Contents

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

xv

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

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

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

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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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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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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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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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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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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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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31. Viruses and Some Other Proven and Suspected Foodborne
Biohazards ............................................................................................... 611
Viruses ............................................................................................. 611
Bacteria and Prions .......................................................................... 616
Toxigenic Phytoplanktons ................................................................. 622

Appendices ............................................................................................ 629

Appendix A: Relationships of Common Foodborne Genera of GramNegative Bacteria .................................................................................... 629
Appendix B: Relationship of Common Foodborne Genera of GramPositive Bacteria ...................................................................................... 631
Appendix C: Biofilms ...................................................................................... 633
Appendix D: Grouping of the Gram-Negative Asporogenous Rods,
Polar-Flagellate, Oxidase Positive, and Not Sensitive to 2.5 IU
Penicillin, on the Results of Four Other Tests ......................................... 635

Index ....................................................................................................... 637

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