SCIENTIFIC AND HUMANE ISSUES IN THE USE OF RANDOM SOURCE DOGS AND CATS IN RESEARCH

Committee on Scientific and Humane Issues in the Use of Random Source Dogs and Cats in Research

Institute for Laboratory Animal Research

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS

Washington, D.C.
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SCIENTIFIC AND HUMANE ISSUES IN THE USE OF RANDOM SOURCE DOGS AND CATS IN RESEARCH Committee on Scientific and Humane Issues in the Use of Random Source Dogs and Cats in Research Institute for Laboratory Animal Research Division on Earth and Life Studies

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Govern- ing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineer- ing, 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 study was supported by the National Institutes of Health through Contract Number N-01-OD-4-2139 Task Order #207. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the organizations or agencies that provided support for the project. The content of this publication does not necessarily reflect the views or policies of the National Institutes of Health, nor does mention of trade names, commercial products, or organizations imply endorsement by the US government. International Standard Book Number-13: 978-0-309-13807-9 (Book) International Standard Book Number-10: 0-309-13807-8 (Book) International Standard Book Number-13: 978-0-309-13808-6 (PDF) International Standard Book Number-10: 0-309-13808-6 (PDF) Library of Congress Control Number: 2009939412 Additional copies of this report are available from The National Academies Press, 500 Fifth Street, NW, Lockbox 285, Washington, DC 20001; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu Copyright 2009 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Acad- emy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineer- ing programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is presi- dent of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Insti- tute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sci- ences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON SCIENTIFIC AND HuMANE ISSuES IN THE uSE OF RANDOM SOuRCE DOgS AND CATS IN RESEARCH Members Stephen W. Barthold (Chair), University of California, Center for Comparative Medicine Donald C. Bolser, University of Florida, College of Veterinary Medicine Kelly D. garcia, University of Illinois at Chicago Joseph R. Haywood, Michigan State University Stuart E. Leland, Wyeth Research Lila Miller, American Society for the Prevention of Cruelty to Animals Randall J. Nelson, University of Tennessee James Serpell, University of Pennsylvania School of Veterinary Medicine Michael R. Talcott, Washington University School of Medicine Robert A. Whitney, U.S. Public Health Service (retired) Staff Christine Henderson, Project Director Joanne Zurlo, Director Lida Anestidou, Study Director Kathleen Beil, Administrative Coordinator Cameron Fletcher, Senior Editor Rhonda Haycraft, Senior Project Assistant Erin Sorrell, Mirzayan Fellow 

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INSTITuTE FOR LABORATORy ANIMAL RESEARCH COuNCIL Members Stephen W. Barthold (Chair), University of California, Center for Comparative Medicine, Davis, California Kathryn A. Bayne, Association for Assessment and Accreditation of Laboratory Animal Care International, Frederick, Maryland Myrtle A. Davis, National Cancer Institute, Bethesda, Maryland Jeffrey I. Everitt, GlaxoSmithKline Research and Development, Comparative Medicine and Investigator Support, Research Triangle Park, North Carolina James g. Fox, Massachusetts Institute of Technology, Division of Comparative Medicine, Cambridge, Massachusetts Nelson L. garnett, Johns Hopkins University, Baltimore, Maryland (retired) Estelle B. gauda, Johns Hopkins University School of Medicine, Johns Hopkins Hospital, Baltimore, Maryland Joseph W. Kemnitz, University of Wisconsin, Primate Research Center, Madison, Wisconsin Judy A. MacArthur Clark, Home Office, London, England Martha K. McClintock, University of Chicago, Departments of Psychology and Comparative Human Development, Chicago, Illinois Leticia V. Medina, Abbott Laboratories, Abbott Park, Illinois Timo Olavi Nevalainen, University of Kuopio, National Laboratory Animal Center, Kuopio, Finland Bernard E. Rollin, Colorado State University, Department of Animal Sciences, Fort Collins, Colorado Abigail L. Smith, University of Pennsylvania, School of Veterinary Medicine, Philadelphia, Pennsylvania Stephen A. Smith, Virginia Polytechnic Institute and State University, Department of Biomedical Sciences and Pathobiology, Blacksburg, Virginia James E. Womack, Texas A&M University, College Station, Texas Staff Joanne Zurlo, Director Lida Anestidou, Program Officer Kathleen Beil, Administrative Coordinator Rhonda Haycraft, Senior Project Assistant Cameron Fletcher, Managing Editor, ILAR Journal Erin Sorrell, Mirzayan Fellow i

