety andApplied Nutrition

College Park, Maryland

J.-M Monier

Laboratoire d’Ecologie Microbienne

Universite´ Claude Bernard Lyon 1

Center for Food Safety

Department of Food Science and

Eastern Regional Research Center

Agricultural Research Service

U.S Department of Agriculture

Wyndmoor, Pennsylvania

Travis L SelbyDepartment of Food SciencesPurdue University

West Lafayette, Indiana

Charles R SterlingDepartment of Veterinary Scienceand Microbiology

University of ArizonaTucson, Arizona

Dike O UkukuEastern Regional Research CenterAgricultural Research ServiceU.S Department of AgricultureWyndmoor, Pennsylvania

B.G WernerDepartment of Food SciencesCornell University

Ithaca, New York

Ahmed E YousefDepartment of Food Science andTechnology

The Ohio State UniversityColumbus, Ohio

SECTION I Contamination and State of Microflora

on Fruits and Vegetables

Mary Ann Dombrink-Kurtzman

Chapter 14

Safety of Minimally Processed, Acidified, and Fermented

Vegetable Products 313

F Breidt, Jr

SECTION IV Interventions to Reduce Spoilage and

Risk of Foodborne Illness

Chapter 15

HACCP: A Process Control Approach for Fruit and Vegetable Safety 339William C Hurst

Chapter 16

Effect of Quality Sorting and Culling on the Microbiological

Quality of Fresh Produce 365Susanne E Keller

SECTION V Microbiological Evaluation of Fruits

and Vegetables

Chapter 24

Sampling, Detection, and Enumeration of Pathogenic and

Spoilage Microorganisms 543Larry R Beuchat

Chapter 25

Rapid Detection of Microbial Contaminants 565Daniel Y.C Fung

Chapter 26

Methods in Microscopy for the Visualization of Bacteria and

Their Behavior on Plants 595Maria T Brandl and J.-M Monier

Index 621

Section I

Contamination and State of Microflora on Fruits and Vegetables

1 Microbial Contamination of Fresh Fruits

and Vegetables

Jim Gorny

CONTENTS

1.1 Introduction 4

1.2 Produce Contamination 5

1.3 Microorganisms of Concern 7

1.4 Incidence and Association of Human Pathogens with Produce 8

1.4.1 FDA Imported Produce Survey 8

1.4.2 FDA Domestic Produce Survey 9

1.4.3 USDA Microbiological Data Program (MDP) 10

1.4.4 Produce-Associated Foodborne Illness Traceback Investigation Results 12

1.5 Potential Sources of Produce Contamination by Human Pathogens 13

1.5.1 Food Safety Risk Factors Associated with Production of Fresh Produce 13

1.5.1.1 Land Use 14

1.5.1.2 Soil Amendments 14

1.5.1.3 Wild and Domestic Animal Control 14

1.5.1.4 Irrigation Water 15

1.5.1.5 Harvest Operations 15

1.5.2 Food Safety Risk Factors Associated with Postharvest Handling of Produce 16

1.5.2.1 Employee Hygiene 16

1.5.2.2 Equipment 16

1.5.2.3 Wash and Hydrocooling Water 17

1.5.2.4 Cold Storage Facilities 17

1.5.2.5 Packaging Materials 18

1.5.2.6 Modified Atmosphere Packaging of Fresh Produce 18

3

1.5.2.7 Refrigerated Transport, Distribution, and

Cold Storage 19

1.5.3 Food Safety Risk Factors Associated with Foodservice, Restaurant, and Retail Food Stores Handling of Produce 20

1.5.4 Consumer Handling of Produce from Purchase to Plate 21

1.6 Effective Management Strategies: Contamination Prevention and Intervention 21

1.6.1 Good Agricultural Practices (GAPs) 22

1.6.2 Current Good Manufacturing Practices (cGMPs) 23

1.6.3 Hazard Analysis Critical Control Point (HACCP) 24

1.7 Research Needs 25

1.7.1 Microbial Ecology of Human Pathogens in the Agricultural Production Environment 26

1.7.2 Agricultural Water 26

1.7.3 Soil Amendments 26

1.7.4 Proximity Risk of Potential Contaminant Sources 27

1.7.5 Intervention Strategies to Reduce the Risk of Human Pathogen Contamination of Fresh Produce 27

1.8 Summary 27

References 28

1.1 INTRODUCTION

Fresh fruits and vegetables are perceived by consumers to be healthful and nutritious foods because of the plethora of scientifically substantiated and documented health benefits derived from consuming fresh fruits and vegetables [1] However, recent foodborne illness outbreaks in the U.S and throughout the world have been increasingly linked epidemiologically to consumption of fresh fruits, vegetables, and unpasteurized juices These incidents have caused growers, shippers, fresh-cut produce processors, distributors, retailers, import-ers, and government public health officials to re-evaluate the risk of con-tracting foodborne illness from consumption of fresh fruits and vegetables and to re-evaluate current production and handling practices

While the probability of contracting a foodborne illness via consumption

of fresh fruits or vegetables is very low, a small probability does exist Because fresh fruits and vegetables are often consumed uncooked so that there is

no ‘‘kill’’ step, prevention of produce contamination with human pathogens

is the only practical and effective means of ensuring that these food pro-ducts are wholesome and safe for human consumption This means that a complete supply chain approach to prevent contamination at any point in the produce continuum is essential to ensuring public health by minimizing the incidence of foodborne illness associated with produce consumption Ensuring

the integrity of produce from field to fork is the responsibility of everyone inthe produce continuum, including growers, shippers, processors, distributors,retailers, and consumers It must also be remembered that the health benefitsderived from eating at least five servings of fresh fruits and vegetables dailyfar outweigh the very small probability of contracting a foodborne illness.

