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Part VI. Indicators of Food Safety and Quality, Principles of Quality Control, and Microbial Criteria</b>

Part VI. Indicators of Food Safety and Quality, Principles of Quality Control, and Microbial Criteria</b>

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Modern Food Microbiology

Sixth Edition



James M. Jay

Professor Emeritus

Wayne State University

Detroit, Michigan

Adjunct Professor

University of Nevada Las Vegas

Las Vegas, Nevada



AN ASPEN PUBLICATION®

Aspen Publishers, Inc.

Gaithersburg, Maryland

2000



The author has made every effort to ensure the accuracy of the information herein. However, appropriate information

sources should be consulted. The author, editors, and the publisher cannot be held responsible for any typographical or

other errors found in this book.



Library of Congress Cataloging-in-Publication Data



Jay, James M. (James Monroe), 1927—

Modern food microbiology / James M. Jay.—6th ed.

p. cm. — (Aspen food science text series)

Includes bibliographical references and index.

ISBN 0-8342-1671-X

1. Food—Microbiology. I. Title. II. Series.

QR115.J3 2000

664'001'579—dc21

99-054735



Copyright O 2000 by Aspen Publishers, Inc.

A Wolters Kluwer Company

www.aspenpublishers.com

All rights reserved.



Aspen Publishers, Inc., grants permission for photocopying for limited personal or internal use.

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Editorial Services: Joan Sesma

Library of Congress Catalog Card Number: 99-054735

ISBN: 0-8342-1671-X



Printed in the United States of America



2 3 4 5



Preface



The sixth edition of Modern Food Microbiology, like the previous edition, focuses on the

general biology of the microorganisms that are

found in foods. Thus, the contents are suitable

for its use in a second or subsequent course in a

microbiology curriculum, or as a primary food

microbiology course in a food science or food

technology curriculum. Although organic chemistry is a desirable prerequisite, it is not necessary for one to get a good grasp of the topics

covered.

When used as a microbiology text, the following sequence has been found to be suitable.

A synopsis of the information in Chapter 1 will

provide students with a sense of the historical

developments that have shaped this discipline

and how it continues to evolve. Memorization

of the many dates and events is not recommended

since much of this information is presented again

in the respective chapters. The material in Chapter 2 is designed to provide a brief background

on microorganisms in nature with emphasis on

those that are important in foods. This material

can be combined with the intrinsic and extrinsic

parameters of growth in Chapter 3 as they exist

in food products and as they affect the common

foodborne organisms. Chapters 4 to 9 deal with

specific food products and they may be covered

to the extent desired with appropriate reviews of

the relevant topics in Chapter 3. Chapters 10 to

12 cover methods for culturing and identifying



foodborne organisms and/or their products, and

these topics may be dealt with in this sequence

or just before foodborne pathogens. The food

preservation methods in Chapters 13 to 19 include information that goes beyond the usual

scope of a second course. Chapters 14 and 19

are new to the sixth edition. Chapter 14 consolidates information from the previous edition that

was scattered throughout several chapters, and

it contains much new information on modified

atmosphere packaging. Chapter 19 covers high

pressure and pulsed electric field processing of

foods, and it contains two sections taken from

the chapter on high temperature processing in

the previous edition.

Chapters 20 and 21 deal with food sanitation,

indicator organisms, and the HACCP system, and

coverage of these topics is suggested before dealing with the pathogens. Chapters 22 to 31 deal

with the known (and some suspected) foodborne

pathogens including their biology and methods

of control. Chapter 22 is also new to this edition and it is intended to provide an overview of

the chapters that follow. The material in this chapter that deals with mechanisms of pathogenesis

is probably best dealt with when the specific

pathogens are covered in their respective chapters.

For most semester courses with a 3-credit lecture and accompanying 2 or 3 credit laboratory,

only about 70% of the material in this edition is



likely to be covered. The remainder is meant for

reference purposes. Citations for new and updated material can be found in the Reference lists

at the end of the chapters.

The following individuals assisted me by

critiquing various parts or sections of the sixth



edition, and I pay my special thanks to each:

P. Druggan, P. Feng, R.B. Gravani, D.R. Henning,

YJ. Lee, J.A. Seiter, L.A. Shelef, J.N. Sofos,

A.C.L. Wong, and A.E. Yousef. Those who assisted me with the previous five editions are acknowledged in the respective editions.



