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ANTIMICROBIALS
IN FOOD
Third Edition
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FOOD SCIENCE AND TECHNOLOGY
A Series of Monographs, Textbooks, and Reference Books
Editorial Advisory Board
Gustavo V. Barbosa-CánovasWashington State University–Pullman
P. Michael DavidsonUniversity of Tennessee–Knoxville
Mark Dreher McNeil Nutritionals, New Brunswick, NJ
Richard W. HartelUniversity of Wisconsin–Madison
Y. H. HuiScience Technology System, West Sacramento, CA
Lekh R. JunejaTaiyo Kagaku Company, Japan
Marcus KarelMassachusetts Institute of Technology
Ronald G. LabbeUniversity of Massachusetts–Amherst
Daryl B. LundUniversity of Wisconsin–Madison
David B. MinThe Ohio State University
Leo M. L. NolletHogeschool Gent, Belgium
Seppo SalminenUniversity of Turku, Finland
James L. SteeleUniversity of Wisconsin–Madison
John H. Thorngate IIIAllied Domecq Technical Services, Napa, CA
Pieter WalstraWageningen University, The Netherlands
John R. WhitakerUniversity of California–Davis
Rickey Y. YadaUniversity of Guelph, Canada
76. Food Chemistry: Third Edition, edited by Owen R. Fennema
77. Handbook of Food Analysis: Volumes 1 and 2, edited by Leo M. L. Nollet
78. Computerized Control Systems in the Food Industry, edited by Gauri S. Mittal
79. Techniques for Analyzing Food Aroma, edited byRay Marsili
80. Food Proteins and Their Applications, edited by Srinivasan Damodaran
and Alain Paraf
81. Food Emulsions: Third Edition, Revised and Expanded, edited by
Stig E. Friberg and Kåre Larsson
82. Nonthermal Preservation of Foods, Gustavo V. Barbosa-Cánovas,
Usha R. Pothakamury, Enrique Palou, and Barry G. Swanson
83. Milk and Dairy Product Technology, Edgar Spreer
84. Applied Dairy Microbiology, edited by Elmer H. Marth and James L. Steele
85. Lactic Acid Bacteria: Microbiology and Functional Aspects, Second Edition,
Revised and Expanded, edited by Seppo Salminen and Atte von Wright
86. Handbook of Vegetable Science and Technology: Production, Composition,
Storage, and Processing, edited by D. K. Salunkhe and S. S. Kadam
87. Polysaccharide Association Structures in Food, edited by Reginald H. Walter
88. Food Lipids: Chemistry, Nutrition, and Biotechnology, edited by
Casimir C. Akoh and David B. Min
89. Spice Science and Technology, Kenji Hirasa and Mitsuo Takemasa
90. Dairy Technology: Principles of Milk Properties and Processes,
P. Walstra, T. J. Geurts, A. Noomen, A. Jellema, and M. A. J. S. van Boekel
91. Coloring of Food, Drugs, and Cosmetics,Gisbert Otterstätter
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92. Listeria, Listeriosis, and Food Safety: Second Edition, Revised and Expanded,
edited byElliot T. Ryser and Elmer H. Marth
93. Complex Carbohydrates in Foods, edited by Susan Sungsoo Cho,
Leon Prosky, and Mark Dreher
94. Handbook of Food Preservation, edited by M. Shafiur Rahman
95. International Food Safety Handbook: Science, International Regulation, and
Control, edited by Kees van der Heijden, Maged Younes, Lawrence Fishbein,
and Sanford Miller
96. Fatty Acids in Foods and Their Health Implications: Second Edition, Revised
and Expanded, edited by Ching Kuang Chow
97. Seafood Enzymes: Utilization and Influence on Postharvest Seafood Quality,
edited by Norman F. Haard and Benjamin K. Simpson
98. Safe Handling of Foods, edited by Jeffrey M. Farber and Ewen C. D. Todd
99. Handbook of Cereal Science and Technology: Second Edition, Revised and
Expanded, edited by Karel Kulp and Joseph G. Ponte, Jr.
