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F O U R T H E D I T I O N
Karl R. Matthews, Kalm ia E. Kniel, and Thomas J. Montville
Karl MatthewsDepartm ent o f Food Science, Rutgers University,New Brunsw ick, New Jersey
Kalm ia E. KnielDepartm ent o f A nim al and Food Sciences,University o f Delaware, Newark, Delaware
Thomas J. MontvilleDepartm ent o f Food Science, Rutgers University,New Brunsw ick, New Jersey
AASMPRESSWashington, DC
Copyright © 2017 by ASM Press. ASM Press is a registered trademark of the American Society for Microbiology. All rights reserved. No part of this publication may be reproduced or transmitted in whole or in part or reutilized in any form or by any means, electronic or mechanical, including photocopying and recording,
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Disclaimer: To the best of the publisher’s knowledge, this publication provides information concerning the subject matter covered that is accurate as of the date of publication. The publisher is not providing legal, medical, or other
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Library of Congress Cataloging-in-Publication DataNames: Matthews, Karl R., author. | Kniel, Kalmia E., author, j
Montville, Thomas J., author.Title: Food microbiology : an introduction / Karl R. Matthews, Department of
Food Science, Rutgers University, New Brunswick, New Jersey, Kalmia E. Kniel, Department of Animal and Food Sciences, University of Delaware,
Newark, Thomas J. Montville, Department of Food Science, Rutgers University, New Brunswick, New Jersey.
Description: 4th edition. | Washington, DC : ASM Press, [2017] | Revision of: Food microbiology / Thomas J. Montville, Karl R. Matthews, Kalmia E.
Kniel. 3rd ed. 2012. | Includes bibliographical references and index. Identifiers: LCCN 2017003891 (print) | LCCN 2017005242 (ebook) |
ISBN 9781555819385 (hardcover) | ISBN 9781555819392 (ebook)Subjects: LCSH: Food— Microbiology.
Classification: LCC QR115 .M625 2017 (print) | LCC QR115 (ebook) |DDC 664.001/579— dc23
LC record available at https://lccn.loc.gov/2017003891
doi:10.1128/9781555819392
Printed in the United States o f America
10 9 8 7 6 5 4 3 2 1
Address editorial correspondence to: ASM Press, 1752 N St., N.W., Washington, DC 20036-2904, USA.
Send orders to: ASM Press, P.O. Box 605, Herndon, VA 20172, USA.Phone: 800-546-2416; 703-661-1593. Fax: 703-661-1501.
E-mail: books@asmusa.org Online: http://www.asmscience.org
Contents
Preface | XV
About the Authors I xvii
SECTION BASICS OF FOOD MICROBIOLOGY
m m mThe Trajectory of Food Microbiology 13Introduction | 3
Who’s on First? | 4
Food Microbiology, Past and Present | 4
To the Future and Beyond | 8
Summary | 10
Suggested reading | 11
Questions fo r critical thought | 11
2
Microbial Growth,Survival, and Death in Foods 1 13
Introduction | 13
Food Ecosystems, Homeostasis, and Hurdle Technology | 15
Foods as Ecosystems 115
Classical Microbiology and Its Limitations 116Limitations of Detection and Enumeration Methods | 16 Plate Counts | 16Selective, or Differential, Media 116 Most-Probable-Number Methods | 19 Enrichment Techniques | 20
Physiological States of Bacteria | 20 Introduction | 20 Injury | 21Viable but Nonculturable I 22
Quorum Sensing and Signal Transduction [ 23Introduction | 23 Quorum Sensing | 24 Signal Transduction | 25 Biofilms | 25
Factors That Influence Microbial Growth | 27Intrinsic Factors | 27 Extrinsic Factors | 33Homeostasis and Hurdle Technology | 36
Growth Kinetics | 39
Microbial Physiology and Metabolism | 41Carbon Flow and Substrate-Level Phosphorylation | 43 The TCA Cycle Links Glycolysis to Aerobic Respiration | 44
Conclusion | 45
Summary | 46
Suggested reading | 46
Questions fo r critical thought | 47
3
Spores and Their SignificanceIntroduction | 49
Spores in the Food Industry | 49Low-Acid Canned Foods | 50 Bacteriology of Sporeformers of Public Health Significance | 53 Heat Resistance of C. botulinum Spores | 55 Spoilage of Acid and Low-Acid Canned and Vacuum-Packaged Foods by Sporeformers | 57
