Microbiology of Fruits and Vegetables

MICROBIOLOGY OF

Fruits and

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.

MICROBIOLOGY OF

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

6000 Broken Sound Parkway NW, Suite 300

Boca Raton, FL 33487-2742

© 2006 by Taylor & Francis Group, LLC

CRC Press is an imprint of Taylor & Francis Group

No claim to original U.S. Government works

Printed in the United States of America on acid-free paper

10 9 8 7 6 5 4 3 2 1

International Standard Book Number-10: 0-8493-2261-8 (Hardcover)

International Standard Book Number-13: 978-0-8493-2261-7 (Hardcover)

Library of Congress Card Number 2005046298

This book contains information obtained from authentic and highly regarded sources. Reprinted material is

quoted with permission, and sources are indicated. A wide variety of references are listed. Reasonable efforts

have been made to publish reliable data and information, but the author and the publisher cannot assume

responsibility for the validity of all materials or for the consequences of their use.

No part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic,

mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and

recording, or in any information storage or retrieval system, without written permission from the publishers.

For permission to photocopy or use material electronically from this work, please access www.copyright.com

(http://www.copyright.com/) or contact the Copyright Clearance Center, Inc. (CCC) 222 Rosewood Drive,

Danvers, MA 01923, 978-750-8400. CCC is a not-for-profit organization that provides licenses and registration

for a variety of users. For organizations that have been granted a photocopy license by the CCC, a separate

system of payment has been arranged.

Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only

for identification and explanation without intent to infringe.

Library of Congress Cataloging-in-Publication Data

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

p. cm.

Includes bibliographical references and index.

ISBN 0-8493-2261-8

1. Fruit--Microbiology. 2. Vegetables--Microbiology. I. Sapers, Gerald M. II. Gorny, James R. III.

Yousef, Ahmed Elmeleigy.

QR115.M495 2005

664'.8'001579--dc22 2005046298

Visit the Taylor & Francis Web site at

http://www.taylorandfrancis.com

and the CRC Press Web site at

http://www.crcpress.com

Taylor & Francis Group

is the Academic Division of T&F Informa plc.

2261_Discl.fm Page 1 Friday, July 22, 2005 10:27 AM

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 3/14

Preface

Fruits and vegetables represent an important part of the human diet, providing

essential vitamins, minerals, and fiber, and adding variety to the diet. In their

Food 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 per

day. In today’s global economy, fresh fruits and vegetables are available year

round.

In the U.S. and other technologically advanced countries, high-quality fresh

and processed fruits and vegetables are widely available. Fresh-cut fruits

and vegetables represent a large and rapidly growing segment of the fresh

produce industry. These commodities have an excellent safety record with

respect to incidence of foodborne illness. Nevertheless, surveillance statistics

compiled by the U.S. Centers for Disease Control and Prevention indicate that

significant and increasing numbers of outbreaks have been associated with

fresh fruits and vegetables, or their products. The presence of human patho￾gens in fresh produce is borne out by U.S. Food and Drug Administration

product recall data, and by microbiological surveys of domestically produced

and imported commodities. Increased recognition of a food safety problem

with produce may reflect greater consumption of fruits and vegetables,

more frequent eating out, greater reliance on imports of out-of-season fruits

and vegetables from ‘‘third world’’ producers, and improved surveillance and

reporting methods by public health agencies.

In addition to safety concerns, microbial spoilage of fresh produce repre￾sents a source of waste for consumers, and an economic loss to growers,

packers, and retailers. Post-harvest decay, bacterial soft rot, and microbial

spoilage of fresh-cuts and processed juices are continuing problems.

In recent years, extensive research has been conducted on microbiological

problems relating to the safety and spoilage of fruits and vegetables. Active

areas of research include incidence of human pathogen contamination, sources

of microbial contamination, microbial attachment to produce surfaces, intract￾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.

In this book, we have attempted a comprehensive examination of these

topics, 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 of

produce or production of fermented vegetables, which are adequately covered

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 4/14

elsewhere. We have selected chapter authors who are active researchers in their

respective 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 of

Microflora on Fruits and Vegetables; (II) Microbial Spoilage of Fruits and

Vegetables; (III) Food Safety Issues; (IV) Interventions to Reduce Spoilage

and Risk of Foodborne Illness; and (V) Microbiological Evaluation of Fruits

and Vegetables. Within each section we have grouped chapters that cover

specific issues related to the overall topic. For example, Section I contains

chapters on sources of microbial contamination, attachment of microorgan￾isms to fresh produce, internalization and infiltration of microorganisms in

produce, and stress adaptation by microorganisms and safety of produce.