100. Food Analysis by HPLC: Second Edition, Revised and Expanded, edited by
Leo M. L. Nollet
101. Surimi and Surimi Seafood, edited by Jae W. Park
102. Drug Residues in Foods: Pharmacology, Food Safety, and Analysis,
Nickos A. Botsoglou and Dimitrios J. Fletouris
103. Seafood and Freshwater Toxins: Pharmacology, Physiology, and Detection,
edited by Luis M. Botana
104. Handbook of Nutrition and Diet, Babasaheb B. Desai
105. Nondestructive Food Evaluation: Techniques to Analyze Properties
and Quality, edited by Sundaram Gunasekaran
106. Green Tea: Health Benefits and Applications, Yukihiko Hara
107. Food Processing Operations Modeling: Design and Analysis, edited by
Joseph Irudayaraj
108. Wine Microbiology: Science and Technology, Claudio Delfini
and Joseph V. Formica
109. Handbook of Microwave Technology for Food Applications, edited by
Ashim K. Datta and Ramaswamy C. Anantheswaran
110. Applied Dairy Microbiology: Second Edition, Revised and Expanded,
edited by Elmer H.Marth and James L. Steele
111. Transport Properties of Foods, George D. Saravacos and Zacharias B. Maroulis
112. Alternative Sweeteners: Third Edition, Revised and Expanded,edited by
Lyn O’Brien Nabors
113. Handbook of Dietary Fiber,edited by Susan Sungsoo Cho and Mark L. Dreher
114. Control of Foodborne Microorganisms, edited by Vijay K. Juneja
and John N. Sofos
115. Flavor, Fragrance, and Odor Analysis, edited by Ray Marsili
116. Food Additives: Second Edition, Revised and Expanded, edited by
A. Larry Branen, P. Michael Davidson, Seppo Salminen,
and John H. Thorngate, III
117. Food Lipids: Chemistry, Nutrition, and Biotechnology: Second Edition,
Revised and Expanded, edited by Casimir C. Akoh and David B. Min
118. Food Protein Analysis: Quantitative Effects on Processing,
R. K. Owusu- Apenten
119.Handbook of Food Toxicology, S. S. Deshpande
120.Food Plant Sanitation, edited by Y. H. Hui, Bernard L. Bruinsma,
J. Richard Gorham, Wai-Kit Nip, Phillip S. Tong, and Phil Ventresca
121.Physical Chemistry of Foods, Pieter Walstra
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122. Handbook of Food Enzymology, edited by John R. Whitaker,