Spore Biology | 58
vi | Contents
Structure | 58 Macromolecules | 59 Small Molecules | 60 Dormancy | 61 Resistance | 61Freezing and Desiccation Resistance | 61 Pressure Resistance | 62 y-Radiation Resistance | 62 UV Radiation Resistance | 62 Chemical Resistance | 62 Heat Resistance | 62
The Cycle of Sporulation and Germination | 64Sporulation | 64Activation | 65Germination | 65Outgrowth | 67
Summary | 67
Suggested reading | 68
Questions fo r critical thought | 68
4
Detection and Enumeration of Microbes in Food 169Introduction | 69
Sample Collection and Processing | 71
Analysis | 72Metabolism-Based Methods | 76 Surface Testing | 76
Summary | 79
Suggested reading | 79
Questions fo r critical thought \ 79
m m mRapid and Automated Microbial Methods 18iIntroduction | 81
Sample Processing | 82
Requirements and Validation of Rapid Methods | 83
Rapid Methods Based on Traditional Methods | 84
Immunologically Based Methods | 88
Molecular Methods | 90
A Potpourri of Rapid Methods | 95
Summary | 96
Suggested reading ] 96
Questions fo r critical thought | 97
■ M V
Indicator Microorganisms and Microbiological Criteria 199Introduction | 99The Purpose of Microbiological Criteria | 99 The Need to Establish Microbiological Criteria | 100 Definitions 1100Who Establishes Microbiological Criteria? 1101
Sampling Plans | 102Types of Sampling Plans 1102
Establishing Limits | 104
Indicators of Microbiological Quality | 104Indicator Microorganisms | 105Metabolic Products 1107
Indicators of Foodborne Pathogens and Toxins [ 107Indicator Organisms | 111 Fecal Coliforms and E. coli | 111 Metabolic Products 1112
Application and Specific Proposals for Microbiological Criteria for Food and Food Ingredients | 114
Current Status | 114
Summary | 116
Suggested reading | 116
Questions fo r critical thought | 116
Contents | vii
SECTION FOODBORNE PATHOGENIC BACTERIA
Regulatory Issues 1 121
Introduction | 121
U.S. Agencies Involved in Food Regulation | 122The USDA 1122The FDA 1125The CDC | 130
Surveillance | 130
When an Outbreak Occurs 1135
Agroterrorism | 139
What’s Next? | 140
Global Perspective | 141
“It Takes a Village” and Maybe More | 141
Summary | 142
Suggested reading | 142
Questions fo r critical thought \ 143
8
Bacillus cereus \ 145Outbreak | 145
Introduction | 146
Characteristics of the Organism 1146
Environmental Sources 1148
Foodborne Outbreaks | 149
Characteristics of Disease | 149
Dose | 149
Virulence Factors and Mechanisms of Pathogenicity 1150The Emetic Toxin 1150 Enterotoxins 1152B. cereus as a Medical Pathogen | 152The Spore | 153
Summary [ 154
Suggested reading | 155
Questions fo r critical thought | 155
9
Campylobacter Species 1 157Outbreak | 157
Introduction 1158
Characteristics of the Organism 1158
Environmental Susceptibility 1158
Reservoirs and Foodborne Outbreaks | 159
Characteristics of Disease | 160C. jejuni and C. coli | 160 Other Campylobacter Species 1161
Epidemiological Subtyping Systems Useful for Investigating Foodborne Illnesses | 161
Infective Dose and Susceptible Populations | 162
Virulence Factors and Mechanisms of Pathogenicity | 162Cell Association and Invasion 1163 Flagella and Motility | 163 Toxins | 163 Other Factors 1163 Autoimmune Diseases 1163
Immunity 1164
Summary 1164
Suggested reading \ 164
Questions fo r critical thought 1165
Clostridium botulinum \ i67Introduction | 167Botulism | 169
Characteristics of the Disease 1173Toxic Doses | 176
Characteristics of C. botulinum \ 176Classification | 176Tolerance to Preservation Methods | 178
Sources of C. botulinum | 181Occurrence of C. botulinum in the Environment | 181
viii | Contents
Occurrence of C. botulinum in Foods ] 181
Virulence Factors and Mechanisms of Pathogenicity 1183Structure of the Neurotoxins 1183 Genetic Regulation of the Neurotoxins | 185 Mode of Action of the Neurotoxins | 185
Summary | 186
