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Suggested Citation:"Front Matter." Institute of Medicine and National Research Council. 1985. An Evaluation of the Role of Microbiological Criteria for Foods and Food Ingredients. Washington, DC: The National Academies Press. doi: 10.17226/372.
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An Evaluation of the Role of Microbiological Criteria for Foods and Food Ingre(lients Subcommittee on Microbiological Criteria Committee on Food Protection Food and Nutrition Board National Research Council NATIONAL ACADEMY PRESS Washington, D.C. 1985

NATIONAL ACADEMY PRESS · 2101 CONSTITUTION AVENUE, NW · WASHINGTON, DC 20418 NOTICE: The project that is the subject of this report was approved by the Governing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropriate balance. This report has been reviewed by a group other than the authors according to procedures approved by a Report Review Committee consisting of members of the National Academy of Sciences, the National Academy of Engineering, and the Institute of Medicine. The National Research Council was established by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy's purposes of furthering knowledge and of advising the federal government. The Council operates in accordance with general policies determined by the Academy under the authority of its congressional charter of 1863, which established the Academy as a private, nonprofit, self-governing membership corporation. The Council has become the principal operating agency for both the National Academy of Sciences and the National Academy of Engineering in the conduct of their services to the government, the public, and the scientific and engineering communities. It is administered jointly by both Academies and the Institute of Medicine. The National Academy of Engineering and the Institute of Medicine were established in 1964 and 1970, respectively, under the charter of the National Academy of Sciences. The work on which this publication is based was performed pursuant to Contract No. Na80 GA-C-0060 from the Food and Drug Administration, the Department of the U.S. Army Natick Research and Development Center, the U.S. Department of Agriculture, and the National Marine Fisheries Service of the Department of Commerce, which served as administrator of the contract. Library of Congress Cataloging in Publication Data National Research Council (U.S.). Food Protection Committee. Subcommittee on Microbiological Criteria. An evaluation of the role of microbiological criteria for foods and food ingredients. Includes bibliographies and index. 1. Food Microbiology Congresses. 2. Food poisoning Congresses. I. Title. QRl l5.N37 1985 664'.028 84-25555 ISBN 0-309-03497-3 Copyright C) 1985 by the National Academy of Sciences No part of this book may be reproduced by any mechanical, photographic, or electronic process, or in the form of a phonograph recording, nor may it be stored in a retrieval system, transmitted or otherwise copied for public or private use without written permission from the publisher, except for purposes of official use by the United States government. Printed in the United States of America First Printing, May 1985 Second Printing, May 1988 Third Printing, October 1988 Fours Printing, September 1990

Subcommittee on Microbiological Criteria for Foods and Food Ingredients CARL VANDERZANT, Department of Animal Science, Texas Agricultural Experiment Station, Texas A&M University, College Station, Chairman DON F. SPLITTSTOESSER, Department of Food Science and Technology, Agricultural Experiment Station, Cornell University, Geneva, New York, Vice-Chairman DAVID H. ASHTON, Hunt-Wesson Foods, Fullerton, California FRANK L. BRYAN, Centers for Disease Control, Atlanta, Georgia DAVID L. COLLINS-THOMPSON, Department of Environmental Biology, Ontario Agricultural College, University of Guelph, Guelph, Ontario, Canada EDWIN M. FOSTER, Food Research Institute, University of Wisconsin, Madison JAMES J. JEZESKI, Department of Food Science and Nutrition, University of Florida, Gainesville RICHARD V. LECHOWICH, Technical Center, General Foods, Tarrytown, New York RUSSELL J. MARINO, Corporate Quality Assurance, Ralston Purina Company, St. Louis, Missouri JOSEPH C. OLSON, JR., Sun City Center, Florida JOHN H. SILLIKER, Silliker Laboratories, Carson, California MARGARET R. STEWART, Blacksburg, Virginia, Staff Officer Committee on Food Protection DON F. SPLITTSTOESSER, Department of Food Science and Technology, Agricultural Experiment Station, Cornell University, Geneva, New York, Chairman ANDREW G. EBERT, Pet, Inc., St. Louis, Missouri FREDERICK J. FRANCIS, Department of Food Science and Nutrition, University of Massachusetts, Amherst JESSE F. GREGORY, III, Department of Food Science and Human Nutrition, IFAS, University of Florida, Gainesville ALBERT C. KOLB YE, The Nutrition Foundation, Inc., Washington, D.C. DAVID R. LINEBACK, North Carolina State University, Department of Food Science, Raleigh, North Carolina RUSSELL J. MARINO, Corporate Quality Assurance, Ralston Purina Company, St. Louis, Missouri . . .