Contents



Preface ....................................................................................................



xv



Part I. Historical Background ..............................................................



1



1. History of Microorganisms in Food ..........................................................



3



Historical Developments ...................................................................



4



Part II. Habitats, Taxonomy, and Growth Parameters .......................



11



2. Taxonomy, Role, and Significance of Microorganisms in Foods ............



13



Bacterial Taxonomy ..........................................................................



13



Primary Sources of Microorganisms Found in Foods ........................



17



Synopsis of Common Foodborne Bacteria .......................................



19



Synopsis of Common Genera of Foodborne Molds ..........................



24



Synopsis of Common Genera of Foodborne Yeasts .........................



29



3. Intrinsic and Extrinsic Parameters of Foods That Affect Microbial

Growth .....................................................................................................



35



Intrinsic Parameters .........................................................................



35



Extrinsic Parameters ........................................................................



49



Combined Intrinsic and Extrinsic Parameters: The Hurdle

Concept ......................................................................................



53



Part III. Microorganisms in Foods ......................................................



57



4. Fresh Meats and Poultry .........................................................................



59



Biochemical Events That Lead to Rigor Mortis .................................



60



The Biota of Meats and Poultry ........................................................



60



Incidence/Prevalence of Microorganisms in Fresh Red Meats ..........



60



Microbial Spoilage of Fresh Red Meats ............................................



68



Spoilage of Fresh Livers ...................................................................



76



Incidence/Prevalence of Microorganisms in Fresh Poultry ................



77



Microbial Spoilage of Poultry ............................................................



78



Carcass Sanitizing/Washing .............................................................



81



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v



vi



Contents

5. Processed Meats .....................................................................................



87



Curing ..............................................................................................



87



Smoking ...........................................................................................



89



Sausage, Bacon, Bologna, and Related Products ............................



89



Bacon and Cured Hams ...................................................................



91



Fermented Meat Products ................................................................



93



6. Seafoods .................................................................................................. 101

Microbiological Quality of Various Fresh and Frozen Products ......... 101

Fermented Fish Products ................................................................. 104

Spoilage of Fish and Shellfish .......................................................... 105

7. Fermentation and Fermented Dairy Products ......................................... 113

Fermentation .................................................................................... 113

Dairy Products .................................................................................. 119

Apparent Health Benefits of Fermented Milks ................................... 124

Diseases Caused by Lactic Acid Bacteria ......................................... 128

8. Fruit and Vegetable Products: Whole, Fresh-Cut, and

Fermented ................................................................................................ 131

Fresh and Frozen Vegetables .......................................................... 131

Spoilage of Fruits ............................................................................. 141

Fresh-Cut Produce ........................................................................... 141

Fermented Products ......................................................................... 146

Miscellaneous Fermented Products .................................................. 154

9. Miscellaneous Food Products ................................................................. 163

Delicatessen and Related Foods ...................................................... 163

Eggs ................................................................................................. 164

Mayonnaise and Salad Dressing ...................................................... 167

Cereals, Flour, and Dough Products ................................................. 168

Bakery Products ............................................................................... 168

Frozen Meat Pies ............................................................................. 168

Sugar, Candies, and Spices ............................................................. 169

Nutmeats .......................................................................................... 169

Dehydrated Foods ............................................................................ 170

Enteral Nutrient Solutions (Medical Foods) ....................................... 171

Single-Cell Protein ............................................................................ 171

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Contents



vii



Part IV. Determining Microorganisms and/or Their Products in

Foods ........................................................................................ 177

10. Culture, Microscopic, and Sampling Methods ........................................ 179

Conventional Standard Plate Count .................................................. 179

Membrane Filters ............................................................................. 182

Microscope Colony Counts ............................................................... 184

Agar Droplets ................................................................................... 184

Dry Film and Related Methods ......................................................... 185

Most Probable Numbers ................................................................... 186

Dye Reduction .................................................................................. 186

Roll Tubes ........................................................................................ 187

Direct Microscopic Count .................................................................. 187

