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 Probiotics in
Food Safety and
Human Health
Edited by
Ipek Goktepe
Vijay K. Juneja
Mohamed Ahmedna

Boca Raton London New York

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

© 2006 by Taylor & Francis Group, LLC

DK3341_Discl.fm Page 1 Wednesday, August 24, 2005 4:00 PM

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: 1-57444-514-6 (Hardcover)
International Standard Book Number-13: 978-1-57444-514-5 (Hardcover)
Library of Congress Card Number 2005046938
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,
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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

Goktepe, Ipek.
Probiotics in food safety and human health / Ipek Goktepe, Vijay K. Juneja and Mohamed Ahmedna.
p. cm.
Includes bibliographical references and index.
ISBN 1-57444-514-6 (alk. paper)
1. Intestines--Microbiology. 2. Food--Microbiology. 3. Microorganisms--Therapeutic use. 4.
Functional foods. I. Juneja, Vijay K., 1956- II. Title.

QR171.I6G645 2005
616.3'301--dc22 2005046938

Visit the Taylor & Francis Web site at

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Taylor & Francis Group and the CRC Press Web site at
is the Academic Division of T&F Informa plc. http://www.crcpress.com

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 5 Thursday, September 1, 2005 10:44 AM

PREFACE

Our understanding of the functions of intestinal microflora and the use of

probiotic microorganisms, a novel concept, to improve human health has
made significant strides. Further, as our knowledge of gastrointestinal dis-
eases increases, the use of probiotics offers an innovative approach for new
food product development in functional foods for specific diseases. Likewise,
the need for better control of microbial contamination in foods has been
paramount in recent years. Foods previously thought not to be involved in
foodborne illness, or believed to be infrequent sources of foodborne illness,
have been associated with outbreaks, or sporadic episodes of illness, which
sometimes have been fatal. Our understanding of foodborne pathogens has
dramatically increased at an unprecedented rate in the last two decades, and
so have the types of microorganisms, previously unknown, or not known to
be causes of foodborne illness, which have recently been linked with docu-
mented outbreaks of illness. This makes it necessary for scientists, industry,
and regulators to reconsider the traditional approach to food preservation
for pathogen control in order to enhance food safety.
The variety of medical approaches to tackle gastrointestinal diseases and
the challenge in ensuring microbiological safety of our food supply empha-
size the need for a comprehensive book on probiotics. These observations,
and our involvement through the years in research addressing microbiolog-
ical safety of foods, led us to the conclusion that such a book is timely. The
intent of this book is to present an in-depth characterization and diagnostics
of probiotic strains, their mechanism of action in humans, food applications
role in the development of new products that contribute to our well-being
by guarding against gastrointestinal diseases and regulatory status. Every
effort was pronounced to make this book as comprehensive and current as
possible. This book is written at a level which presupposes a general back-
ground in medical and food microbiology needed to understand the basic
mechanisms of probiotic action and the functionality of foods. The unique
feature of this book is its thorough coverage of the various topics pertaining
to probiotics, thereby creating new opportunities for food and nutrition
scientists to develop functional foods with specific health benefits for differ-
ent subpopulations. Such a thorough coverage of probiotics is expected to
be equally useful to healthcare professionals. The material in each chapter
is arranged in a logical, systematic, and concise sequence. Each chapter is
written in an easy-to-follow format by a nationally and internationally
renowned expert or team of experts in their particular fields. At the end of
each chapter, citations from the scientific literature by experts in that partic-
ular field of probiotics are included.

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 6 Thursday, September 1, 2005 10:44 AM

It is necessary for the food industry and regulatory agencies to have

personnel who are knowledgeable of the functional properties of foods
aimed at improving human health. Currently, such information is available
in a variety of diverse sources that are not always readily available. Accord-
ingly, this book should be of special benefit to individuals who have little
or no opportunity for additional classroom training and is a valuable text
for those who directly or indirectly are involved in food product develop-
ment or serve as nutritionists or doing research on food functionality and
gastrointestinal disease control, which includes individuals in academic,
industrial, and government institutions, including federal, state, and local
agencies, food consultants, and food lobbyists.
We are grateful to all of our coauthors for their relentless effort in contrib-
uting the chapters. The credit for making this book a reality goes to them.
We hope that this book will help in identifying potential new approaches to
develop new microbiologically safe functional foods and significantly con-
tribute to decreasing the incidence of bacterial foodborne illness outbreaks
and gastrointestinal diseases.

