GUIDELINES FOR THE HUMANE TRANSPORTATION OF RESEARCH ANIMALS

Committee on Guidelines for the Humane Transportation of Laboratory Animals

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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GUIDELINES FOR THE HUMANE TRANSPORTATION OF RESEARCH ANIMALS Committee on Guidelines for the Humane Transportation of Laboratory Animals Institute for Laboratory Animal Research Division on Earth and Life Studies THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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THE NATIONAL ACADEMIES PRESS, 500 Fifth Street, N.W., Washington, DC 20001 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 study was supported by the Elizabeth R. Griffin Research Foundation, the National Center for Infectious Disease, and Contract No. N01-OD-4-2139, Task Order 118 between the National Institutes of Health and the National Academy of Sciences. 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. Library of Congress Cataloging-in-Publication Data Guidelines for the humane transportation of research animals / Committee on Guidelines for the Humane Transportation of Laboratory Animals, Institute for Laboratory Animal Research, Division on Earth and Life Studies. p. ; cm. Includes bibliographical references and index. ISBN 0-309-10110-7 (pbk.) 1. Laboratory animals—Transportation. I. Institute for Laboratory Animal Research (U.S.). Committee on Guidelines for the Humane Transportation of Laboratory Animals. [DNLM: 1. Animals, Laboratory—Guideline. 2. Transportation —standards—Guideline. 3. Animal Welfare—standards—Guideline. 4. Laboratory Animal Science—standards—Guideline. 5. Safety Management—standards—Guideline. QY 52 G946 2006] SF406.7.G85 2006 636.088′5—dc22 2006010872 ISBN 0-309-65724-5 (PDF) 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 Disclaimer: The Internet information and government forms referenced in this report were correct, to the best of our knowledge, at the time of publication. It is important to remember, however, the dynamic nature of the Internet. Resources that are free and publicly available one day may require a fee or restrict access the next, and the location of items may change as menus and homepages are reorganized. Copyright 2006 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 Academy 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 engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achieve- ments of engineers. Dr. Wm. A. Wulf is president 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 Institute acts under the responsibil- ity 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 Sciences 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. Wm. A. Wulf are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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This report is respectfully dedicated to the memory of CHARLES KEAN March 25, 1942 – June 25, 2004 who dedicated his life to the care of humans and animals alike v

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COMMITTEE ON GUIDELINES FOR THE HUMANE TRANSPORTATION OF LABORATORY ANIMALS Ransom L. Baldwin (Chair), University of California, Davis, California Chandra R. Bhat, University of Texas, Austin, Texas Donald H. Bouyer, University of Texas, Galveston, Texas Firdaus S. Dhabhar, Stanford University School of Medicine, Stanford, California Steven L. Leary, Washington University School of Medicine, St. Louis, Missouri John J. McGlone, Texas Tech University, Lubbock, Texas Eric Raemdonck, International Air Transport Association, Montreal, Quebec, Canada Jennie L. Smith, Yale University, New Haven, Connecticut Janice C. Swanson, Kansas State University, Manhattan, Kansas Staff Jennifer Obernier, Study Director Marsha Barrett, Project Assistant Kathleen Beil, Administrative Assistant Kori Brabham, Intern Norman Grossblatt, Senior Editor Johnny Hernandez, Intern John Horigan, Fellow Susan Vaupel, Editor vii