Suggested reading \ 186
Questions fo r critical thought | 186
11
Clostridium perfringens \ mIntroduction | 189A Spore’s-Eye View of Clostridium perfringens Toxicoinfections | 189
The Foodborne Illness | 189Cruel and Unusual Punishment 1189 Incidence 1190Vehicles for C. perfringens Foodborne Illness | 192 Factors Contributing to C. perfringens Type A Foodborne Illness 1192 Preventing C. perfringens Type A Foodborne Illness | 193Identification of C. perfringens Type A Foodborne Illness Outbreaks 1193
Characteristics of C. perfringens Type A Foodborne Illness | 194
Infectious Dose for C. perfringens Type A Foodborne Illness [ 194
The Organism | 194Overview 1194Classification: Toxin Typing of C. perfringens | 195 Control of C. perfringens | 197
Reservoirs for C. perfringens Type A | 197
Virulence Factors Contributing to C. perfringens Type A Foodborne Illness | 198Heat Resistance | 198 C. perfringens Enterotoxin 1198
Summary [ 200
Suggested reading | 200
Questions fo r critical thought | 201
12
Enterohemorrhagic Escherichia coli \ 203
Outbreak | 203
Introduction | 204Categories of E. coli | 204
Characteristics of E. coli 0157:H7 and Non-0157 EHEC | 208Acid Tolerance | 209 Antibiotic Resistance | 209 Inactivation by Heat and Irradiation | 210
Reservoirs of E. coli 0157:H7 | 210 Detection of E. coli 0157:H7 and Other EHEC Strains on Farms | 210Factors Associated with Bovine Carriage of E. coli 0157:H7 | 211Cattle Model for Infection by E. coli 0157:H7 | 211Domestic Animals and Wildlife | 211Humans | 211
Disease Outbreaks | 212Geographic Distribution | 212Seasonality of E. coli 0157:H7 Infection | 212Age of Patients | 212Transmission of E. coli 0157:H7 | 213Examples of Foodborne and WaterborneOutbreaks | 213
Characteristics of Disease | 215
Infectious Dose | 215
Mechanisms of Pathogenicity | 216Attaching and Effacing | 216The Focus of Enterocyte Effacement | 217The 60-MDa Plasmid (p0157) | 217
Conclusion | 219
Summary | 220
Suggested reading | 220
Questions fo r critical thought | 220
Contents be
13
Listeria monocytogenes \ 223
Outbreak | 223
Introduction | 224
Characteristics of the Organism | 226Classification: The Genus Listeria | 226 Susceptibility to Physical and Chemical Agents | 227
Listeriosis and Specific Foods | 228Ready-to-Eat Foods | 228 Milk Products | 228 Cheeses | 229Meat and Poultry Products | 229 Seafoods | 230 Other Foods | 230Environmental Sources of L. monocytogenes | 230Food-Processing Plants | 230Prevalence and the Regulatory Statusof L. monocytogenes | 232Human Carriers | 235
Foodborne Outbreaks | 236
Characteristics of Disease | 238
Infectious Dose | 239
Virulence Factors and Mechanisms of Pathogenicity | 239Pathogenicity of L. monocytogenes | 239Specific Genes Mediate Pathogenicity | 240
Summary | 241
Suggested reading | 241
Questions fo r critical thought | 242
More questions than answers | 242
14
Salmonella Species 1243Outbreak [ 243
Introduction | 244
Characteristics of the Organism | 246Biochemical Identification | 246 Taxonomy and Nomenclature | 247 Serological Identification | 248 Physiology | 249
Reservoirs | 252
Characteristics of Disease | 253Symptoms and Treatment | 253
Preventative Measures | 254Antibiotic Resistance | 254
Infectious Dose | 255
Pathogenicity and Virulence Factors | 256Specific and Nonspecific Human Responses | 256Attachment and Invasion | 257Growth and Survival within Host Cells | 257Virulence Plasmids | 257Other Virulence Factors | 258
Summary | 259
Suggested reading | 259
Questions fo r critical thought | 259
15
Staphylococcus aureus \ 271Outbreak \ 271
Characteristics of the Organism | 272Historical Aspects and General Considerations 2“2 Sources of Staphylococcal Food Contaminat e: r. 2“2 Resistance to Adverse Environmental Conditions I 273
Shigella Species 1261Outbreak | 261
Introduction | 262Classification and BiochemicalCharacteristics | 263Shigella in Foods | 264Survival and Growth in Foods | 265
Characteristics of Disease | 265