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 7 Thursday, September 1, 2005 10:44 AM

THE EDITORS

IPEK GOKTEPE Ipek Goktepe is an assistant professor of food microbiol-

ogy and toxicology and teaches principles of toxicology, environmental tox-
icology, and food biotechnology at North Carolina Agricultural and
Technical State University in Greensboro, North Carolina, where she has
been a faculty member since 2000. She received her B.S. in fisheries from the
University of Istanbul, Turkey in 1993, an M.S. in food science in 1996, a
Ph.D. in food science in 1999, and a second M.S. in environmental toxicology
in 2000, all from Louisiana State University. She is a member of the Institute
of Food Technologists (IFT), the American Society for Microbiology (ASM),
the American Association of Family and Consumer Sciences (AAFCS), the
Society of Environmental Toxicology and Chemistry (SETAC), Gamma
Sigma Delta, Honor Society of Agriculture; The Honor Society of Phi Kappa
Phi; Phi Tau Sigma, Honorary Society of Food Science; and Kappa Omicron
Nu Honor Society of Family and Consumer Sciences. Dr. Goktepe is the
author of over 70 papers and abstracts on various topics in environmental
toxicology, food microbiology, and food science. Her research focuses on the
use of probiotic bacteria in food safety and human health, development of
new antimicrobial and anticarcinogenic compounds from select plants, and
toxicological assessment of select pesticides on farm workers. Dr. Goktepe
is also co-inventor of two patent applications entitled “A Fiber-Optic Bio-
sensor for Rapid Detection of Pathogens in Poultry Products” and “Special
Packaging Technique to Preserve Freshness of Exotic Mushrooms.” Dr. Gok-
tepe is the recipient of the 2004 Gamma Sigma Delta Honor Society Excel-
lence in Research Award, the 2005 NCART Outstanding Young Investigator
Award, and serves as an associate editor for the Journal of the Science of Food
and Agriculture.

VIJAY K. JUNEJA Vijay K. Juneja is a supervisory microbiologist and lead

scientist in the Microbial Food Safety Research Unit at the Eastern Regional
Research Center (ERRC) of the Agricultural Research Service (ARS) branch
of the United States Department of Agriculture (USDA) in Wyndmoor, Penn-
sylvania. Dr. Juneja received his B.V.Sc. and A.H. (D.V.M.) from G. B. Pant
University of Agriculture and Technology, India, in 1978 and an M.S. (Ani-
mal Science) and Ph.D. degrees in Food Technology and Science from the
University of Tennessee in 1988 and 1991, respectively. Soon after receiving
his Ph.D., he was appointed as a microbiologist at the ERRC-USDA. Dr.
Juneja has developed a nationally and internationally recognized research
program on foodborne pathogens, with emphasis on microbiological safety
of minimally processed foods and predictive microbiology. He is a coeditor

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 8 Thursday, September 1, 2005 10:44 AM

of three books including one entitled, Control of Foodborne Microorganisms

and serves on the editorial board of the Journal of Food Protection, Foodborne
Pathogens & Disease and the International Journal of Food Microbiology. He also
serves as an associate editor for the “Food Microbiology and Safety Section”
of the Journal of Food Science. Dr. Juneja is recipient of several awards includ-
ing the ARS, North Atlantic Area (NAA), Early Career Research Scientist of
the Year, 1998; ARS–FSIS Cooperative Research Award, 1998; ARS, NAA,
Senior Research Scientist of the year, 2002; USDA–ARS Certificate of Merit
for Outstanding Performance, 1994, 1996, 1999, 2001, 2002, 2003. Currently,
Dr. Juneja is a group leader for a multidisciplinary research project concern-
ing the assurance of microbiological safety of processed foods. He develops
strategies for research plans, oversees projects, reports results to user groups,
and advises regulators (FDA, FSIS, etc.) on technical matters, i.e., research
needs, and emerging issues. His research interests include intervention strat-
egies for control of foodborne pathogens and predictive modeling. Dr.
Juneja’s research program has been highly productive, generating over 110
publications including 70 peer-reviewed articles, 3 books (coeditor), plus 105
abstracts of presentations at national and international scientific meetings,
primarily in the area of food safety and predictive microbiology.