A meaningful assessment of the risk associated with contracting afoodborne illness from consumption of fresh fruits and vegetables involvesunderstanding the microbiology of fresh fruits and vegetables as well as fieldproduction, processing, and handling practices As such, the fresh produceindustry is extraordinarily diverse and complex in the number of productsproduced, how the products are grown and handled, and the geographicareas from which these products are sourced A typical retail grocer in NorthAmerica will have available on a daily basis upwards of 300 differentproduce items for sale The morphological characteristics of a produce itemmay also contribute to its propensity for contamination, since produceitems may be derived from the leaves, stems, stalks, roots, fruits, and flowers

of plants Because the produce continuum represents such diversity, it isonly possible to describe broad generalities about current practices of theproduce continuum and the food safety risk associated with them, as anin-depth analysis of this plethora of products would be encyclopedic in volume

1.2 PRODUCE CONTAMINATION

Contamination of fruits and vegetables by human pathogens can occuranywhere in the farm to table continuum including contamination of seedstocks and during production, harvesting, postharvest handling, storage,processing, transport distribution, retail display, and/or preparation (food-service or home) Produce contaminated with human pathogens cannot becompletely disinfected by washing or rinsing the product in an aqueoussolution, and low sporadic levels of human pathogens can be found on pro-duce [2,3] In 2004 the Alliance for Food and Farming [4] analyzed Centersfor Disease Control and Prevention (CDC) data sets [5,6] and summa-rized information regarding foodborne illness outbreaks that have beenassociated with produce consumption The study’s objective was to analyzelikely sources of produce contamination and categorize the most likely placethat the contamination occurred, that being either during production/growing or during postproduction handling The ‘‘postproduction’’ categoryincluded produce-associated foodborne illnesses that were most likely due toimproper handling at the foodservice, retail, or consumer level, while the

‘‘grower’’ category included foodborne illnesses associated with produce thatwere most likely attributable to the farm, packing, shipping, or otheragricultural postharvest handling Analysis of CDC data indicated thatimproper handling of fruits and vegetables at foodservice establishments or

by consumers caused 83% of produce-associated foodborne illness outbreaks,while ‘‘grower’’-implicated cases comprised 17% of produce-associated

foodborne illness outbreaks Data from this report presented in Figure 1.1show that the percentage of ‘‘grower’’-related contamination incidents as apercent of all produce related outbreaks has been declining since 1996, and thistrend is most likely due to implementation of good agricultural practices(GAPs) by grower/shipper/packers.

The Alliance for Food and Farming 2004 report and the CDC [7] bothindicate that about 12% of foodborne illnesses occurring in the U.S between

1990 and 2001 has been associated with consumption of fresh fruits andvegetables This figure of 12% of outbreak cases associated with produceconsumption represents a greater proportion of foodborne illness burden beingrepresented by fresh fruits and vegetables than was reported in the past(Table 1.1) CDC data also indicate that produce-related outbreaks havebecome larger, involving more individuals and increasing in frequency.Foodborne illness outbreak reports related to produce consumption havemost likely increased due to:

Better detection and diagnostic methods for human pathogens whichcan epidemiologically associate produce consumption with illness(PulseNet, SODA salmonella outbreak detection algorithm, etc.)

FIGURE 1.1 Produce-associated outbreaks due to suspected farm contamination versuspostproduction handling (Adapted from Analysis of Produce Related Foodborne IllnessOutbreaks, Alliance for Food and Farming, April 2004, www.foodandfarming.info/documents/85876_produce_analysis_604.pdf.)

Increased surveillance for human pathogens by public healthagencies.

Increased per capita consumption of fresh fruits and vegetables inNorth America

Increased awareness that produce may be a potential vehicle forhuman pathogens, thus leading to increased epidemiological investi-gations of produce as a potential vector

Increased global sourcing of produce items to ensure year aroundsupply of the broad diversity of produce available in modern grocerystores

Longer postharvest storage and longer shipment times that mayalso contribute to increased potential for illness by allowing forproliferation of an initial low number of human pathogens to aninfectious or disease-causing dosage

1.3 MICROORGANISMS OF CONCERN

Harris et al [8] extensively reviewed outbreaks associated with fresh produceand reported that the most common human pathogens associated with producefoodborne illness outbreaks are: E coli O157:H7, Salmonella spp., Shigellaspp., Listeria monocytogenes, Crytosporidium spp [9], Cyclospora spp.,Clostridium botulinum, hepatitis A virus, Norwalk virus, and Norwalk-likeviruses These microorganisms can be categorized as follows:

Soil-associated pathogenic bacteria (Clostridium botulinum, Listeriamonocytogenes)

Feces-associated pathogenic bacteria (Salmonella spp., Shigella spp.,

E coli O157:H7, and others)

Pathogenic parasites (Cryptosporidium, Cyclospora)

Pathogenic viruses (hepatitis A, enterovirus, Norwalk-like viruses).Many of these pathogens are spread via a human (or domestic animal)

to food to human transmission route Handling of fruits and vegetables by

TABLE 1.1Trends in Burden: Foodborne Outbreaks Related to Fresh Produce,1973–1997

Adapted from Sivapalasingham, S., Friedman, C.R., Cohen, L., and Tauxe, R.V.,

J Food Prot 67, 10, 2004.

