An I n t r o d u c t i o n

Karl R. Matthews Kalmia E. Kniel

Thomas J. Montville

T H E D I T I O N

Food

F O U R T H E D I T I O N

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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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

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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

| Contents

Critical Thinking Skills 1549

Useful Websites for Food Safety Information 1553

Glossary 1555

Answers to Crossword Puzzles 1565

Answers to Selected Questions for Critical Thought |Index 1585