Foodborne Outbreaks | 267
Virulence Factors | 267Genetic Regulation | 268
Conclusions | 268
Summary | 269
Suggested reading | 269
Questions fo r critical thought | 269
16
| Contents
Foodborne Outbreaks | 274Incidence of Staphylococcal Food Poisoning | 274 A Typical Large Staphylococcal Food Poisoning Outbreak | 274
Characteristics of Disease | 275
Toxic Dose | 276Toxin Dose Required | 276
Microbiology, Toxins, and Pathogenicity | 276Nomenclature, Characteristics, and Distribution of Enterotoxin-Producing Staphylococci | 276 Introduction to and Nomenclature of the Staphylococcal Enterotoxins: Current Classification Scheme Based on Antigenicity | 278 Staphylococcal Regulation of Staphylococcal Enterotoxin Expression | 280
Summary | 283
Suggested reading | 283
Questions fo r critical thought | 283
Vibrio Species 1285Outbreak | 285
Introduction | 286
Characteristics of the Organism | 286 Epidemiology | 287
Characteristics of Disease | 287
Susceptibility to Physical and Chemical Treatments | 288
V. cholerae | 288Isolation and Identification | 288 Reservoirs | 289 Foodborne Outbreaks | 289 Characteristics of Disease | 289 Virulence Mechanisms | 290
V. mimicus | 290 Foodborne Outbreaks | 290 Characteristics of Disease | 290 Virulence Factors | 291
V. parahaemolyticus \ 291 Classification | 291 Reservoirs | 291
Foodborne Outbreaks | 291 Characteristics of Disease | 292 Virulence Mechanisms | 292
V. vulnificus | 292 Classification | 293Susceptibility to Control Methods | 293 Reservoirs | 293 Foodborne Outbreaks | 293 Characteristics of Disease | 294 Virulence Mechanisms | 294
V.fluvialis, V.furnissii, V. hollisae, and V. alginolyticus | 294
Summary | 294
Suggested reading \ 295
Questions fo r critical thought j 295
Yersinia enterocolitica \ 297
Outbreak \ 297
Introduction | 298Characteristics of the Organism | 298 Classification | 298 Susceptibility and Tolerance | 299
Characteristics of Infection | 300
Reservoirs | 302
Foodborne Outbreaks | 303
Mechanisms of Pathogenicity | 304 Pathological Changes | 304
Virulence Determinants | 304 Chromosomal Determinants of Virulence | 304 Other Virulence Determinants | 305 Pathogenesis of Yersinia-Induced Autoimmunity | 306
Summary | 306
Suggested reading | 306
Questions fo r critical thought | 307
Contents | xi
SECTION OTHER MICROBES IMPORTANT IN FOOD
Lactic Acid Bacteria and Their Fermentation Products 1311Introduction | 311
The Biochemical Foundation of Food Fermentation | 311Catabolic Pathways | 313Genetics of Lactic Acid Bacteria | 314
Dairy Fermentations | 315Starter Cultures | 318Production of Aroma Compounds | 318
Vegetable Fermentations | 319Ingredients and Additives Used duringFermentations | 320Sauerkraut Fermentation [ 320Pickle Fermentation | 321
Meat Fermentations | 322
Summary | 324
Suggested reading | 325
Questions fo r critical thought | 325
20
Yeast-Based and Other Fermentations 1 32 7
Introduction | 327
Fermentations That Use Yeast | 328Bread | 328 Beer | 329 Wine | 332
Vinegar Fermentation | 334
Cocoa and Coffee Fermentations | 335Cocoa | 335 Coffee | 339
Fermented Foods of Non-Western Societies | 339
Summary | 340
Suggested reading | 340
Questions fo r critical thought | 340
21Spoilage Organisms 1 343
Introduction | 343
Meat, Poultry, and Seafood Products | 344Origin of the Microbiota in Meat 344Origin of the Microbiota in Poultry | 344Origins of Microbiota in Finflsh j 345Origins of Microbiota in She 345Bacterial Attachment to Food and FoodContact Surfaces | 345Microbial Progression during Storage I 346Muscle Tissue as a Growth Medium | 347Factors Influencing Spoilage | 348Control of Spoilage of Muscle Foods | 351
Milk and Dairy Products 353Milk and Dairy Products asGrowth Media | 354Psychrotrophic Spoilage : 355Spoilage by Fermentative Nonsporeformers | 359Spore-Forming Bacteria | 360Yeasts and Molds | 361