infected field-workers or consumers, cross contamination, use of nated water, use of inadequately composted manure, or contact with con-taminated soil are just a few of the ways that transmission of human pathogens

contami-to food can occur

Data from the CDC foodborne outbreak surveillance system show thatfrom 1988 to 1998 the two most commonly reported microorganismsassociated with fresh produce foodborne illness outbreaks were Salmonellaspp and E coli O157:H7 with 45% and 38% of the fruit and vegetable linkedoutbreaks, respectively, being attributed to these two microorganisms How-ever, recent foodborne illness outbreaks associated with produce consumptionhave been caused by viruses (hepatitis A) and parasites (Cyclospora spp.) CDCdata demonstrate that the majority of reported foodborne illnesses in theU.S are of unknown etiology and are most likely caused by viruses such asNorwalk-like viruses [10,11] Unfortunately, diagnostic tools for detectionand enumeration of viruses that may cause foodborne illnesses are severelylacking

1.4 INCIDENCE AND ASSOCIATION OF HUMAN

PATHOGENS WITH PRODUCE 1.4.1 FDA IMPORTEDPRODUCE SURVEY

In March 1999 the U.S Food and Drug Administration (FDA) initiated

a 1000-sample survey of imported fresh produce raw agricultural ties from 21 countries and included: broccoli, loose-leaf lettuce (radicchio,escarole, endive, chicory leaf, mesclun, and others), cantaloupe, celery, straw-berries, scallions/green onions, tomatoes, parsley, culantro (a herb), andcilantro [12] Loose-leaf lettuce products included radicchio, escarole, endive,chicory and others These high-volume imported fresh produce rawagricultural commodities were selected by the FDA for the importedproduce sampling assignment based on the following risk factor criteria:epidemiological outbreak data, structural characteristics of the produce item,growing conditions, processing and consumption rates Raw agriculturalcommodities are defined in the Federal Food, Drug, and Cosmetic Act as ‘‘anyfood in its raw or natural state, including all fruits that are washed, colored, orotherwise treated in the unpeeled natural form prior to marketing.’’ These rawagricultural commodities were analyzed for the presence of Salmonellaspp and E coli O157:H7 All commodities except for cilantro, culantro, andstrawberries also were analyzed for Shigella spp Produce imported fromMexico, Canada, Costa Rica, Guatemala, the Netherlands, Honduras,Belgium, Italy, Israel, Chile, Peru, Colombia, Trinidad and Tobago, NewZealand, Nicaragua, the Dominican Republic, France, Argentina, Ecuador,Haiti, and Korea were sampled Six countries provided 25 or more samples foranalysis: Mexico, Canada, Costa Rica, Guatemala, the Netherlands, andHonduras

commodi-Data presented in Table 1.2 show that of 1003 samples that were collectedand analyzed, 35 samples (3.5% of the total number of samples) were found

to have detectable levels of Salmonella spp., 9 samples (0.9% of the totalnumber of samples) were found to have detectable levels of Shigella spp., and nosamples (0%) were found to have detectable levels of E coli O157:H7 These 44samples positive for the presence of a human pathogen represent approx-imately 4.4% of the total number of product samples tested

The three produce items with the greatest incidence of pathogen tamination were cilantro, cantaloupe, and culantro, accounting for 1.6, 1.1,and 0.6%, respectively, of the overall contamination (4.4%) The remainingproduce items each contributed 0.3% or less to the overall contamination

In March 2000 the FDA initiated a 1000-sample survey of domestic freshfruit and vegetable raw agricultural commodities [13] Cantaloupe, celery,cilantro, loose-leaf lettuce, parsley, scallions (green onions), strawberries, andtomatoes were collected and analyzed for Salmonella spp and E coli O157:H7.Cantaloupe, celery, parsley, scallions, and tomatoes were also analyzed forShigellaspp This survey was the domestic complement to the FDA importedproduce survey

TABLE 1.2

Number of Samples Collected and Analyzed and the Number of SamplesConfirmed Positives for Human Pathogens Per Each Type of ImportedProduce

Produce item

No of samples

No human pathogen positive samples (% positive per produce item)

Salmonella spp.

Shigella spp.

Note: N/A ¼ not analyzed.

Adapted from FDA Survey of Imported Fresh Produce, U.S Food and Drug Administration Center for Food Safety and Applied Nutrition, Office of Plant and Dairy Foods and Beverages, January 30, 2001, www.cfsan.fda.gov/dms/prodsur6.html.

Data presented in Table 1.3 show that of 1028 domestic samples thatwere collected and analyzed, 6 samples (0.58% of the total number of samples)were found to have detectable levels of Salmonella spp., 5 samples (0.49% ofthe total number of samples) were found to have detectable levels of Shigellaspp., and no samples (0%) were found to have detectable levels of E coliO157:H7 One or more samples of cantaloupe, cilantro, lettuce, parsley, andscallions were found to have detectable levels of human pathogens.Cantaloupes had the highest number of positive samples (5), followed byscallions (3), cilantro, lettuce, and parsley (1 each).

When adjusted to account for the number of samples of each commoditycollected, scallions had the highest detectable rate of human pathogens (3.2%)

of the total 93 samples collected Cantaloupe had a 3.1% rate of detectablehuman pathogens with 5 out of 164 samples collected testing positive One of

85 cilantro samples tested positive for the presence of a human pathogen giving

a detection rate of 1.2% One of 90 parsley samples (1.1%) was found to havedetectable levels of Shigella spp and one of 142 (0.7%) lettuce samples wasfound to have detectable levels of Salmonella spp

No human pathogen positive samples (% positive per produce item)

Salmonella spp.

Shigella spp.

Note: N/A ¼ not analyzed.

Adapted from FDA Survey of Domestic Fresh Produce, U.S Department of Health and Human Services, U.S Food and Drug Administration Center for Food Safety and Applied Nutrition, Office of Plant and Dairy Foods and Beverages, January 2003, www.cfsan.fda.gov/dms/ prodsu10.html.

foodborne pathogens and indicator organisms on domestic and importedfresh fruit and vegetable raw agricultural commodities USDA’s AgriculturalMarketing Service (AMS) was appointed to undertake the program that iscurrently known as the microbiological data program (MDP) MDP wasprimarily designed to provide data on microbial presence in order to establish amicrobial baseline to assess the risks of contamination, if any, in the domesticfood supply.