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INSTITuTE FOR LABORATORy ANIMAL RESEARCH PuBLICATIONS Recognition and Alleviation of Pain in Laboratory Animals (2009) Recognition and Alleviation of Distress in Laboratory Animals (2008) Toxicity Testing in the 21st Century: A Vision and a Strategy (2007) Overcoming Challenges to Develop Countermeasures Against Aerosolized Bioterrorism Agents: Appropriate Use of Animal Models (2006) Guidelines for the Humane Transportation of Research Animals (2006) Science, Medicine, and Animals: Teacher’s Guide (2005) Animal Care and Management at the National Zoo: Final Report (2005) Science, Medicine, and Animals (2004) The Development of Science-based Guidelines for Laboratory Animal Care: Proceedings of the November 2003 International Workshop (2004) Animal Care and Management at the National Zoo: Interim Report (2004) National Need and Priorities for Veterinarians in Biomedical Research (2004) Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research (2003) International Perspectives: The Future of Nonhuman Primate Resources, Proceedings of the Workshop Held April 17-19, 2002 (2003) Occupational Health and Safety in the Care and Use of Nonhuman Primates (2003) Definition of Pain and Distress and Reporting Requirements for Laboratory Animals: Proceedings of the Workshop Held June 22, 2000 (2000) Strategies That Influence Cost Containment in Animal Research Facilities (2000) Microbial Status and Genetic Evaluation of Mice and Rats: Proceedings of the 1999 US/Japan Conference (2000) Microbial and Phenotypic Definition of Rats and Mice: Proceedings of the 1998 US/Japan Conference (1999) Monoclonal Antibody Production (1999) The Psychological Well-Being of Nonhuman Primates (1998) Biomedical Models and Resources: Current Needs and Future Opportunities (1998) Approaches to Cost Recovery for Animal Research: Implications for Science, Animals, Research Competitiveness and Regulatory Compliance (1998) Chimpanzees in Research: Strategies for Their Ethical Care, Management, and Use (1997) Occupational Health and Safety in the Care and Use of Research Animals (1997) Guide for the Care and Use of Laboratory Animals (1996) ii

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Guide for the Care and Use of Laboratory Animals—Korean Edition (1996) Guide for the Care and Use of Laboratory Animals—Chinese Version (1996) Guide for the Care and Use of Laboratory Animals—Spanish Version (1996) Guide for the Care and Use of Laboratory Animals—Russian Version (1996) Guide for the Care and Use of Laboratory Animals—French Version (1996) Guide for the Care and Use of Laboratory Animals—Taiwanese Edition (1996) Guide for the Care and Use of Laboratory Animals—Portuguese Edition (1996) Guide for the Care and Use of Laboratory Animals—Japanese Edition (1996) Rodents (1996) Nutrient Requirements of Laboratory Animals, Fourth Revised Edition (1995) Laboratory Animal Management: Dogs (1994) Recognition and Alleviation of Pain and Distress in Laboratory Animals (1992) Education and Training in the Care and Use of Laboratory Animals: A Guide for Developing Institutional Programs (1991) Companion Guide to Infectious Diseases of Mice and Rats (1991) Infectious Diseases of Mice and Rats (1991) Immunodeficient Rodents: A Guide to Their Immunobiology, Husbandry, and Use (1989) Use of Laboratory Animals in Biomedical and Behavioral Research (1988) Animals for Research: A Directory of Sources, Tenth Edition and Supplement (1979) Amphibians: Guidelines for the Breeding, Care and Management of Laboratory Animals (1974) Copies of these reports can be ordered from the National Academies Press (800) 624-6242 or (202) 334-3313 www.nap.edu iii