I wish to thank the individual chapter authors for the authoritative

and comprehensive coverage of their respective topics, and my co-editors,

Dr. James R. Gorny and Dr. Ahmed E. Yousef, for their assistance in

developing the concept and organizational structure of the book, identifying

suitable chapter authors, reviewing the completed chapters, and helping me

assemble the manuscripts into a form suitable for publication. I also thank

Susan Lee, Food Science Editor at Dekker/CRC Press and her editorial staff

for their guidance, invaluable help, and patience in working with us on this

project. I thank my employer, the USDA Agricultural Research Service’s

Eastern Regional Research Center, for allowing me the time, and providing

the resources, that enabled me to participate in this project. Finally, I must

thank my wife for her unlimited patience and understanding during the

many long hours when I was attached to the computer and unavailable to meet

her needs.

Gerald M. Sapers

Preface

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 5/14

Editors

Gerald M. Sapers received his Ph.D. in food technology from MIT in 1961. He

joined the USDA’s Eastern Regional Research Center (ERRC) in 1968, after 2

years 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 minimally

processed fruits and vegetables, mushroom washing, and microbiological

safety of fresh produce, which is his current area of research. He has been a

Lead Scientist at ERRC since 1991. Dr. Sapers has published 110 scientific

papers, 3 book chapters and 5 patents. He is an active member of the Institute

of Food Technologists’ Fruit and Vegetable Products Division, and the

International Fresh-cut Produce Association.

James R. Gorny received his Ph.D. in plant biology from the University of

California, Davis, and his M.S. and B.S. degrees in food science from

Louisiana State University in Baton Rouge. He is currently vice president of

Technology and Regulatory Affairs for the International Fresh-cut Produce

Association, and has been the author and editor of numerous scientific

publications including: Editor-In-Chief of the IFPA Food Safety Guidelines

for the Fresh-cut Produce Industry and a contributor to the chapter on

‘‘Produce Food Safety’’ in the recently revised U.S. Department of Agriculture

Handbook 66. His research has focused on the effects of modified atmos￾pheres on the quality and safety of whole and fresh-cut fruit produce. He

has been actively involved in the fresh-cut produce industry since 1986, and

has worked extensively as a consultant on food safety, packaging, quality

assurance, operations, and general management issues, both nationally and

internationally.

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

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

of Food Microbiology and Toxicology, UW. Dr. Yousef joined The Ohio

State University (OSU) as an assistant professor in 1991. At OSU, Dr. Yousef

investigated 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 processing

and ohmic heating. He is currently a professor at the Department of Food

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 6/14

Science and Technology and the Department of Microbiology, teaching

the main food microbiology course at OSU. Dr. Yousef has published

2 books, 10 book chapters, and 70 scientific papers and review articles, and a

patent. He is an active member of the Institute of Food Technologists, the

American Society for Microbiology, and the International Association of Food

Protection.