In 2002 USDA MDP analyzed a total 10,317 samples of five raw cultural commodities: cantaloupe, celery, leaf lettuce, romaine lettuce, andtomatoes [14] Samples were collected in commerce at wholesale and/ordistribution centers, and 86% of the samples came from domestic sources;11% of the samples were imported; and no country of origin information wasobtained for 3% of the samples

agri-Samples were analyzed for generic E coli and Salmonella spp with E coliisolates being further analyzed for the presence of the following virulencefactors: enterohemorrhagic shiga-toxins SLT-1 and SLT-2, hemolysin HlyA,invasive trait (intimin-eae) enterotoxigenic toxins (heat stable STa, STb; heat

labile LT), enteropathogenic — invasive character (intimin eae-a),

enteroag-gregative — gene associated with the virulent plasmid, necrotizing cytotoxic —cytotoxic necrotizing factor (CNF-1 and 2), enteroinvasive — IpaH geneknown to be associated with EIEC, and K1 capsular antigen The presence ofvirulence factors does not necessarily mean that the strains isolated from theproduce items are pathogenic to humans, but may have pathogenic potential.Data presented in Table 1.4 show that of the 10,315 USDA MDPsamples that were collected and analyzed for Salmonella spp., only 3 samples(0.03% of the total number of samples) were found to have detectable levels

of Salmonella spp Of the 10,276 USDA MDP samples that were collected

TABLE 1.4

Summary of the USDA MDP Analysis for Salmonella spp and E coli withAssociated Virulence Factors for Cantaloupe, Celery, Leaf Lettuce, RomaineLettuce, and Tomatoes

Produce item

No of samples tested for Salmonella spp.

No of samples tested for

E coli

No and % of samples testing positive for Salmonella spp.

No and % of samples testing positive for

E coli with a virulence factor

and analyzed for E coli, 64 samples (0.62% of the total number of samples)were found to have detectable levels of E coli with associated virulencefactors Twenty-seven (1.25%) of 2161 leaf lettuce and 29 (1.34%) of 2158romaine lettuce samples were found to have detectable levels of E coli withassociated virulence factors Cantaloupe, celery, and tomato had incidencerates for the presence of E coli with associated virulence factors of 0.19, 0.14,and 0.11%, respectively.

Follow-up FDA farm investigations and other information from boththe agency’s imported and domestic produce surveys indicated that failure

to follow GAPs was often associated with the findings of pathogen tamination In particular, inadequate manure management and lack ofappropriate field and transport sanitation practices were most frequentlyassociated with overall contamination Specific problems included fields thatwere open to domestic animals or were fertilized by untreated animal manure,equipment and tools that were not being sanitized, unsanitary harvestingand/or packing equipment or practices (e.g., woven plastic bags to collectcilantro after harvest), and unsanitary methods of transportation (e.g., truckswashed with nonchlorinated water and/or cleaned infrequently) [12]

con-1.4.4 PRODUCE-ASSOCIATEDFOODBORNE ILLNESS

TRACEBACK INVESTIGATION RESULTS

Traceback investigations have yielded no definitive information as to thecauses of recent produce-associated foodborne illness outbreaks The inability

to identify clearly where contamination occurred and the actual causes ofrecent foodborne illness outbreaks associated with produce consumption isfrustrating to the industry and regulators alike and is a significant hurdle todeveloping a means of ensuring that similar outbreaks do not recur Withoutscience-based data that clearly identify the cause of recent foodborne ill-nesses associated with produce consumption, only speculation and opinioncan be used to hypothesize about what may have gone wrong It is imperativethat industry, academia, government, and consumers collaborate and take

an active role by working together on developing and implementing measuresthat enhance produce food safety Guzewich [15] reported in a summary

of produce-related outbreak farm investigations that the practices most likely

to have contributed to numerous recent outbreaks related to produceconsumption are:

Questionable practices regarding safe water use

Inadequate animal management (domestic and/or wild animals)

Unsanitary facilities and equipment

Inadequate employee health and hygiene practices

It is important that future investigations do not simply focus on thesuspected primary causes of produce contamination in the supply chain, butallow for identification of hitherto unidentified actual causes of produce

contamination Regulatory agency traceback investigations of facilitiessuspected of being involved in a foodborne illness outbreak must focus ondetermining the efficiency and effectiveness of the facilities’ GAP programand attempt to identify clearly if the contamination occurred due to non-compliance with GAPs or due to deficiencies in GAPs as they are currentlyformulated.

1.5 POTENTIAL SOURCES OF PRODUCE

CONTAMINATION BY HUMAN PATHOGENS

While produce quality can be judged by outward appearance based on suchcriteria as color, turgidity, and aroma, food safety cannot Casual inspection

of produce cannot determine if it is in fact safe and wholesome to consume.Most fresh fruits and vegetables are grown in nonsterile environments, andconventional fruit and vegetable growers have less control over conditions

in the production field as compared to an enclosed production or foodpreparation facility The surfaces of produce have natural microfloracomposed of microorganisms that are generally benign However, low-levelcontamination of produce with pathogenic microorganisms may sporadicallyoccur Production, harvesting, washing, cutting, slicing, packaging, transport-ing, and preparation all offer opportunities for produce contamination While

it is well established from the data presented above that the vast majority ofproduce contamination with human pathogens occurs in postproductionsituations (Figure 1.1), if contamination does occur during growing andinitial postharvest handling of produce, the consequences can be far greater.This is due to the potential for amplification of human pathogens through-out distribution and the increased risk of cross contamination posed byhandling a food product contaminated with a human pathogen