MOHAMED AHMEDNA Mohamed Ahmedna is an associate professor

of food science in the Department of Human Environment and Family Sci-
ences at North Carolina Agricultural and Technical State University, Greens-
boro, North Carolina. Dr. Ahmedna received a B.S. in Fisheries Engineering
in 1989 from the Institut Agronormique et Veterinaire Hassan II, Morocco.
Later he received an M.S. and a Ph.D. in Food Science in 1995 and 1998,
respectively, and an M.S. in Applied Statistics in 1998, all from Louisiana
State University, Baton Rouge. Prior to joining North Carolina A&T faculty,
he worked as a senior research and development scientist at Technology
International Inc., LaPlace, Louisiana. Dr. Ahmedna’s research focuses on
product development with emphasis on functional foods and the develop-
ment of value-added products from underutilized agricultural by-products.
He is the author of over 80 peer-reviewed scientific publications, abstracts,
and proceedings, and has a patent on the development of a biosensor for
rapid detection of pathogens in foods. In addition to teaching several grad-
uate courses, including Research Methods in Food Science and Nutrition,
Food Preservation, and Food Product Development, Dr. Ahmedna serves as
the North Carolina A&T State University campus coordinator for the North
Carolina Agromedicine Institute. He is the recipient of numerous awards
including the 2001 Gamma Sigma Delta Award of Excellence in Research
and the 2002 North Carolina A&T Outstanding Young Investigator Award.
He also holds membership in several professional and honorary societies,
including Gamma Sigma Delta honor society of Agriculture, Kappa Phi
Kappa honor society, Phi Tau Sigma honor society of Food Science, Kappa
Omicron Nu honor society for Family and Consumer Sciences, the Institute
of Food Technologists, the American Statistical Association, the American

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 9 Thursday, September 1, 2005 10:44 AM

Peanut Research and Education Society, and the North Carolina Agromed-
icine Institute. Dr. Ahmedna served on several federal review panels, includ-
ing the U.S. Department of Agriculture (USDA), National Research Initiative
(NRI), Small Business Innovative Research (SBIR), U.S. Department of Health
and Human Services (USDHHS), and as a technical reviewer for reputable
journals such as the Journal of Food Science, Bioresource Technology, and the
Journal of Food Engineering.

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 11 Thursday, September 1, 2005 10:44 AM

CONTRIBUTORS

Analía G. Abraham C e n t r o d e I n v e s t i g a c i ó n y D e s a r r o l l o e n
Criotecnología de Alimentos (CIDCA), CONICET–Facultad de Ciencias
Exactas, Universidad Nacional de La Plata, La Plata, Argentina

Farid E. Ahmed Department of Radiation Oncology, Leo W. Jenkins Cancer

Center, The Brody School of Medicine, East Carolina University,
Greenville, North Carolina, USA

Mohamed Ahmedna Food Science & Nutrition, Department of Human

Environment & Family Sciences, North Carolina Agricultural and
Technical State University, Greensboro, North Carolina, USA

Robin C. Anderson U.S. Department of Agriculture, Agricultural Research

Services, Southern Plains Agricultural Research Center, Food and Feed
Safety Research Unit, College Station, Texas, USA

Graciela L. De Antoni C e n t r o d e I n v e s t i g a c i ó n y D e s a r r o l l o e n
Criotecnología de Alimentos (CIDCA), CONICET-Facultad de Ciencias
Exactas, Universidad Nacional de La Plata and Comisión de
Investigaciones Científicas de la Provincia de Buenos Aires (CIC PBA), La
Plata, Argentina

Juha Apajalahti Danisco Innovation Kantvik, Kantvik, Finland

Todd R. Callaway U.S. Department of Agriculture, Agricultural Research

Services, Southern Plains Agricultural Research Center, Food and Feed
Safety Research Unit, College Station, Texas, USA

Maria L. Callegari Centro Ricerche Biotecnologiche, Cremona, Italy

Nigel Cook Central Science Laboratory, Sand Hutton, York, UK

Collette Desmond Teagasc, Dairy Products Research Centre, Fermoy, Co.