Spoilage of Produce and Grains 362Types of Spoilage | 362Mechanisms of Spoilage | 363Influence of Physiological State | 364Microbiological Spoilage of Vegetables | 365Microbiological Spoilage of Fruits j 367Microbiological Spoilage of Grains andGrain Products | 368
Summary j 370
Suggested reading | 370
Questions fo r critical thought | 370
Molds I 373Introduction | 373
Isolation, Enumeration, and Identification | 373
Aspergillus Species | 377A .fav u s and A. parasiticus | 379
xii | Contents
Other Toxigenic Aspergilli | 383
Penicillium Species | 384Significant Penicillium Mycotoxins | 384
Fusaria and Toxigenic Molds Other than Aspergilli and Penicillia | 386Toxigenic Fusarium Species | 387Detection and Quantitation of FusariumToxins | 388Other Toxic Molds | 389
Summary | 389
Suggested reading | 390
Questions fo r critical thought j 390
23
Parasites 1 391
Outbreak | 391
Introduction | 392
Protozoa | 393Cryptosporidium spp. | 395 Cyclospora cayetanensis | 399 Toxoplasma gondii \ 403 Giardia intestinalis | 407 Other Protozoa of Interest [ 409
Helminths | 412Roundworms (Nematodes) | 412 Tapeworms (Cestodes) | 417 Flukes (Trematodes) | 421
Detection | 422
Preventative Measures | 423
Summary | 424
Suggested reading | 424
Questions fo r critical thought | 424
24
Viruses and Prions 1427
Introduction | 427
Viruses | 429Elementary Virology | 429Viruses as Agents of Foodborne Illness | 432Bacteriophages in the Dairy Industry | 445Beneficial Uses of Viruses | 448
Prions | 449A Short History of the Prion | 450 Prion Biology | 451
Summary | 452
Suggested reading | 453
Questions fo r critical thought | 453
CONTROL OF MICROORGANISMS IN FOODSECTION
25
Chemical Antimicrobials 1457
Introduction | 457
Factors That Affect Antimicrobial Activity | 458
Organic Acids | 461
Parabenzoic Acids | 462
Nitrites | 463
Phosphates | 463
Sodium Chloride | 464
Water Activity | 464
Disinfectants | 466Sulfites | 467 Chlorine | 468Quaternary Ammonium Compounds | 468 Peroxides | 468 Ozone | 469
Naturally Occurring Antimicrobials | 469Lysozyme | 470Lactoferrin and Other Iron-Binding Proteins | 470 Avidin | 471Spices and Their Essential Oils | 471 Onions and Garlic I 472
Contents xiii
Isothiocyanates | 472 Phenolic Compounds | 472 Phage Therapy | 473
Summary | 473
Suggested reading | 474
Questions fo r critical thought | 474
26
Biologically Based Preservation and Probiotic Bacteria 1475
Introduction | 475
Biopreservation by Controlled Acidification | 476
Bacteriocins | 477General Characteristics | 477 Bacteriocin Applications in Foods | 478
Probiotic Bacteria | 481 The Human GI Tract Is a Microbial Ecosystem | 482
Summary | 486
Suggested reading | 486
Questions fo r critical thought | 487
Physical Methods of Food Preservation 1489Introduction | 489
Physical Dehydration Processes | 489Drying | 489 Freeze-Drying | 490
Cool Storage | 491Controlled-Atmosphere Storage | 491 Modified-Atmosphere Packaging | 492
freezing and Frozen Storage | 492
Preservation by Heat Treatments | 494Technological Fundamentals | 496 Thermobacteriology | 497 Calculating Heat Processes for Foods | 502 Heat Resistance? [ 502
Summary | 504
Suggested reading [ 504
Questions fo r critical thought | 505
28
Nonthermal Processing 1507Introduction | 507
Acceptance | 508
High-Pressure Processing | 511
Ozone | 515
Ultraviolet Light | 517
Pulsed Electric Fields and Pulsed Light | 520
Oscillating Magnetic Fields | 522
Ultrasound | 522
Conclusions | 524
Summary | 524
Suggested reading | 525
Questions fo r critical thought | 525
Sanitation and Related Practices 1527Introduction | 527
Food Safety Objectives [ 528
Good Manufacturing Practices | 528General Provisions (Subpart A) | 529Buildings and Facilities (Subpart B) | 529Equipment (Subpart C) | 530Production and Process Controls (Subpart E) | 530DALs (Subpart G) | 531
Sanitation | 533
SSOPs | 537
HACCP | 537
Food Safety Modernization Act | 545
Conclusions | 545
Summary | 546
Suggested reading | 546
Questions fo r critical thought | 546
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