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Preface The ancient Indian fable of the Blind Men and the Elephant describes a group of blind men who each touch a different part of an elephant and, when they compare their individual impressions of the animal before them, discover that they are in complete disagreement. While assorted versions of this fable vary about the contentiousness of the debate and how it is resolved, the primary lesson is that opinions can differ among individuals. The secondary message is that differences must be resolved in order to reach consensus. Such were the challenges of this committee. The National Academies endeavor to appoint committees that repre- sent a broad range of perspectives and expertise in order to accomplish a fair and balanced study, and this committee was no exception. But what seemed to be a relatively straightforward task in determining the desir- ability and necessity of random source dogs and cats from Class B dealers for National Institutes of Health (NIH) research turned out to be far more complex than the committee initially realized. The complexity goes back to the very origins of medical research and the animal protectionist move- ment, and is steeped in the American public’s emotional ties to dogs and cats (which Frank Loew1 termed “America’s Sacred Cows”) and changing trends in public attitudes toward research using these familiar animals. The American public has insisted that their pets be protected, resulting in pas- 1 Personal communication from the late Franklin Loew, DVM, PhD, Diplomate of the American College of Laboratory Animal Medicine, member of the Institute of Medicine, former Dean of Tufts School of Veterinary Medicine and Cornell School of Veterinary Medicine, past President of Becker College, research scientist, and advocate for research animal welfare. ix

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x PREFACE sage of the original Animal Welfare Act in 1966, with several subsequent revisions. The enforcement arm of the Act, the U.S. Department of Agricul- ture (USDA) Animal and Plant Health Inspection Service (APHIS), has also repeatedly amended its Animal Welfare Regulations to better enforce the Act. Despite these efforts, infractions continue, including recent egregious ones that sparked renewed concern by the public and Congress, which was the impetus for convening this committee. In contrast to the emotion and conviction that pervade public sentiment toward dogs and cats, the scientific community views the “elephant” ratio- nally. The U.S. dog and cat population, with its many breeds and numbers, represents a rich resource for advancing medical knowledge through dis- covery and use of models with homology to many human diseases. The panel of experts on this committee represented a broad spectrum of perspectives, and endeavored to approach its task without bias, despite strong and admittedly emotional personal opinions. As Chairman of this committee, I was impressed that its members set aside their individual dif- ferences in order to reach consensus, and as a result were able to factually describe the entire elephant, with all of its complexity. The committee acknowledges with appreciation a number of indi- viduals who provided input and testimony from their varied perspectives for the committee’s deliberations. At the first meeting, in Washington, DC, on October 7, 2008, the following individuals presented information to the committee: Kimberley Cohen, Covance W. Ron DeHaven, American Veterinary Medical Association (AVMA) Jerry DePoyster, USDA/APHIS David A. Kass, Johns Hopkins University Cathy Liss, Animal Welfare Institute Stacey Pritt, Covance Margaret Snyder, NIH sponsor and contact person Bill yates, University of Pittsburgh The following additional individuals presented information to the com- mittee during its January 12, 2009, meeting in Washington, DC: Stephen O’Brien, National Cancer Institute, NIH Robert Willems, USDA/APHIS Others who provided invaluable assistance to the committee include: Chester gipson, USDA/APHIS Jodie Kulpa-Eddy, USDA/APHIS