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INSTITUTE FOR LABORATORY ANIMAL RESEARCH COUNCIL Stephen W. Barthold (Chair), University of California, Center for Comparative Medicine, Davis, California William C. Campbell, Drew University, Madison, New Jersey Jeffrey I. Everitt, GlaxoSmithKline Research and Development, Comparative Medicine and Investigator Support, Research Triangle Park, North Carolina Michael F. Festing, Leicestershire, United Kingdom James G. Fox, Massachusetts Institute of Technology, Division of Comparative Medicine, Cambridge, Massachusetts Estelle B. Gauda, Johns Hopkins University School of Medicine, Johns Hopkins Hospital, Baltimore, Maryland Janet Gonder Garber, Pinehurst, North Carolina Coenraad F.M. Hendriksen, Netherlands Vaccine Institute, Bilthoven, The Netherlands Jon H. Kaas, Vanderbilt University, Nashville, Tennessee Jay R. Kaplan, Wake Forest University School of Medicine, Department of Pathology, Winston-Salem, North Carolina Joseph W. Kemnitz, University of Wisconsin, Primate Research Center, Madison, Wisconsin Leticia V. Medina, Abbott Laboratories, Abbott Park, Illinois Abigail L. Smith, University of Pennsylvania, University Laboratory Animal Resources, Philadelphia, Pennsylvania Stephen A. Smith, Virginia Polytechnic Institute and State University, Department of Biomedical Sciences and Pathobiology, Blacksburg, Virginia Peter Theran, Massachusetts Society for the Prevention of Cruelty to Animals, Angell Animal Medical Center, Boston, Massachusetts Staff Joanne Zurlo, Director Kathleen Beil, Administrative Assistant viii

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Preface T his project was initiated in response to a letter from Charles Kean, an Associate Professor of Physiology and Pharmacology and Director of the Animal Care Facility at Loma Linda University, to the National Research Council’s (NRC’s) Institute for Laboratory Animal Research (ILAR), the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC) International, and the Office of Laboratory Animal Welfare (OLAW) of the National Institutes of Health (NIH) outlining the research animal care community’s concerns about the safe and humane transportation of research animals. Dr. Kean requested that those organizations look into the transportation of research animals and into issues that were adversely affecting animal welfare. In response, ILAR hosted a meeting of various stakeholders to identify and discuss important issues in the transportation of research animals. The meeting was funded by NIH and included representatives of the scientific com- munity, professional veterinary organizations, regulatory and accrediting agencies, animal breeders, and the transportation industry. Special thanks are due to the following for participating in the meeting, which took place December 4, 2001: Kathryn Bayne, AAALAC International Frank Black, Air Transportation Association of America, Inc. Ralph Dell, ILAR Nelson Garnett, OLAW James Geistfeld, Taconic Farms, Inc. Charles Kean, Loma Linda University ix

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x PREFACE Carl Kole, United Airlines J. Michael Krop, US Postal Service Steven Leary, Washington University Emilie Rissman, University of Virginia Robert Russell, Harlan Sprague Dawley, Inc. James Taylor, Office of Animal Care and Use, NIH Richard Watkins, US Department of Agriculture (USDA) Animal and Plant Health Inspection Service William White, Charles River Laboratories The meeting delineated the problems encountered during and result- ing from air and ground transportation of live animals. The participants also focused on mechanisms to solve the problems, including the poten- tial for a future ILAR study. As a result of this meeting, the Elizabeth R. Griffin Research Foundation, NIH, and the National Center for Infectious Diseases sponsored an ILAR committee to address problems associated with transportation of research animals and produce a report that includes recommendations intended for government agencies as well as for indi- vidual investigators/animal facility managers who may need to ship animals in the future. Transportation of research animals may raise concerns related to the well-being of the animals and concerns about how animals are affected by general environmental conditions. These concerns often depend on the species being transported. Shipments from breeders to research institu- tions are generally well executed through the use of company-owned fleets of environmentally controlled vehicles, but arranging transport from vendors without established transport systems, or between research insti- tutions, can be challenging. Animals may be shipped in vehicles without controlled environments and could be subjected to extreme temperatures. Specific requests for temperature-controlled vehicles may not be honored because the shipper may not have temperature-controlled vehicles avail- able or the request may not have been passed on to a subcontractor hired by the shipper to transport the animals. The USDA has regulatory juris- diction and inspection authority over transportation of animals through the Animal Welfare Act. However, most animals shipped are rats and mice, which are not covered under the act. The Public Health Service, whose oversight does include those species, does not inspect research animal transportation activities unless a complaint is filed. The major problem in transporting nonhuman primates is that few airlines are willing to carry the animals. International shipment, the most common transportation of nonhuman primates, is often delayed by a cumbersome, multiagency permitting process involving the USDA Vet-