1.5.1 FOOD SAFETYRISKFACTORS ASSOCIATED WITH

PRODUCTION OF FRESH PRODUCE

Management of growing conditions is of paramount importance in ing the contamination of fresh produce by human pathogens There are riskfactors to consider such as growing conditions, agricultural practices used

prevent-by specific growers, the time of year, growing region/environment, andmanagement practices that may change over the course of a season Climate,weather, water quality, soil fertility, pest control, as well as irrigation, andother management practices are difficult to integrate towards the develop-ment and implementation of microbial risk prevention and reduction programs

on the farm [16]

Organic foods including organic fresh fruits and vegetables are one ofthe fastest-growing segments of the U.S food industry, and there aremany product claims among organic producers and handlers that organicproducts are safer and more nutritious Only a limited number of studies

have been conducted comparing conventional versus organic fruit andvegetable production practices and the effects on product food safety risk.There is currently no scientific evidence to support claims that organicallygrown fruits and vegetables are either safer or pose a greater food safety riskthan conventionally grown produce [17–19].

1.5.1.1 Land Use

The safety of fruits and vegetables grown on any given piece of land is notonly influenced by the current agricultural practices but also by former landuse practices Human pathogens may persist in soils for long periods oftime [20–22] There may be increased risk of soil contamination if produc-tion land was previously used as a feedlot or for animal grazing since fecalcontamination of the soil may be extensive However, it is difficult to deter-mine exactly the magnitude of the risk as the persistence of human patho-gens in soil varies by the pathogen in question, soil type, climate, irrigationregimes, initial pathogen population numbers, etc [23]

1.5.1.2 Soil Amendments

Soil amendments are commonly but not always incorporated into tural soils used for fruit and vegetable production to add organic andinorganic nutrients to the soil as well as to reduce soil compaction Humanpathogens may persist in animal manures for weeks or even months [24,25].Proper composting via thermal treatment will reduce the risk of potentialfoodborne illness However, the persistence of many human pathogens inuntreated agricultural soils is currently unknown and under extensiveinvestigation [26–28]

agricul-1.5.1.3 Wild and Domestic Animal Control

Wild and domestic animals such as birds, deer, dogs, rodents, amphibians,insects, and reptiles are known to be potential reservoirs for human patho-gens and their feces may facilitate the spread of human pathogens inagricultural production settings, packinghouses, processing, and duringdistribution [29–31] Food processing, warehousing, and distribution facilitiesroutinely have animal control programs in place to prevent contamination

of fruits and vegetables However, production agriculture in open fields

is challenged by infestation of wildlife and has only a limited number ofremedies available to deal with periodic infestations by these pests There

is little or no data available for production agriculture operations toassess the risks associated with the presence of a particular wild animalspecies in production fields, field harvesting equipment, and/or in an adja-cent field While a zero tolerance for the presence of wild animals in produc-tion environs would potentially eliminate the risk of produce contamination,such operating procedures are simply impractical if not impossible toimplement

1.5.1.4 Irrigation Water

Irrigation water is another potential vector by which contaminants may bebrought in contact with fruits and vegetables Well water is perceived to beless likely to be contaminated with human pathogens than surface watersupplies, due to the limited access to sources of potential contamination.Production agriculture operations routinely test irrigation water sourcesfor the presence of human pathogens and/or indicator microorganisms.However, such testing is of only limited value, particularly for flowingsurface water sources, since water tested at any given point in time will notnecessarily be the same water used to irrigate crops in the future Wheneverwater comes in direct contact with edible portions of fruits and vegetables,particular care should be taken to ensure that the water does not containhuman pathogens Pesticide application with contaminated water is thought

to be the cause of the 1996 cyclosporosis outbreak associated with freshraspberries grown in Guatemala [32–34], and recent research has demonstratedthat commonly used pesticides and fungicides do not significantly affect thesurvival or growth of human pathogens [35]

Irrigation water if contaminated with human pathogens may minate soils, and splashing of soils by irrigation or heavy rain may facilitateproduce contamination [36] A number of recent studies have also indicatedthat fresh produce may be contaminated by root uptake of human pathogensduring irrigation with contaminated water [37,38] Other research reportshave indicated that this phenomenon does not occur [39,40] It is currentlyunclear if root uptake of human pathogens is a significant source of con-tamination of fresh produce However, direct contact of contaminated waterwith edible potions of crops is an obvious means of produce contamination byhuman pathogens

conta-1.5.1.5 Harvest Operations

During harvesting operations field personnel may contaminate fresh fruitsand vegetables by simply touching them with an unclean hand or knife blade.Portable field latrines as well as hand wash stations are routinely madeavailable and used by harvest personnel Monitoring and enforcement of fieldworker personal hygiene practices such as hand washing after use of fieldlatrines are critical to reduce the risk of human pathogen contamination onfresh produce Due to the potential for contamination, produce onceharvested should not be placed on bare soils before being placed in cleanand sanitary field containers [41] Field harvesting tools should be clean,sanitary, and when possible not be placed directly in contact with soil Harvestladders are commonly used to harvest tree fruit and may serve as a potentialsource of contamination, if soiled ladder rungs are handled by pickers tomove the ladder Therefore, ladders should be constructed in a sanitarymanner so as to allow the easy movement of the ladder without the fruitpicker having to grip the ladder rungs Reusable field harvest containers

must also be cleaned and sanitized on a regular basis to reduce the potentialfor cross contamination.