Cork, Ireland

Francisco Diez-Gonzalez Department of Food Science and Nutrition,

University of Minnesota, St. Paul, Minnesota, USA

© 2006 by Taylor & Francis Group, LLC

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DK3341_C000.fm Page 12 Thursday, September 1, 2005 10:44 AM

Gary W. Elmer Medicinal Chemistry, University of Washington, Seattle,

Washington, USA

Gerald F. Fitzgerald Department of Microbiology, University College,

Cork, Ireland

Alberto C. Fossati Cátedra de Inmunología, Facultad de Ciencias Exactas,

Universidad Nacional de La Plata, La Plata, Argentina

Udo Friedrich Danisco Innovation Niebüll, Niebüll, Germany

Yoichi Fukushima Nutrition Business Group, Nestlé Japan Ltd., Higashi-

Shinagawa, Shinagawa-ku, Tokyo, Japan

Graciela L. Garrote Centro de Investigación y Desarrollo en Criotecnología

de Alimentos (CIDCA), CONICET–Facultad de Ciencias Exactas,
Universidad Nacional de La Plata, La Plata, Argentina

Kenneth J. Genovese U.S. Department of Agriculture, Agricultural

Research Services, Southern Plains Agricultural Research Center, Food
and Feed Safety Research Unit, College Station, Texas, USA

Ipek Goktepe Department of Human Environment and Family Sciences,

Food and Nutritional Program, North Carolina Agricultural and Technical
State University, Greensboro, North Carolina, USA

Herman Goossens Department of Medical Microbiology, University of

Antwerp, Wilrijk, Belgium

Egon Bech Hansen Danisco Innovation Copenhagen, Copenhagen,

Denmark

Roger B. Harvey U.S. Department of Agriculture, Agricultural Research

Services, Southern Plains Agricultural Research Center, Food and Feed
Safety Research Unit, College Station, Texas, USA

Martine Heyman INSERM EMI 0212, Faculté Necker, Vaugirard, Paris,

France

Kazuhiro Hirayama Department of Veterinary Public Health, The

University of Tokyo, Tokyo, Japan

Wilhelm H. Holzapfel Institute of Hygiene and Toxicology, BFEL,

Karlsruhe, Germany

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 13 Thursday, September 1, 2005 10:44 AM

Geert Huys Department of Biochemistry, Physiology and Microbiology,

Ghent University, Ghent, Belgium

Hisakazu Iino Department of Food Science & Nutrition, Faculty of

Practical Science, Showa Women's University, Setagaya-ku, Tokyo, Japan

Marlene E. Janes Assistant Professor, Department of Food Science,

Louisiana State University Agricultural Center, Baton Rouge, Louisiana,
USA

Anu Lähteenmäki Functional Foods Forum, University of Turku, Turku,

Finland

Liisa Lähteenmäki VTT Biotechnology, Espoo, VTT, Finland

Liesbeth Masco Laboratory of Microbial Ecology and Technology, Ghent

University, Ghent, Belgium

Tiina Mattila-Sandholm Valio Ltd., Helsinki, Espoo, Finland

Lynne V. McFarland Health Services, University of Washington, Seattle,

Washington, USA

Sandrine Ménard INSERM EMI 0212, Faculté Necker, Vaugirard, Paris,

France

Lorenzo Morelli Instituto di Microbiologia, Piacenza, Italy

David J. Nisbet U.S. Department of Agriculture, Agricultural Research

Services, Southern Plains Agricultural Research Center, Food and Feed
Safety Research Unit, College Station, Texas, USA

Daniel J. O’Sullivan Department of Food Science and Nutrition, Center

for Microbial and Plant Genomics, University of Minnesotta, St. Paul,
Minnesota, USA

Arthur C. Ouwehand Department of Biochemistry and Food Chemistry &

Functional Foods Forum, University of Turku, Turku, Finland

Joseph Rafter Department of Medical Nutrition, Karolinska Institutet,

Novum, Huddinge, Sweden

Paul Ross Teagasc, Dairy Products Research Centre, Fermoy, Co. Cork,
Ireland

Maria Saarela VTT Biotechnology, VTT, Espoo, Finland

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 14 Thursday, September 1, 2005 10:44 AM

Gerry P. Schamberger Department of Food Science and Nutrition,

University of Minnesota, St. Paul, Minnesota, USA

Ralf-Christian Schlothauer Danisco Innovation Niebüll, Niebüll, Germany

Katja Schmid Danisco Innovation Niebüll, Niebüll, Germany

María Serradell Cátedra de Inmunología, Facultad de Ciencias Exactas,

Universidad Nacional de La Plata, La Plata, Argentina

Catherine Stanton Teagasc, Dairy Products Research Centre, Fermoy, Co.