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xi PREFACE erinary Service, US Fish and Wildlife Service, the Centers for Disease Control and Prevention (CDC), and the Department of Transportation (DOT). Airlines have little incentive to carry the animals because it is not profitable and workers must wear protective clothing when handling them. The latter is disturbing both for workers and for travelers who see them. Finally, many animal rights activists have successfully lobbied the airlines to stop transporting nonhuman primates nationally and internationally. Transportation of research animals is an essential component of the research enterprise. The integrity and well-being of the animals being transported are necessary for the quality of the research and the welfare of the animals. The lack of clear guidelines that cover all species can cause confusion for individuals without extensive experience in arranging trans- portation for research animals. In addition, investigators may find it difficult to identify a responsible shipper that will arrange for appropriate caging, inclusion of food and water, and other animal needs during transportation. In the aftermath of the bioterror incidents involving anthrax in the fall of 2001, the possibility that research animals will be used to carry or dis- seminate bioterrorism agents must be considered. Breaches in good trans- portation practices, either purposeful or accidental, could result in the spread of infectious agents. In addition, new legislation (such as the Animal Health Protection Act of 2002) and several guidelines related to homeland security have the potential to complicate the importing, export- ing, and transportation of animals and specimens for biomedical research. The issues identified in the preceding statements led to appointment of the ILAR Committee on Guidelines for the Humane Transportation of Laboratory Animals. The committee held three meetings—in April, Sep- tember, and December 2004. During the course of its deliberations, the committee sought assistance from many people, who gave generously of their time to provide valuable advice and information that were used in its deliberations. Special thanks are due to the following: Richard Phelan, Taconic Farms, Inc. Bonnie P. Dalton, Science Directorate, Ames Research Center, National Aeronautics and Space Administration Gale Galland, Division of Global Migration and Quarantine, National Center for Infectious Diseases Frank Kohn, FWS John Monetti, World Courier Erik Liebegott, Transportech, LLC Robert Fernandez, Direct Services William White, Charles River Laboratories

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xii PREFACE Carol Wigglesworth, OLAW Bobby Brown, CDC Carl Kole, Special Cargos, United Airlines Charles Kean, Animal Research Facility, Loma Linda University Barbara Kohn, Office of Animal Care, USDA Eileen Edmonson, Office of Hazardous Materials Safety, DOT The report has been reviewed in draft form by individuals chosen for their diverse perspective and technical expertise, in accordance with pro- cedures approved by the NRC’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integ- rity of the deliberative process. We wish to thank the following individuals for their review of the report: Susan Eicher, Purdue University, West Lafayette, IN Steven Griffey, University of California, Davis, CA Kathleen Hancock, Virginia Polytechnic University, Alexandria, VA Barbara Hansen, All Children’s Hospital, St. Petersburg, FL Donald Lay, Purdue University, West Lafayette, IN Tim Morris, GlaxoSmithKline, United Kingdom William Morton, Paris NHP, Edmonds, WA Barbara Orlans, Georgetown University, Washington, DC Frankie Trull, National Association for Biomedical Research, Washington, DC William White, Charles River Laboratories, Wilmington, MA Walter Woolf, Air Animal, Tampa, FL Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the conclu- sions or recommendations, nor did they see the final draft of the report before its release. The review of the report was overseen by: Johanna Dwyer, Tufts University, Boston, MA Steven Pakes, University of Texas Southwestern Medical Center and VA North Texas Health Care System, Dallas, TX Appointed by the NRC, they were responsible for making certain that an independent examination of the report was carried out in accordance