1.5.2 FOOD SAFETYRISKFACTORS ASSOCIATED WITH

POSTHARVESTHANDLING OF PRODUCE

Depending upon the commodity, produce may be field packaged in containersthat will go all the way to the destination market or may be temporarilyplaced in bulk bins, baskets, or bags that will be transported to a packingshed Employees, equipment, cold storage facilities, packaging materials, andany water that directly or indirectly contacts harvested produce must bekept clean and sanitary to prevent contamination

1.5.2.1 Employee Hygiene

Human beings are a significant reservoir for human pathogens and thereforegloves, hairnets, and clean smocks are routinely worn by packinghouseemployees and field harvest crews to reduce the potential for contamination

of fresh produce during handling The cleanliness and personal hygiene ofemployees handling produce at all stages of production and handling must bemanaged to minimize the risk of contamination Availability of adequaterestroom facilities and hand washing stations and their proper use arecritical to preventing contamination of produce by employees Shoe or bootcleaning stations may also be in place to reduce the amount of field dirt andpotential contamination from field operations that may enter packing sheds,processing plants, and distribution centers Employee training regardingsanitary food handling practices, in a language in which employees are fluent,

is essential to reducing the potential for employees contaminating foodproducts that they are handling This is particularly difficult in the produceindustry as employees are often seasonal or temporary contract employees;thus a strategy of repetitive training is often needed

handling at packinghouse facilities should be avoided to reduce mechanicaldamage and punctures to fruit which may allow for the introduction of plantspoilage pathogens via these wounds, as this has been demonstrated to enhancethe potential for growth and survival of some human pathogens [44].

1.5.2.3 Wash and Hydrocooling Water

All water that comes in contact with produce for drenching, washing, cooling, or vacuum cooling must be of sufficient microbial quality to preventcontamination Recirculated water should have sufficient quantities of anapproved wash water disinfectant to reduce the potential for cross contamina-tion of all produce in the drenching, washing, or hydrocooling system Washwater disinfectants are not capable of sterilizing the surface of produce.Research has demonstrated that washing produce in cold chlorinated waterwill reduce microbial populations by two or three log units (100- to 1000-fold),but complete elimination of microbes is never achieved because microorga-nisms adhere so tenaciously to the surface of produce and may be present inmicroscopic hydrophobic areas on the produce surface [2,3] or in inaccessibleattachment sites (stomata, lenticels, punctures) Rinsing produce with waterthat contains a wash water disinfectant will significantly reduce the number ofmicroorganisms present on the produce but it will not remove or inactivate allbacteria Human pathogens cannot be completely removed from produce bywashing in cold chlorinated water [20,45] (See Chapter 17 for more details.)

hydro-It is particularly important that water used for hydrocooling produce

be free of pathogenic microorganisms, as when warm produce is placed incold water, intercellular air spaces within fruits and vegetables contract,creating a partial vacuum (pressure differential) This has been demons-trated to facilitate infiltration of water, which may contain human patho-gens, into fresh produce items While this phenomenon is known to be animportant source of plant pathogen infections during postharvest handling

of fruit and vegetables [46–49], only recently has direct evidence been broughtforward to show that human pathogens may enter produce by this same mecha-nism In a follow-up investigation of potential sources of imported mangocontamination, Penteado et al [50] provided evidence that Salmonella spp.may be internalized in fresh mangoes during simulated postharvest hot waterinsect disinfestation procedures which included a water bath cooling step [51].However, Richards and Beuchat [52] demonstrated that adhering to orinfiltrating of S Poona cells into cantaloupe tissue via the stem scar isnot dictated entirely by the temperature differential between the melon andthe immersion solution containing salmonella cells, but it is also influenced

by properties unique to tissue surfaces

1.5.2.4 Cold Storage Facilities

Cold storage facilities and, in particular, refrigeration coils, refrigeration drippans, forced air cooling fans, drain tiles, walls, and floors are potential

harborages for human pathogens and as such should be cleaned and tized on a frequent and regular basis Listeria monocytogenes can proliferatequite slowly at refrigerated temperatures and may contaminate cold storedproduce if condensation from refrigeration units or the ceiling drips ontoproduce Placing warm produce with field heat into a cold room withinsufficient refrigeration capacity will cause a temperature rise in the roomand, as the room cools, a fog or mist may occur As the water condenses out

sani-of the air and onto surfaces sani-of walls and ceilings that harbor human gens, contaminated condensate may end up dripping onto the stored produce.Therefore, it is imperative that sufficient cooling capacity is availablewhen cooling produce

to reduce the probability of rodent/animal infestation, and measures should betaken to allow for easily identifiable indicators of an infestation Plastic fieldbins and totes are preferred to wooden containers, since plastic surfaces aremore amenable to cleaning and sanitizing, which should be done after every use

to reduce the potential for cross contamination Wooden containers orfield totes are almost impossible to surface sanitize since they have a poroussurface Cardboard field bins if reused should be visually inspected forcleanliness and lined with a polymeric plastic bag before reuse to preventthe potential risk of cross contamination

1.5.2.6 Modified Atmosphere Packaging of

Fresh ProduceThe risk of Clostridium botulinum on ready-to-eat modified atmospherepackaged (MAP) fresh-cut fruits and vegetables has been investigated exten-sively by a number of research groups in recent years [53–57] C botulinum is

a spore-forming bacterium commonly found in agricultural environs Undersuitable environmental conditions (temperatures above 5C, low oxygenconditions, and a pH above 4.6) this microorganism may produce a deadlytoxin Recent research efforts have examined C botulinum risk factorsfor various fresh-cut MAP produce In general, overt gross spoilage of fresh-cut produce occurs well before toxin is produced on shredded cabbage,shredded lettuce, broccoli florets, sliced carrots, and rutabaga The endemicmicroflora on fresh-cut produce play an important role in signaling the end

of shelf life and are also believed to suppress toxin production by C botulinum

[58] However, some products such as butternut squash and onions havebeen demonstrated under temperature abuse conditions to have the poten-tial of appearing acceptable although containing botulinal toxin [53] Theimportant interaction between MAP and microbial food safety must always

be considered, and continued research efforts to understand fully theserelationships are currently underway An in-depth assessment of the risk ofbotulism contributed by MAP of fresh-cut produce may be found in Gorny

et al [59] Several studies at research institutes have found that MAPtechnologies commonly used in the fresh-cut industry have varying effects

on the survival and growth of E coli O157:H7, Salmonella spp., Shigella spp.,and L monocytogenes [60–63] While some pathogenic strains may be inhib-ited, others are unaffected, weakly inhibited, or even stimulated Because