Microbiological Examination of Surfaces .......................................... 188

Metabolically Injured Organisms ....................................................... 190

Viable but Nonculturable Organisms ................................................ 194

11. Physical, Chemical, Molecular, and Immunological Methods ................ 201

Physical Methods ............................................................................. 201

Chemical Methods ............................................................................ 206

Methods for Characterizing and Fingerprinting Foodborne

Organisms .................................................................................. 214

Immunological Methods .................................................................... 221

12. Bioassay and Related Methods .............................................................. 237

Whole-Animal Assays ....................................................................... 237

Animal Models Requiring Surgical Procedures ................................. 242

Cell Culture Systems ........................................................................ 243



Part V. Food Preservation and Some Properties of

Psychrotrophs, Thermophiles, and Radiation-Resistant

Bacteria ..................................................................................... 251

13. Food Preservation with Chemicals .......................................................... 253

Benzoic Acid and the Parabens ........................................................ 253

Sorbic Acid ....................................................................................... 255

The Propionates ............................................................................... 257

Sulfur Dioxide and Sulfites ............................................................... 257



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viii



Contents

Nitrites and Nitrates .......................................................................... 258

NaCl and Sugars .............................................................................. 264

Indirect Antimicrobials ...................................................................... 265

Acetic and Lactic Acids ..................................................................... 268

Antibiotics and Bacteriocins .............................................................. 268

Antifungal Agents for Fruits .............................................................. 274

Ethylene and Propylene Oxides ....................................................... 274

Miscellaneous Chemical Preservatives ............................................. 275

14. Food Preservation with Modified Atmospheres ...................................... 283

Definitions ........................................................................................ 283

Primary Effects of CO2 on Microorganisms ....................................... 286

Food Products .................................................................................. 288

The Safety of MAP Foods ................................................................. 290

Spoilage of MAP and Vacuum-Packaged Meats .............................. 293

15. Radiation Preservation of Foods and Nature of Microbial

Radiation Resistance ............................................................................... 301

Characteristics of Radiations of Interest in Food Preservation .......... 301

Principles Underlying the Destruction of Microorganisms by

Irradiation ................................................................................... 303

Processing of Foods for Irradiation ................................................... 305

Application of Radiation .................................................................... 305

Radappertization, Radicidation, and Radurization of Foods ............. 306

Legal Status of Food Irradiation ........................................................ 312

Effect of Irradiation on Food Quality ................................................. 313

Storage Stability of Irradiated Foods ................................................. 315

Nature of Radiation Resistance of Microorganisms .......................... 315

16. Low-Temperature Food Preservation and Characteristics of

Psychrotrophic Microorganisms .............................................................. 323

Definitions ........................................................................................ 323

Temperature Growth Minima ............................................................ 324

Preparation of Foods for Freezing .................................................... 324

Freezing of Foods and Freezing Effects ........................................... 325

Storage Stability of Frozen Foods .................................................... 327



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Contents



ix



Effect of Freezing on Microorganisms .............................................. 327

Some Characteristics of Psychrotrophs and Psychrophiles .............. 331

The Effect of Low Temperatures on Microbial Physiologic

Mechanisms ............................................................................... 333

Nature of the Low Heat Resistance of Psychrotrophs ....................... 336

17. High-Temperature Food Preservation and Characteristics of

Thermophilic Microorganisms ................................................................. 341

Factors Affecting Heat Resistance in Microorganisms ...................... 342

Relative Heat Resistance of Microorganisms ................................... 346

Thermal Destruction of Microorganisms ........................................... 348

Some Characteristics of Thermophiles ............................................. 351

Other Aspects of Thermophilic Microorganisms ................................ 354

Canned Food Spoilage ..................................................................... 356

18. Preservation of Foods by Drying ............................................................. 363

Preparation and Drying of Low-Moisture Foods ................................ 363

Effect of Drying on Microorganisms .................................................. 364

Storage Stability of Dried Foods ....................................................... 366

Intermediate-Moisture Foods ............................................................ 367

19. Other Food Preservation Methods .......................................................... 375

High-Pressure Processing ................................................................ 375

Pulsed Electric Fields ....................................................................... 379