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xiii PREFACE with institutional procedures and that all review comments were care- fully considered. Responsibility for the final content of the report rests entirely with the authoring committee and the institution. Ransom L. Baldwin, Chair Committee on Guidelines for the Humane Transportation of Laboratory Animals

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Contents TABLES AND FIGURES xvii ABBREVIATIONS AND ACRONYMS xix SUMMARY 1 Major Recommendations, 3 1 INTRODUCTION 7 2 REGULATIONS AND GUIDELINES FOR THE TRANSPORTATION OF RESEARCH ANIMALS 11 National Regulations and Guidelines, 11 Department of Agriculture, 14 US Fish and Wildlife Service, 14 Centers for Disease Control and Prevention, 18 US Department of Transportation, 20 Public Health Service, 21 Food and Drug Administration, 21 State Health and Agricultural Regulations, 22 International Regulations for Transporting Research Animals, 22 CITES, 23 International Civil Aviation Organization, 25 International Air Transport Association, 27 World Animal Health Organization, 28 The European Union, 29 xv

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xvi CONTENTS 3 GOOD PRACTICES IN THE TRANSPORTATION OF RESEARCH ANIMALS 33 Stress During Transportation, 34 Allometric Scaling and Implication for Transportation Practices, 38 Thermal Environment, 39 Space Allocation, 52 Food and Water, 54 Social Interaction and Group Transportation, 59 Handling, 59 Monitoring Transportation, 60 Emergency Procedures, 61 Personnel Training, 61 4 BIOSECURITY 65 Protecting Public Health and Agricultural Resources, 66 Protecting the Biological Integrity of Research Animals and Colonies, 71 5 RECOMMENDATIONS 81 REFERENCES 89 APPENDIXES A SUMMARY OF THE ANIMAL WELFARE ACT REGULATIONS PERTAINING TO TRANSPORTATION 97 Dogs and Cats (9 CFR 3.13 – 3.19), 97 Nonhuman Primates (9 CFR 3.86-3.92), 104 Guinea Pigs and Hamsters, Rabbits, and Other Animals (9 CFR 3.35-3.41, 9 CFR 3.60-3.65, 9 CFR 3.136 – 3.142), 110 B PATTERNS IN THE GROUND TRANSPORTATION OF RESEARCH ANIMALS IN THE UNITED STATES 117 Background, 117 Data Preparation, 118 Quantitative Analysis, 119 Empirical Results, 120 Summary, 126 ABOUT THE AUTHORS 127 INDEX 131

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Tables and Figures TABLE 1-1 Checklist of Issues to Consider When Arranging Transportation Between Research Facilities 10 TABLE 2-1 Federal Statutes/Programs Relevant to the Transportation of Vertebrate Research Animals and Products in the United States 12 TABLE 2-2 Designated Port for Importation or Exportation of Wildlife or Derivatives 16 TABLE 2-3 Endangered Species Act Listed Species of Nonhuman Primates 17 TABLE 2-4 Permitting Requirements Under CITES 25 TABLE 2-5 CITES Listed Species of Nonhuman Primates 26 TABLE 2-6 Checklist of Research Animal Regulations and Guidelines 31 TABLE 3-1 Thermoregulation Data on Common Research Animal Species 40 FIGURE 3-1 Graph representing relationship between metabolic rate and ambient temperature in homeotherms. 42 FIGURE 3-2 Changes in thermoneutral zone (range of ambient temperatures at which an animal’s heat production is at a minimum) with age and size in chickens. 43 FIGURE 3-3 TNZ of various agricultural animals. 44 TABLE 3-2 Ambient Temperature Ranges for Safe Transportation of Common Adult Research Animals 48 xvii