RICHARD A. SCANLAN, Department of Food Science and Technology, Oregon State University, Corvallis, Oregon STEPHEN L. TAYLOR, Food Research Institute, University of Wisconsin, Madison ROBERT A. MATHEWS, Staff Officer Food and Nutrition Board KURT J. ISSELBACHER, Chairman, Massachusetts General Hospital, Boston RICHARD L. HALL, Vice-Chairman, Science and Technology, McCormick and Company, Hunt Valley, Maryland HAMISH N. MUNRO, Vice-Chairman, Human Nutrition Research Center on Aging, Tufts University, Boston, Massachusetts WILLIAM E. CONNOR, Department of Medicine, Oregon Health Science University, Portland PETER GREENWALD, Division of Cancer Prevention and Control, National Cancer Institute, National Institutes of Health, Bethesda, Maryland JOAN D. GUSSOW, Department of Nutrition Education, Teachers College, Columbia University, New York, New York RICHARD J. HAVEL, Cardiovascular Research Institute, University of California School of Medicine, San Francisco, California VICTOR HERBERT, Department of Medicine, Hahnemann University School of Medicine, Philadelphia, Pennsylvania JAMES R. KIRK, Campbell Soup Company, Camden, New Jersey REYNALDO MARTORELL, Food Research Institute, Stanford University, Stanford, California J. MICHAEL McGINNIS, Office of Disease Prevention and Health Promotion, Department of Health and Human Services, Washington, D.C. MALDEN C. NESHEIM, Division of Nutritional Sciences, Cornell University, Ithaca, New York ROBERT H. WASSERMAN, New York State College of Veterinary Medicine, Cornell University, Ithaca, New York MYRON WINICK, College of Physicians and Surgeons, Columbia University, New York, New York SUSHMA PALMER, Executive Director, National Research Council, Washington, D.C. 1V

Foreword Over the last 20 years interest in and controversy over the application of microbiological criteria to classify foods as either microbiologically acceptable or microbiologically unacceptable have grown steadily. A 1964 report of the National Research Council, An Evaluation of Public Health Hazards from Microbiological Contamination of Foods made some early recommendations toward establishment of meaningful microbiological criteria. In recent years food industry groups at the national and international levels have expressed concern that microbiological criteria for foods es- tablished by regulatory agencies often were not based on sound principles and for some foods were set without justifiable rationale. Regulatory agencies charged with enforcement of laws and regulations on safety and quality of foods must evaluate a myriad of complex production, process- ing, and distribution practices and must frequently do so with limited staff and an extremely tight budget. Microbiological criteria often provide a definitive figure on which a decision to classify a food as being micro- biologically acceptable or unacceptable can be based. When microbiological criteria for foods are not based on definite needs, sound principles, and statistically solid background information, they may become a burden to the food industry, give a false sense of security to the public and lessen confidence in the ability of regulatory agencies to regulate the food supply. Lack of sound guiding principles for the establishment of microbio- logical criteria has, at least in part, been responsible for the large number of standards and guidelines (particularly at the state and local level) that are impractical, unenforceable, and without uniformity. v