Alphons G. J. Voragen, and Dominic W. S. Wong
123. Postharvest Physiology and Pathology of Vegetables: Second Edition,
Revised and Expanded, edited by Jerry A. Bartz and Jeffrey K. Brecht
124. Characterization of Cereals and Flours: Properties, Analysis, and Applications,
edited by Gönül Kaletunç and Kenneth J. Breslauer
125. International Handbook of Foodborne Pathogens, edited by
Marianne D. Miliotis and Jeffrey W. Bier
126. Food Process Design, Zacharias B. Maroulis and George D. Saravacos
127. Handbook of Dough Fermentations, edited by Karel Kulp and Klaus Lorenz
128. Extraction Optimization in Food Engineering, edited by Constantina Tzia
and George Liadakis
129. Physical Properties of Food Preservation: Second Edition, Revised
and Expanded, Marcus Karel and Daryl B. Lund
130. Handbook of Vegetable Preservation and Processing, edited by Y. H. Hui,
Sue Ghazala, Dee M. Graham, K. D. Murrell, and Wai-Kit Nip
131. Handbook of Flavor Characterization: Sensory Analysis, Chemistry,
and Physiology, edited by Kathryn Deibler and Jeannine Delwiche
132. Food Emulsions: Fourth Edition, Revised and Expanded, edited by
Stig E. Friberg, Kare Larsson, and Johan Sjoblom
133. Handbook of Frozen Foods, edited by Y. H. Hui, Paul Cornillon,
Isabel Guerrero Legarret, Miang H. Lim, K. D. Murrell, and Wai-Kit Nip
134. Handbook of Food and Beverage Fermentation Technology, edited by
Y. H. Hui, Lisbeth Meunier-Goddik, Ase Solvejg Hansen, Jytte Josephsen,
Wai-Kit Nip, Peggy S. Stanfield, and Fidel Toldrá
135. Genetic Variation in Taste Sensitivity, edited by John Prescott
and Beverly J. Tepper
136. Industrialization of Indigenous Fermented Foods: Second Edition, Revised
and Expanded, edited by Keith H. Steinkraus
137. Vitamin E: Food Chemistry, Composition, and Analysis, Ronald Eitenmiller
and Junsoo Lee
138. Handbook of Food Analysis: Second Edition, Revised and Expanded,
Volumes 1, 2, and 3, edited by Leo M. L. Nollet
139. Lactic Acid Bacteria: Microbiological and Functional Aspects: Third Edition,
Revised and Expanded, edited by Seppo Salminen, Atte von Wright,
and Arthur Ouwehand
140. Fat Crystal Networks, Alejandro G. Marangoni
141. Novel Food Processing Technologies, edited by Gustavo V. Barbosa-Cánovas,
M. Soledad Tapia, and M. Pilar Cano
142. Surimi and Surimi Seafood: Second Edition, edited by Jae W. Park
143. Food Plant Design, edited by Antonio Lopez-Gomez;
Gustavo V. Barbosa-Cánovas
144. Engineering Properties of Foods: Third Edition, edited by M. A. Rao, Syed S.H.
Rizvi, and Ashim K. Datta
145. Antimicrobials in Food: Third Edition, edited by P. Michael Davidson, John N.
Sofos, and A. L. Branen
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ANTIMICROBIALS
IN FOOD
Third Edition
Edited by
P. Michael Davidson
John N. Sofos
A. L. Branen
Boca Raton London New York Singapore
A CRC title, part of the Taylor & Francis imprint, a member of the
Taylor & Francis Group, the academic division of T&F Informa plc.
DK2313_C000.fm Page 10 Friday, April 1, 2005 10:09 AM
Published in 2005 by
CRC Press
Taylor & Francis Group
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Boca Raton, FL 33487-2742
© 2005 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: 0-8247-4037-8 (Hardcover)
International Standard Book Number-13: 978-0-8247-4037-5 (Hardcover)
Library of Congress Card Number 2004062074
This book contains information obtained from authentic and highly regarded sources. Reprinted material is quoted with
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Library of Congress Cataloging-in-Publication Data
Antimicrobials in food / edited by P. Michael Davidson, John N. Sofos, A.L. Branen.--3rd ed.
p. cm. -- (Food science and technology ; 143)
Includes bibliographical references and index.
ISBN 0-8247-4037-8
1. Food additives. 2. Anti-infective agents. I. Davidson, P. Michael, 1950- II. Sofos,
John Nikolaos. III. Branen, Alfred Larry, 1945- IV. Food science and technology (Marcel
Dekker, Inc.) ; 143.
TX553.A3A57 2004
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Preface
The consequences of unintended microbial growth in foods are hazards due to the presence of
pathogenic microorganisms or economic losses due to spoilage microorganisms. Preservation
technologies are designed to protect foods from the effects of microorganisms and inherent dete-
rioration. Microorganisms in foods may be inhibited or inactivated by physical methods (e.g., heat,
cold, reduced water activity) or through application of antimicrobial compounds. Food antimicro-
bials, including chemical sanitizers, may be broadly defined as chemical compounds present in or
added to foods, food packaging, food contact surfaces, or food processing environments that inhibit
the growth of, or inactivate, pathogenic or spoilage microorganisms. Historically, the primary
function of food antimicrobials has been to prolong shelf life and preserve quality through the
inhibition of spoilage microorganisms. In the past 10 to 15 years, however, antimicrobials have
been increasingly utilized as a primary intervention for the inhibition or inactivation of pathogenic
microorganisms in foods. This function becomes increasingly important as food processors search
for more and better tools to improve food safety.
Antimicrobials continue to be one of the most important classes of food additives. Research
on antimicrobials, especially naturally occurring compounds, has increased dramatically in the past
10 to 15 years. The primary incentive for searching for effective antimicrobials among naturally
occurring compounds is to expand the spectrum of antimicrobial activity over that of the traditional,
regulatory-approved substances. Most of the traditional food antimicrobials have limited application
due to pH or food component interactions. Interest in natural antimicrobials is also driven by the
fact that international regulatory agencies are generally very strict as to requirements for toxico-
logical evaluation of novel direct food antimicrobials. An argument often used to justify natural
antimicrobials is that they will produce “green” labels (i.e., with few or no “synthetic” additives
in the ingredient list). However, this justification may lead consumers to the mistaken belief that
antimicrobial food additives currently in use are potentially toxic and should be avoided. In short,
natural antimicrobials have excellent potential but likely will not produce miracles. This has not
stopped researchers from continuing to look for the “perfect” food antimicrobial. However, a single
compound that is effective against all microorganisms in all storage situations and in all foods
likely does not exist. More research is needed on the effectiveness of antimicrobial combinations
and antimicrobials in combination with physical methods (e.g., hurdle technology) that are effective
against different groups of microorganisms. Combinations could well be the ideal antimicrobial
for which everyone is searching.