L monocytogenescan grow at refrigeration temperatures, there is concern thatlow inoculum levels, coupled with extended shelf life obtained by the use

of MAP, may allow L monocytogenes to proliferate to infectious dosageslate in shelf life The FDA recently reviewed the risk associated withconsumption of fresh fruits and vegetables as well as 20 other ready-to-eat food categories and published, as a draft, a risk assessment on therelationship between foodborne L monocytogenes and human health(www.fda.gov) Risk from human pathogens due to the use of MAP must beassessed on a per product basis This is due to the complex interactionsbetween the produce, the indigenous microflora, the pathogen, and itsenvironment An excellent example of this interaction is the inhibitory effect

of carrot extract on growth of L monocytogenes [64] Due to these complexinteractions, broad generalities cannot be drawn regarding the risk of specifichuman pathogens on various fresh-cut fruits or vegetables and interactionswith MAP

1.5.2.7 Refrigerated Transport, Distribution, and

Cold StorageProduce is best shipped in temperature-controlled refrigerated vehicles.Maintaining perishables at their appropriate temperature when being trans-ported to destination markets will extend shelf life When appropriate,holding fresh fruits and vegetables at or below 5C will significantly reducethe growth rate of microbes including human pathogens However, coldtemperatures and high relative humidity conditions which are often optimalfor shelf life extension of fresh fruits and vegetables may actually help favorthe viability of some human pathogens such as viral particles

Trucks used during transportation are also a potential source of tamination from human pathogens Therefore, trucks should be routinelycleaned and sanitized on a regular basis, and trucks that have been used

con-to transport live animals, animal products, or con-toxic materials should not

be used to transport produce or used only after effective cleaning andsanitation

1.5.3 FOOD SAFETYRISKFACTORS ASSOCIATED WITH

FOODSERVICE, RESTAURANT, AND RETAIL FOOD

STORES HANDLING OF PRODUCE

In 2003 the FDA collected data via site visits to over 900 establishmentsrepresenting nine distinct facility types including restaurants, institutionalfoodservice operations, and retail food stores Direct observations of producehandling practices were supplemented with information gained from discus-sions with management and food workers and were used to document theestablishments’ compliance status based on provisions in the 1997 ModelFDA Food Code [65]

Failure to control product holding temperatures, poor personal hygiene,use of contaminated equipment/failure to protect food handling equip-ment from contamination, and risk of potential chemical contamination werethe risk factors found to be most often out of compliance with the 1997FDA Model Food Code The percentages of ‘‘out of compliance’’ observationsfor each of these risk factors were found to be: improper holding time/temperature (49.3%), poor personal hygiene (22.3%), contaminated equip-ment (20.5%), and chemical contamination (13.5%) Specifically, for theimproper holding time and temperature risk factor, it was found thatmaintaining cold holding temperatures at or below 5C (41F) for produceitems that are classified as potentially hazardous foods (PHFs) did not occur

in 70.2% of the observed situations Holding PHFs at or below 5C (41F) iscritical to preventing the potential growth of human pathogens, which mayrapidly proliferate on inadequately refrigerated PHFs Date marking ofrefrigerated ready-to-eat PHFs is also an important component of any foodsafety system, and it is designed to promote proper food rotation and limitthe growth of L monocytogenes during cold storage However, appropriatedate marking of ready-to eat PHF produce items made on-site did not occur

in 34% of the observations

The personal hygiene risk factors associated with produce that are most

in need of attention at retail and foodservice operations include adequate,available, and accessible hand washing facilities These personal hygiene riskfactors were found by the survey to be not in compliance with the 1997FDA Model Food Code 33.3, 26.2, and 20.6% of the time, respectively Handsare very common vehicles for the transfer of human pathogens to foodproducts, and food handlers’ hands may become contaminated when theyengage in activities such as handling raw meat products, using the lavatory,coughing, or handling soiled tableware

Food safety procedures for cleaning and sanitizing food contact surfacesand utensils for handling produce were found to be not in compliance withthe 1997 FDA Model Food Code in 44.4% of the observations in thisstudy Proper cleaning and sanitization of food contact surfaces is essential topreventing cross contamination The 2004 FDA report clearly indicates thatfoodservice and retail operators must ensure that their produce food safety

management systems are designed to achieve active managerial control overthe risk factors associated with handling produce identified in the report.