Aseptic Packaging ............................................................................ 380

Manothermosonication (Thermoultrasonication) ............................... 381



Part VI. Indicators of Food Safety and Quality, Principles of

Quality Control, and Microbial Criteria ................................... 385

20. Indicators of Food Microbial Quality and Safety ..................................... 387

Indicators of Product Quality ............................................................ 387

Indicators of Food Safety .................................................................. 388

The Possible Overuse of Fecal Indicator Organisms ........................ 401

Predictive Microbiology/Microbial Modeling ...................................... 402

21. The HACCP System and Food Safety .................................................... 407

Hazard Analysis Critical Control Point System ................................. 407

Microbiological Criteria ..................................................................... 415



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x



Contents



Part VII. Foodborne Diseases .............................................................. 423

22. Introduction to Foodborne Pathogens ..................................................... 425

Introduction ...................................................................................... 425

Host Invasion ................................................................................... 425

Pathogenesis .................................................................................... 428

Summary .......................................................................................... 434

23. Staphylococcal Gastroenteritis ................................................................ 441

Species of Concern in Foods ............................................................ 441

Habitat and Distribution .................................................................... 443

Incidence in Foods ........................................................................... 443

Nutritional Requirements for Growth ................................................. 444

Temperature Growth Range ............................................................. 444

Effect of Salts and Other Chemicals ................................................. 444

Effect of pH, Water Activity, and Other Parameters .......................... 444

Staphylococcal Enterotoxins: Types and Incidence .......................... 445

The Gastroenteritis Syndrome .......................................................... 453

Incidence and Vehicle Foods ............................................................ 454

Ecology of S. aureus Growth ............................................................ 455

Prevention of Staphylococcal and Other Food-Poisoning

Syndromes ................................................................................. 455

24. Food Poisoning Caused by Gram-Positive Sporeforming

Bacteria .................................................................................................... 461



Clostridium perfringens Food Poisoning ........................................... 461

Botulism ........................................................................................... 466



Bacillus Cereus Gastroenteritis ........................................................ 477

25. Foodborne Listeriosis .............................................................................. 485

Taxonomy of Listeria ........................................................................ 485

Growth .............................................................................................. 488

Distribution ....................................................................................... 492

Thermal Properties ........................................................................... 494

Virulence Properties ......................................................................... 497

Animal Models and Infectious Dose .................................................. 498

Incidence and Nature of the Listeriosis Syndromes .......................... 500

Resistance to Listeriosis ................................................................... 502

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Contents



xi



Persistence of L. monocytogenes in Foods ...................................... 503

Regulatory Status of L. monocytogenes in Foods ............................. 504

26. Foodborne Gastroenteritis Caused by Salmonella and Shigella ............ 511

Salmonellosis ................................................................................... 511

Shigellosis ........................................................................................ 525

27. Foodborne Gastroenteritis Caused by Escherichia coli .......................... 531

Serological Classification .................................................................. 531

The Recognized Virulence Groups ................................................... 531

Prevention ........................................................................................ 543

Travelers' Diarrhea ........................................................................... 543

28. Foodborne Gastroenteritis Caused by Vibrio, Yersinia, and

Campylobacter Species ........................................................................... 549

Vibriosis (Vibrio parahaemolyticus) .................................................. 549

Other Vibrios .................................................................................... 552

Yersiniosis (Yersinia enterocolitica) .................................................. 556

Campylobacteriosis (Campylobacter jejuni) ...................................... 560

Prevention ........................................................................................ 563

29. Foodborne Animal Parasites ................................................................... 569

Protozoa ........................................................................................... 569

Flatworms ......................................................................................... 579

Roundworms .................................................................................... 584

30. Mycotoxins ............................................................................................... 595

Aflatoxins .......................................................................................... 595

Alternaria Toxins .............................................................................. 600

Citrinin .............................................................................................. 600

Ochratoxins ...................................................................................... 601

Patulin .............................................................................................. 601

Penicillic Acid .................................................................................... 602

Sterigmatocystin ............................................................................... 602

Fumonisins ....................................................................................... 602

Sambutoxin ...................................................................................... 606

Zearalenone ..................................................................................... 606

Control of Production ........................................................................ 606



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