V1 FOREWORD For these reasons, the National Research Council through a subcom- mittee of the Food and Nutrition Board's Committee on Food Protection initiated in 1980 a study to formulate general principles for the consid- eration and application of microbiological criteria for foods and food ingredients and to provide recommendations for a unified, coordinated approach. The study was to include (1) definitions, purposes, priorities, and evaluation of methods for microbiological criteria; (2) recommendations for sampling plans, collection locations, and interpretation of analytical results; and (3) evaluation of existing or proposed international and federal programs. The subcommittee has sought the advice and counsel of representatives of the sponsoring agencies: the Food and Drug Administration, the U.S. Department of Agriculture, the National Marine Fisheries Service, and the U.S. Army Natick Research and Development Center. Meetings were held with members of the Food and Nutrition Board's Industry Liaison Panel and representatives of the Centers for Disease Control, the Canadian Bureau of Microbiological Hazards, and 15 industry and public health groups. The subcommittee has benefited from the assistance and advice of many colleagues in industry, government, and academia. The contri- bution of all these groups is gratefully acknowledged. In this book, the subcommittee has tried to set forth the principles for establishment of meaningful microbiological criteria. Recommendations are given on the need for microbiological criteria for 22 "commodity" groups. In addition, plans of action are presented for implementation of the Hazard Analysis Critical Control Point (HACCP) system and of mi- crobiological criteria for foods and food ingredients.

Acknowledgments The Subcommittee on Microbiological Criteria for Foods and Food Ingredients wishes to acknowledge the valuable assistance of the following individuals on the staffs of the contracting agencies: E. Spencer Garrett, National Marine Fisheries Service of the Department of Commerce, Project Officer for the study R. B. Read, Jr., J. David Clem, Howard J. Pippin, Barry Wentz, Robert Weik, Robert Sanders, and Garrett Higginbotham of the Food and Drug Administration of the Department of Health and Human Services Ralph W. Johnston, T. R. Murtishaw, W. H. Dubbert, Gerald Parlett, Eddie F. Kimbrell, George Fry, and Richard Webber of the Department of Agriculture Durwood B. Rowley, Edmund Powers, and Gerald Silverman of the U.S. Army Natick Research and Development Center of the Department of the Army The subcommittee also wishes to acknowledge the assistance and advice of the following individuals in the development of its report: O. Brian Allen, Department of Mathematics and Statistics, University of Guelph, Ontario, Canada Bruce Brown, Health Protection Branch, Health & Welfare, Canada D. S. Clark, Bureau of Microbiological Hazards, Health Protection Branch, Health & Welfare, Canada Donald A. Corlett, Jr., Corporate Quality Assurance, Del Monte Cor- poration, San Francisco, California F. A. Gardner, Department of Poultry Science, Texas A&M University, College Station . . V11

V111 ACKNOWLEDGMENTS Keith A. Ito, National Food Processors Association, Concord, Cali ~ . rornla G. Jarvis, Health Protection Branch, Health and Welfare, Canada D. C. Kilsby, Unilever Research Laboratory, Colworth House, Sharn- brook, Bedford, United Kingdom R. Nickelson, II, Seafood Technology Section, Department of Animal Science, Texas A&M University, College Station A. Peterson, Campbell Soup Company, Camden, New Jersey H. Michael Wehr, Oregon State Department of Agriculture, Salem Roy Widdus, Institute of Medicine, Washington, D.C.

Contents Executive Summary . Introduction, 2 Basic Considerations, 3 Application of Microbiological Criteria to Foods and Food Ingredients, 6 Expansion of the HACCP System in Food Protection Programs, 13 Plans of Action, 14 Recommendations · · ~ 1 Introduction ................... Sources of Microorganisms in Foocis, 41 Microbial Activities in Foods, 41 · · · Historical Aspects, 41 Spoilage, Pathogenic, and Useful Microorganisms, 42 Food as a Selective Environment, 43 Microflora of Processed Foods, 44 Control of Microorganisms in Foods, 46 Approaches to Microbiological Control in Foods, 48 Education and Training Programs, 48 Inspection of Facilities and Operations, 48 Microbiological Testing, 50 Composite Programs, 50 The Hazard Analysis Critical Control Point (HACCP) System, 50 1X .. 15 . 41