Editors

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 7/14

Contributors

Bassam A. Annous

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

Jerry A. Bartz

Department of Plant Pathology

University of Florida

Gainesville, Florida

Robert B. Beelman

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 Chikthimmah

Department of Food Science

Pennsylvania State University

University Park, Pennsylvania

Pascal Delaquis

Food Safety and Quality

Agriculture and Agri-Food Canada

Summerland, British Columbia,

Canada

Mary Ann Dombrink-Kurtzman

National Center for Agricultural

Utilization Research

Agricultural Research Service

U.S. Department of Agriculture

Peoria, Illinois

Elazar Fallik

Department of Postharvest Sciences

of Fresh Produce

ARO-The Volcani Center

Bet-Dagan, Israel

William F. Fett

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

Daniel Y.C. Fung

Department of Animal Sciences and

Industry

Kansas State University

Manhattan, Kansas

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 8/14

Jim Gorny

International Fresh-cut Produce

Association

Davis, California

Lisa Gorski

Western Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Albany, California

Dongsheng Guan

Department of Animal and Food

Sciences

University of Delaware

Newark, Delaware

Yingchan Han

Department of Food Sciences

Purdue University

West Lafayette, Indiana

Dallas G. Hoover

Department of Animal and Food

Sciences

University of Delaware

Newark, Delaware

J.H. Hotchkiss

Department of Food Sciences

Cornell University

Ithaca, New York

William C. Hurst

Department of Food Science and

Technology

University of Georgia

Athens, Georgia

Lauren Jackson

Center for Food Safety and

Applied Nutrition

U.S. Food and Drug Administration

Bedford, Illinois

Susanne E. Keller

National Center for Food Safety

and Technology

U.S. Food and Drug

Administration

Summit Argo, Illinois

Michael F. Kozempel

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

Ching-Hsing Liao

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

Richard H. Linton

Center for Food Safety Engineering

Purdue University

West Lafayette, Indiana

Robert E. Mandrell

Western Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Albany, California

Pamela G. Marrone

AgraQuest, Inc.

Davis, California

Julien Mercier

AgraQuest, Inc.

Davis, California

Arthur J. Miller

U.S. Food and Drug

Administration

Center for Food Safety and

Applied Nutrition

College Park, Maryland

Contributors

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 9/14

J.-M. Monier

Laboratoire d’Ecologie Microbienne

Universite´ Claude Bernard Lyon 1

Villeurbanne, France

Philip E. Nelson

Department of Food Sciences

Purdue University

West Lafayette, Indiana

Ynes R. Ortega

Center for Food Safety

Department of Food Science and

Technology

University of Georgia

Griffin, Georgia

Mickey E. Parish

Citrus Research and Education

Center

University of Florida

Lake Alfred, Florida

Luis A. Rodriguez-Romo

Department of Food Science and

Technology

The Ohio State University

Columbus, Ohio

Gerald M. Sapers

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

Travis L. Selby

Department of Food Sciences

Purdue University

West Lafayette, Indiana

Charles R. Sterling

Department of Veterinary Science

and Microbiology

University of Arizona

Tucson, Arizona

Dike O. Ukuku

Eastern Regional Research Center

Agricultural Research Service

U.S. Department of Agriculture

Wyndmoor, Pennsylvania

B.G. Werner

Department of Food Sciences

Cornell University

Ithaca, New York

Ahmed E. Yousef

Department of Food Science and

Technology

The Ohio State University

Columbus, Ohio

Contributors

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 10/14

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 11/14

Contents

SECTION I Contamination and State of Microflora

on Fruits and Vegetables

Chapter 1

Microbial Contamination of Fresh Fruits and Vegetables.......................... 3

Jim Gorny

Chapter 2

Attachment of Microorganisms to Fresh Produce .................................... 33

Robert E. Mandrell, Lisa Gorski, and

Maria T. Brandl

Chapter 3

Internalization and Infiltration .................................................................. 75

Jerry A. Bartz

Chapter 4

Microbial Stress Adaptation and Safety of Produce ................................. 95

Luis A. Rodriguez-Romo and Ahmed E. Yousef

SECTION II Microbial Spoilage of Fruits

and Vegetables

Chapter 5

Bacterial Soft Rot ...................................................................................... 117

Ching-Hsing Liao

File: {Books}4539-Sapers/Revises-III/3d/4539-Sapers-FM.3d

Creator: iruchan/cipl-un1-3b2-1.unit1.cepha.net Date/Time: 23.7.2005/2:57am Page: 12/14

Chapter 6

Microbial Spoilage of Fresh Mushrooms .................................................. 135

Naveen Chikthimmah and Robert B. Beelman

Chapter 7

Spoilage of Juices and Beverages by Alicyclobacillus spp.......................... 159

Mickey E. Parish

SECTION III Food Safety Issues

Chapter 8

Interventions to Ensure the Microbial Safety of Sprouts.......................... 187

William F. Fett

Chapter 9

Microbiological Safety of Fresh Citrus and Apple Juices ......................... 211

Susanne E. Keller and Arthur J. Miller

Chapter 10

Microbiological Safety Issues of Fresh Melons ......................................... 231

Dike O. Ukuku and Gerald M. Sapers

Chapter 11

Fresh-Cut Vegetables ................................................................................. 253

Pascal Delaquis

Chapter 12

Outbreaks Associated with Cyclospora and Cryptosporidium.................... 267

Ynes R. Ortega and Charles R. Sterling

Chapter 13

Patulin ........................................................................................................ 281

Lauren Jackson and

Mary Ann Dombrink-Kurtzman

Chapter 14

Safety of Minimally Processed, Acidified, and Fermented

Vegetable Products..................................................................................... 313

F. Breidt, Jr.

Contents