It has been approximately 12 years since the second edition of Antimicrobials in Foods was
published. In that time, many changes have taken place in the field of food microbiology and the
research area of food antimicrobials. At the time of the second edition, major outbreaks of Escher-
ichia coli O157:H7 and Listeria monocytogenes had not occurred, consumer and regulatory
demands for improved food safety were only beginning, and use of naturally occurring antimicro-
bials was in its infancy. At the time of the second edition, lysozyme, lactoferrin, ozone, and several
other compounds were not approved for use in or on foods in the United States. Since the time of
the second edition, a great deal of progress has been made on determining the spectrum of action,
environmental effects on activity, and mechanisms of action of a number of naturally occurring
antimicrobials.
Because of the many changes since the second edition of Antimicrobials in Foods, considerable
revisions have been made for this third edition. As previously, one thing that has not changed is
the excellent international reputations of the authors of each chapter. Some of the authors are new,
DK2313_C000.fm Page 12 Friday, April 1, 2005 10:09 AM
but, as in the second edition, all are well-recognized experts on their topics. The format for each
chapter varies somewhat depending on the areas each author wishes to emphasize. In general,
chapters on specific antimicrobials include information on spectrum of activity, application to foods,
mechanisms or potential mechanisms of action, regulations, toxicological aspects, and assay in
foods. In the third edition, five new chapters have been added. New chapters on specific antimicro-
bials include those on lysozymes, naturally occurring antimicrobials from animal sources, and
naturally occurring antimicrobials from plant sources. In addition, chapters have been added on
hurdle technology and mechanisms of action, resistance, and stress adaptation. All existing chapters
were extensively revised to reflect research that has taken place since 1993, the publication date
of the second edition. The editors would like to thank the chapter authors for their dedication and
hard work in producing their excellent works. We sincerely hope that these discussions will continue
to be useful for industrial, academic, and regulatory research scientists, technical advisors, industry
consultants, regulators, consumers, and consumer advocates regarding the potential value of anti-
microbials in the food supply.
P. Michael Davidson
John N. Sofos
Larry Branen
DK2313_C000.fm Page 13 Friday, April 1, 2005 10:09 AM
Editors
P. Michael Davidson is a professor of food microbiology at the University of Tennessee, Knoxville.
Serving on the editorial board of several journals and as scientific coeditor of the Journal of Food
Protection, Dr. Davidson is the author or coauthor of more than 150 journal articles, book chapters,
and abstracts. He is a Fellow of the American Academy of Microbiology and the Institute of Food
Technologists (IFT) and is a member of the American Society for Microbiology (ASM), the Society
for Applied Microbiology, and the International Association of Food Protection. He served as chair
of the food microbiology divisions of both the ASM and IFT. Dr. Davidson received the B.S. degree
(1972) from the University of Idaho, Moscow, the M.S. degree (1977) from the University of
Minnesota, Minneapolis-St. Paul, and the Ph.D. degree (1979) in food science and technology from
Washington State University, Pullman.
John N. Sofos, Ph.D., is professor of food microbiology at Colorado State University, Fort Collins.
Serving on the U.S. National Advisory Committee on Microbiological Criteria for Foods and as a
scientific coeditor of the Journal of Food Protection, Dr. Sofos has authored or coauthored more
than 220 referred papers, book chapters, books, and more than 250 abstracts. He is a Fellow of the
American Academy of Microbiology and of the Institute of Food Technologists. He also has received
research awards from the American Meat Science Association and the American Society of Animal
Science, the Educator Award from the International Association for Food Protection, and the United
States Department of Agriculture Secretary’s Honor Award for Superior Service for studies on
bacterial pathogen control. Dr. Sofos received a B.S. degree from the Aristotle University of
Thessaloniki, Greece, and M.S. and Ph.D. degrees from the University of Minnesota.
Alfred Larry Branen is associate vice president for research and outreach and associate director
of the Center for Advanced Microelectronic and Biomolecular Research (CAMBR) at the University
of Idaho Research Park in Post Falls. Formerly dean of the College of Agricultural and Life Sciences
at the University of Idaho and head of the Department of Food Science and Technology at the
University of Nebraska, Lincoln, Dr. Branen is the author or coauthor of more than 50 professional
papers and coeditor, with P. Michael Davidson, John Thorngate, and Seppo Salminen, of Food
Additives. A member of the Institute of Food Technologists and the former chair of its Toxicology
Division, Dr. Branen received the B.S. degree (1967) in food science from the University of Idaho,
Moscow, and the Ph.D. degree (1970) in food science from Purdue University, West Lafayette,
Indiana.