x CONTENTS The Current Role of Criteria in Microbiological Control in Foods, 51 Considerations in Establishing Criteria, 53 The Current Report, 54 References, 54 2 Definitions, Purposes, and Needs for Microbiological Criteria . . . . . . . . . . . . . . . . . . e · · · · · e · e · Definitions, 55 Components of a Microbiological Criterion, 55 Mandatory and Advisory Criteria, 56 Types of Microbiological Criteria, 56 Standard, 56; Guideline, 56; Specification, 57 Purposes, 57 Need for Establishment, 58 Applications of Criteria, 59 Standards, 59; Guidelines, 59; Specifications, 60 Relationship to Codex, 60 Attributes of Quality Amenable to Measurement by Microbiological Criteria, 61 References, 64 3 Selection of Foods for Criteria Related to Safety Epi(lemiological Experience, 66 Opportunities for Contamination, 67 Opportunities for Growth, 67 Opportunities for Survival, 69 Processing Conditions, 69 Susceptibility of Probable Consumers, 70 Ultimate Treatment, 70 References, 70 55 ..... 65 4 Selection of Pathogens as Components of Microbiological Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . Introduction, 72 Pathogens, 73 Severe Hazards, 78 Clostridium botulinum, 78; Shigella, 79; Vibrio cholerae, 80; Salmonella, 81; Brucella abortus, Brucella melitensis, 72

CONTENTS X1 Brucella suds, and Mycobacterium bovis, 81; Viruses, 82; Fish and shellfish toxins, 83; Mycotoxins, 84 Moderate Hazards, Potentially Extensive Spread, 85 Salmonella, 85; Pathogenic Escherichia cold (PEC), 87; Streptococcus pyogenes (Lancefield Group A, beta hemolytic), 87 Moderate Hazards, Limited Spread, 88 Staphylococcus aureus, 88; Clostridium perfringens, 89; Bacillus cereus, 90; Vibrio parahaemolyticus, 91; Coxiella burnetii, 91; Histamine poisoning, 92; Yersinia enterocolitica, 93 Campylobacter, 94; Trichinella spiralis, 95 References, 96 5 Selection of Indicator Organisms and Agents as Components of Microbiological Criteria 104 Assessment of Numbers of Microorganisms and/or Microbial Activity, 105 Estimating Numbers of Microorganisms, 105 Aerobic Plate Count, 105; Thermoduric, Psychrotrophic, Thermophilic, Proteolytic, and Lipolytic Counts, 107; Direct Microscopic Count, 108; Microscopic Mold Counts, 109; Yeast and Mold Counts, 110; Heat-resistant Molds, 1 10; Thermophilic Spore Count, 1 10 Measuring Metabolic Products, 1 1 1 Organoleptic Examination, 1 1 1; Dye or Indicator Reduction Time, 1 13; pH, 1 13; Trimethylamine and Total Volatile Nitrogen, 1 16; Indole, 1 17; Ethanol, 1 18; Diacetyl, 1 18; Histamine, 1 19; Limulus Amoebocyte Lysate Test, 119; Extract Release Volume, 120; Adenosine Triphosphate, 120 Assessment of Inclicators, 120 Indicators of Potential Human or Fecal Contamination or Possible Presence of Pathogens, 120 Staphylococci, 120; Escherichia coli, 121; Fecal Coliforms, 122; Enterococci, 123; Pseudomonas aeruginosa, 124 Indicators of Post-Heat Processing Contamination, 124 Coliform Bacteria, 124; Enterobacteriaceae, 125 Tests for Other Components, 126 Tests for Metabolic Products of Pathogens That Indicate a Health Hazard, 126 Thermonuclease Test for Evidence of Growth of Staphylococci and Presence of Enterotoxins, 126; Aflatoxin Detection by Ultraviolet Light, 126 Test for Phosphatase, 127 References, 127