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xviii TABLES AND FIGURES TABLE 3-3 Effects of Various Factors on Effective Environmental Temperature and Relative Risk to Animal Health and Welfare 49 TABLE 3-4 Behavioral and Physiological Signs of Thermal Status 52 TABLE 3-5 Space Allowances for Group-Transported Animals 55 FIGURE 3-4 Space allowances during transportation. 57 TABLE 4-1 Agents and Toxins That Require Registration of the Facility with CDC 67 TABLE 4-2 Elements of an Emergency Plan 68 TABLE 4-3 Characteristics of a Good Shipper 68 TABLE 4-4 Examples of Zoonotic Diseases Transmissible from Research Animals to Humans 69 TABLE 4-5 Infectious Agents and the Susceptible Species of Research Animals 72 TABLE 4-6 Recommendations for Shipment of Research Animals Between Institutions 76 FIGURE 5-1 Locations of research facilities using nonhuman primates, major importation sites, and vendors of nonhuman primates in the United States. 83 FIGURE B-1 Candidate set for the facility-location problem. 121 FIGURE B-2 Solution set for the facility location problem for the NIH grants data set (rodents). 122 TABLE B-1 Total Weighted-System Travel-Distance Reduction with Increase in Supply Points for NIH Grants Data Set (Rodents) 123 TABLE B-2 Total Weighted-System Travel-Distance Reduction with Increase in Supply Points for USDA Cats Data Set 123 FIGURE B-3 Solution set for the facility location problem for the USDA cats data set. 124 FIGURE B-4 Solution set for the facility location problem for the USDA dogs data set. 125 TABLE B-3 Total Weighted-System Travel-Distance Reduction with Increase in Supply Points for USDA Dogs Data Set 126

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Abbreviations and Acronyms AAALAC Association for Assessment and Accreditation of Laboratory Animal Care International AATA Animal Transportation Association APHIS Animal and Plant Health Inspection Service AVMA American Veterinary Medical Association AWA Animal Welfare Act BMBL Biosafety in Microbiological and Biomedical Laboratories CDC Centers for Disease Control and Prevention CITES Convention on International Trade in Endangered Species of Wild Fauna and Flora DGMQ Division on Global Migration and Quarantine DRGs Dangerous Goods Regulations DOT Department of Transportation EAIPP Etiologic Agent Import Permit Program EDIM Group A rotavirus ESA Endangered Species Act EU European Union FASS Federation of Animal Science Societies FDA Food and Drug Administration xix

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xx ABBREVIATIONS AND ACRONYMS FY fiscal year FWS Fish and Wildlife Service GD-VII Theiler’s murine encephalomyelitis virus strain GIS Geographic Information System HANT Hantaan HEPA high-efficiency particulate air (filters) HMR Hazardous Materials Regulation HPA hypothalamic pituitary adrenal axis IATA International Air Transport Association ICAO International Civil Aviation Organization ILAR Institute for Laboratory Animal Research KRV Kilham Rat virus LARS Live Animals Regulations LCM Lymphocytic choriomeningitis LCMV Lymphocytic choriomeningitis virus LCT lower critical temperature MAD Mouse adenovirus MCMV Murine cytomegalovirus MHV Mouse hepatitis virus MPV (OPV) Mouse parvovirus (Orphan parvovirus) MTLV Mouse thymic virus MVM Minute virus of mice NAP National Academies Press NCRR National Center for Research Resources NIH National Institutes of Health NPRC National Primate Research Center NRC National Research Council OIE Office International des Épizooties OLAW Office of Laboratory Animal Welfare PhRMA Pharmaceutical Research and Manufacturers of America PHS Public Health Service PPE personal protective equipment PVM pneumonia virus of mice

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ABBREVIATIONS AND ACRONYMS xxi REO 3 Reovirus type 3 RHD Rabbit haemorrhagic disease RPV (OPV) Rat parvovirus (Orphan parvovirus) RRV Ross River virus SARS Sudden Acute Respiratory Syndrome SDA/RCV Sialodacryoadentitis virus/Rat corona virus SIV Simian immunodeficiency virus SPS Agreement Agreement on the Application of Sanitary and Phytosanitary Measures TNZ thermoneutral zone UCT upper critical temperature USDA US Department of Agriculture WTO World Trade Organization

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