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xi PREFACE The committee also received written material submitted for consider- ation by the American Physiological Society, the Humane Society of the United States, and individuals with business or personal interests in the sub- ject of the committee’s deliberations. In addition, the committee received information from several Class B dealers in response to specific questions posed by the committee. The draft of this report was reviewed by individuals chosen for their diverse perspectives and expertise, in accordance with procedures approved by the Report Review Committee of the National Research Council (NRC). The purpose of this independent review is to provide candid and critical comments that will assist the committee in making its published report as sound as possible, and to ensure that the report meets institutional stan- dards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberation process. The committee thanks the following individuals for their review of the draft report: B. Taylor Bennett, Management Consultant Larry Carbone, University of California—San Francisco Jerry Collins, Yale University Linda Cork, Stanford University W. Ron DeHaven, American Veterinary Medical Association Betty goldentyer, U.S. Department of Agriculture David A. Kass, Johns Hopkins University Hilton Klein, Taconic Kathy E. Laber-Laird, University of South Carolina Scott Marshall, Marshall BioResources Howard g. Rush, The University of Michigan Marty Stephens, The Humane Society of the United States Victoria Voith, Western University Craig L. Wardrip, The University of Chicago Bill yates, University of Pittsburgh The review of the report was overseen by: Peter Ward, University of Michigan Peter Raven, Missouri Botanical Garden Appointed by the NRC, these individuals were responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring Committee and the institution.

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xii PREFACE I extend my sincere appreciation to the members of this Committee, who invested considerable time, effort, and interest in this report. Although we had our distinct perspectives on “the elephant,” the individual members always remained respectful of one other and worked as a team with a uni- fied concern for animal welfare. In addition, I acknowledge the assistance of Christine Henderson. This was her first effort at assisting with an Academy report, and I trust not her last. Stephen W. Barthold, Chair Committee on Scientific and Humane Issues in the Use of Random Source Dogs and Cats in Research

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Contents Summary 1 Background, 1 Mandate and Statement of Task for the Report, 2 Characteristics of Random Source Animals for NIH-funded Research, 3 Trends and Status of Class B Animals and Dealers, 4 General Conclusions, 5 Conclusions and Recommendations, 6 Impact of Recommendations, 8 Concluding Statement, 8 Glossary of Abbreviations Used in This Report, 9 1 Introduction 11 Congressional Mandate for This Study, 11 Timeline for This NRC Study, 12 Animal Welfare Act and USDA Definitions, 12 Overview of Existing Animal Welfare Regulations and Guidelines, 16 Animal Welfare Act Provisions in Regard to Dogs and Cats, 20 Committee Approach to Its Charge, 26 Focus and Organization of This Report, 27 References, 29 xiii

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xi CONTENTS 2 The use of Dogs and Cats in Research: Public Perception and Evolution of Laws and guidelines 31 Public Perceptions of Dogs and Cats and of Their Use in Research, 32 The Animal Protection Movement, 34 Evolution of Animal Care Oversight within the Scientific Community, 35 Effects of Animal Protection Activities on Class B Dealers and on Scientific Access to Random Source Dogs and Cats, 37 History of U.S. Laws and Guidelines Regarding the Use of Dogs and Cats in Research, 37 References, 43 3 use of Random Source Dogs and Cats for Research 45 The “3Rs” Principle, 47 Desirability of Random Source Dogs and Cats for Research, 48 Random Source Dogs: Anatomic and Physiologic Attributes, 49 Random Source Cats: Anatomic and Physiologic Attributes, 55 IACUC and Principal Investigator Considerations Regarding the Use of Random Source Animals for Research, 57 Deleterious Infectious Disease Issues, 59 Zoonotic Disease Hazards among Random Source Animals, 60 Adverse Effects of Infectious Disease on Research, 61 Animal Welfare Issues, 62 References, 64 4 Class B Dealers and Animals 71 Trends in the Number of Class B Dogs and Cats Used in Research, 72 The Role of Class B Dealers in Providing Random Source Animals, 77 Trends in the Number of Class B Dealers, 78 Sources of Dogs and Cats for Class B Dealers, 78 Cost of Animals from Class B Dealers, 81 AWA Enforcement, 82 Inconsistencies in Quality among Class B Dealers, 86 Alternatives to Class B Animals, 86 Unresolved Class B Compliance Issues, 90 References, 91 5 Conclusions and Recommendations 93 APPENDIX: Committee Biographies 99