. . X11 CONTENTS 6 Consideration of Sampling Associated With a Criterion . ~ . . . . ~ . . ~ . . . . . ~ . ~ . . . . ~ . . . . 2-CIass Attributes Sampling Plans, 134 3-CIass Attributes Sampling Plans, 136 Variables Sampling Plans, 136 Operating Characteristic Curves, 137 Establishing Limits, 140 Resampling, 141 Applications, 142 References, 143 132 7 Consideration of Decision (Action) to be Taken When a Criterion (Limit) is Exceeded 145 Decision Categories, 146 Evidence of Existence of a Direct Health Hazard, 146 Evidence That a Direct Health Hazard Could Develop, 148 Indications That a Product Was Not Produced Under Conditions Assuring Safety, 148 Indications That a Raw Material May Adversely Affect Shelf-Life, 149 Evidence That a Critical Control Point Is Not Under Control, 149 References, 150 Current Status of Microbiological Criteria and Legislative Bases . . . . a · ~ · · · · ~ · · ~ ~ Introduction, 152 Early Programs in the United States, 152 Current Levels of Concern and Application, 153 International Activities, 154 Joint FAD/WHO Food Standards Program, 154 European Economic Community, 156 International Commission on Microbiological Specifications for Foods (ICMSF), 157 Canadian Microbiological Standards for Foods, 157 U.S. Federal Agencies, 158 Food and Drug Administration (FDA), 158 Compliance Policy Guides, 159; Food Defect Action Levels, 159; Efforts for Microbiological Standards, 163; Cooperative Programs, 164 . 152

CONTENTS United States Department of Agriculture (USDA), 166 Dairy Products, 167; Dry Milk Products, 167; Egg Products, 168; Meat and Poultry Products, 168 National Marine Fisheries Service (NMFS), 174 History, 174; Current Cooperative Agreements, 175; Research, 176 U.S. Army Natick Research and Development Center, 176 Federal and Regional Level Cooperation, 178 State Level, 178 City-County (Local) Level, 179 Industry, 180 References, 181 9 Application of Microbiological Criteria to Foods and Food Ingredients . . . . . . . . . . . . . . . . . . . . . . . Introduction, 184 Dairy Products, 185 Raw Meats, 193 Processed Meats, 199 Raw (Eviscerated, Ready-To-Cook) Poultry, 221 Processed Poultry Products, 230 Eggs and Egg Products, 239 Fish, Molluscs, and Crustaceans, 249 Fruits and Vegetables, 257 Fruit Beverages, 261 Low-Acid Canned Foods, 264 Acid Canned Foods, 268 Water Activity-Controlled Canned Foods, 270 Cereals and Cereal Products, 272 Fats and Oils, 277 Sugar, Cocoa, Chocolate, and Confectioneries, 283 Spices, 287 Yeasts, 289 Formulated Foods, 290 Nuts, 295 Miscellaneous Additives, 297 Bottled Water, Processing Water, and Ice, 299 Pet Foods, 304 . . . x~ ... 184

XIV 10 Expansion of the HACCP System in Food Protection Programs . e e e e e e e e e e e e e e e e e e e e e e e e e Factors to be Considered For Implementation of HACCP, 308 Problems Associated with Implementation of the HACCP Approach, 311 The Need For Application of HACCP at All Points in the Foot! Chain, 313 Cost/Benefit Aspects of Regulatory Control Through HACCP Inspections, 327 References, 327 CONTENTS e 308 11 Plans of Action for Implementation of the HACCP System and of Microbiological Criteria for Foods and Food Ingredients e e e e e e e e e e e e e e e e e e e Implementation of HACCP, 329 Implementation of Microbiological Criteria For Foods and Food Ingredients, 330 Introduction, 330 The Plan, 333 References, 335 Appendixes e e e e e e e e e A Summary Responses to Specific Contract Items, 339 B General Principles for the Establishment and Application of Microbiological Criteria for Foods, 366 C International Microbiological Specifications, 372 D Excerpts from the Regulations Pursuant to the Food and Drugs Act, a Statute of the Government of Canada, 377 E Microbiological Criteria for Foods Purchased by the Military, 387 F Raw Milk-An Editorial, 395 G Report of the WHO/ICMSF Meeting on Hazard Analysis: Critical Control Point System in Food Hygiene, 399 . e 329 e e 337 Index e e e e e e 421

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The safety and quality of the U.S. food supply depend on a total program of careful microbiological control. Microbiological criteria, which establish acceptable levels of microorganisms in foods and food ingredients, are an essential part of such a program. Says ASM News, "This book provides not only an informed and objective evaluation of microbiological criteria for a wide variety of foods and specific pathogens and the committee's recommendations regarding those criteria, but it also provides an excellent reference book on the applied microbiological aspects of food quality assurance."

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