Cork, Ireland

Christine Staudt Danisco Innovation Niebüll, Niebüll, Germany

Jean Swings Department of Biochemistry, Physiology and Microbiology,

Ghent University, Ghent, Belgium

Robin Temmerman Laboratory of Microbial Ecology and Technology,

Faculty of Bioscience Enginneering, Ghent University, Ghent, Belgium

Marc Vancanneyt Department of Biochemistry, Physiology and Microbiol-

ogy, Ghent University, Ghent, Belgium

Vanessa Vankerckhoven Department of Medical Microbiology, University

of Antwerp, Wilrijk, Belgium

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 15 Thursday, September 1, 2005 10:44 AM

ACKNOWLEDGMENTS

A text of this undertaking on the broad topic of probiotics would not be

possible without the invaluable contributions of the authors who graciously
wrote chapters in their fields of specialty. We especially appreciate the con-
tributors’ patience during the completion of this text. In addition, such an
undertaking would have not been possible without the support provided
by our employers, North Carolina Agricultural and Technical State Univer-
sity and the United States Department of Agriculture and Agricultural
Research Services. We also thank Anita Lekhwani for initiating and coordi-
nating the entire project. The contributions of the editorial and production
staff at Marcel Dekker and CRC Press are gratefully acknowledged for their
support, expertise, and hard work. Finally, we owe a thank you to our
families for their support, love, and patience during the completion of this
book.

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 17 Thursday, September 1, 2005 10:44 AM

CONTENTS

1 Introduction to Prebiotics and Probiotics................................... 1

Wilhelm H. Holzapfel

2 Development of Probiotic Food Ingredients ............................ 35

Katja Schmid, Ralf-Christian Schlothauer, Udo Friedrich,
Christine Staudt, Juha Apajalahti, and Egon Bech Hansen

3 Taxonomy and Biology of Probiotics ........................................ 67

Lorenzo Morelli and Maria L. Callegari

4 Primary Sources of Probiotic Cultures...................................... 91

Daniel J. O’Sullivan

5 Properties of Evidence-Based Probiotics for Human

Health .......................................................................................... 109
Lynne V. McFarland and Gary W. Elmer

6 Genetic Engineering of Probiotic Bacteria ............................. 139

Collette Desmond, Paul Ross, Gerald F. Fitzgerald, and Catherine
Stanton

7 Immunochemical Methods for Detection of Probiotics ........ 165

Analía G. Abraham, María Serradell, Graciela L. Garrote,
Alberto C. Fossati, and Graciela L. De Antoni

8 Molecular-Based Methods Directed toward Probiotics ........ 191

Marlene E. Janes and Nigel Cook

9 Application of Repetitive Element Sequence-Based (rep-)

PCR and Denaturing Gradient Gel Electrophoresis
for the Identification of Lactic Acid Bacteria in
Probiotic Products...................................................................... 207
Robin Temmerman, Liesbeth Masco, Geert Huys, and Jean Swings

10 Genetically Modified Probiotics .............................................. 229

Farid E. Ahmed

© 2006 by Taylor & Francis Group, LLC

DK3341_C000.fm Page 18 Thursday, September 1, 2005 10:44 AM

11 Use of Probiotics in Preharvest Food

Safety Applications ................................................................... 251
Francisco Diez-Gonzalez and Gerry P. Schamberger

12 Preharvest Food Safety Applications of Competitive

Exclusion Cultures and Probiotics........................................... 273
Robin C. Anderson, Kenneth J. Genovese, Roger B. Harvey,
Todd R. Callaway, and David J. Nisbet

13 Probiotics as Biopreservatives for Enhancing

Food Safety ................................................................................. 285
Ipek Goktepe

14 EU Perspectives on Food, Gastrointestinal Tract

Functionality, and Human Health ........................................... 309
Tiina Mattila-Sandholm, Liisa Lähteenmäki, and Maria Saarela

15 Modulation of Epithelial Function and Local Immune

System by Probiotics: Mechanisms Involved......................... 341
Sandrine Ménard and Martine Heyman

16 Probiotics in Cancer Prevention .............................................. 365

Kazuhiro Hirayama and Joseph Rafter

17 Statistical Considerations for Testing the Efficacy

of Probiotics ............................................................................... 383
Mohamed Ahmedna

18 The Safety of Probiotics in Foods in Europe and Its

Legislation .................................................................................. 405
Arthur C. Ouwehand, Vanessa Vankerckhoven, Herman Goossens,
Geert Huys, Jean Swings, Marc Vancanneyt, and Anu Lähteenmäki

19 Probiotics in Food Safety and Human Health: Current

Status of Regulations on the Use of Probiotics in Foods
in Japan ....................................................................................... 431
Yoichi Fukushima and Hisakazu Iino

© 2006 by Taylor & Francis Group, LLC

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