PURCHASE TOPLATE

Li-Cohen and Bruhn [66] in 2002 published the most extensive consumerhandling study of fresh produce from the time of purchase to the plate Via anational mail survey of 624 respondents these researchers quantifiedconsumer produce handling practices as they relate to food safety risk Sixpercent of consumer respondents replied that they never or seldom wash freshproduce before consumption, and greater than 35% of respondents do notwash melons before consumption Approximately half of all respondents didnot wash their hands before handling fresh produce Ninety-seven percent ofall respondents reported that they always washed food preparation surfacesafter contact with raw meat products However, 5% of respondents only drywipe, and 24% of respondents wash these potentially contaminated foodpreparation surfaces only with water (without soap or a disinfectant) Thissurvey also found that many respondents did not separate produce from rawmeat, poultry, or fish in their refrigerators These limited observations clearlyindicate the need for educational outreach to consumers that must emphasizesafe handling practices of produce from purchase to consumption

1.6 EFFECTIVE MANAGEMENT STRATEGIES:

CONTAMINATION PREVENTION AND INTERVENTION

Every foodborne illness outbreak is a tragic event, and an approach thatprevents contamination and possible amplification of human pathogens in theproduce supply chain is the most effective means of ensuring fresh producesafety However, the complexity of effectively implementing this strategy isstated concisely by the FDA [16]:

Although the available scientific literature is adequate to identify sources ofcontamination and estimate microbial persistence on plants, the specific influenceand interactions among the production environments and crop managementpractices are not sufficiently understood to provide detailed guidance to growersand shippers Also, the diversity of cropping systems, scale of operation, use anddesign of equipment, regional and local practices, environmental influences,specifics of on-farm soil related factors, and many other production factorsdefy any attempt to develop an encompassing assignment of microbial risk tocommodities or to crop management practices

Sampling produce is not an effective means of ensuring product safety.Data from the USDA MDP and FDA domestic and imported producesampling surveys indicate that human pathogens are found on fresh produce

infrequently and in low numbers Because of this fact increased sampling forthe presence of human pathogens by either private enterprises or governmentregulators will not effectively reduce foodborne illnesses associated withproduce consumption because it is simply an ineffective strategy Increasedproduce sampling or surveillance would also potentially take valuable limitedresources away from potentially more productive research efforts that identifyrisk factors and mitigation strategies.

Approaches that prevent contamination are warranted and these strategiesinclude effective management and intervention strategies for growing, handling,distributing, and preparing fresh produce that include but are not limited to:

Good Agricultural Practices (GAPs)

Good Manufacturing Practices (GMPs)

Hazard Analysis Critical Control Point (HACCP) programs

1.6.1 GOODAGRICULTURAL PRACTICES(GAPS)

The FDA published Guidance for Industry: Guide to Minimize Microbial FoodSafety Hazards for Fresh Fruits and Vegetablesin 1998 which has since come

to be referred to as Good Agricultural Practices (GAPs) Although thisdocument carries no regulatory or legal weight, due diligence requiresproducers to take prudent steps to prevent contamination of their crops.GAPs have been widely implemented by the fresh fruit and vegetable industryand as formulated provide the produce industry with an excellent description

of broad prescriptive actions that may be taken to enhance produce foodsafety Numerous retail and wholesale buyers have made compliance to GAPs,and subsequent independent third-party audits to ensure compliance withGAPs, a requirement for the purchase of fresh fruits and vegetables

The guide identifies eight principles of food safety within the realms ofgrowing, harvesting, and transporting fresh produce and suggests that thereader ‘‘use the general recommendations in this guide to develop the mostappropriate good agricultural and management practices for your operation.’’The application of these principles is aimed at preventing contamination offresh produce with human pathogens The eight principles are listed belowfollowed by areas of implementation:

1 Prevention of microbial contamination of fresh produce is favoredover reliance on corrective actions once contamination has occurred

2 To minimize microbial food safety hazards in fresh produce, growers

or packers should use GAPs in those areas over which they have

a degree of control while not increasing other risks to the food supply

or the environment

3 Anything that comes in contact with fresh produce has the potential

of contaminating it For most foodborne pathogens associated withproduce, the major source of contamination is associated with human

or animal feces

4 Whenever water comes in contact with fresh produce, its source andquality dictate the potential for contamination.

5 Practices using manure or municipal biosolid wastes should beclosely managed to minimize the potential for microbial contamina-tion of fresh produce

6 Worker hygiene and sanitation practices during production, ing, sorting, packing, and transport play a critical role in minimizingthe potential for microbial contamination of fresh produce

harvest-7 Follow all applicable local, state, and federal laws and regulations, orcorresponding or similar laws, regulations, or standards for operatorsoutside the U.S for agricultural practices

8 Accountability at all levels of the agricultural environment (farms,packing facility, distribution center, and transport operation) isimportant to a successful food safety program There must be quali-fied personnel and effective monitoring to ensure that all elements

of the program function correctly and to help track produce backthrough the distribution channels to the producer

It is currently unclear if recent outbreaks associated with consumption ofproduce are due to lack of compliance with GAPs or if there are deficiencies

in GAPs as they are currently formulated Little scientifically based dataexist regarding the risk associated with many of the production and post-harvest handling practices commonly used in production agriculture and inpostharvest handling situations or what the most effective risk managementstrategies may be

PRACTICES (CGMPS)

The cGMPs are set forth in 21CFR110 and provide guidelines that ensure thatfood for human consumption is safe and has been prepared, packed, and heldunder sanitary conditions The cGMPs provide food processors, such as fresh-cut produce processors, with the core principles of sanitary food handling, andthey serve as well-recognized and agreed upon standards of conduct andoperation The cGMPs are well written in that they provide general guidanceregarding regulatory expectations of performance and conduct without beingoverly specific or prescriptive, and this aspect of the cGMPs accommodates themany diverse specific situations that are encountered in the food industrytoday The regulations as currently written provide flexibility for the diverseformats under which these regulations are applied, by use of terminology such

as ‘‘adequate facilities,’’ ‘‘where appropriate,’’ ‘‘necessary precautions,’’ and

‘‘adequate controls.’’ This flexibility allows the cGMPs to be applied to theplethora of situations encountered during the production, handling, anddistribution of food products Also, and very importantly, by not being overlyprescriptive the cGMPs allow for incorporation of new technologies andinnovation without the need to revise the regulations The cGMPs are the