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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Page viii Cite
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing-Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25356.
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PREPUBLICATION COPY Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing–Based Biomedical Research PROCEEDINGS OF A WORKSHOP Anne Frances Johnson and Lida Anestidou, Rapporteurs Roundtable on Science and Welfare in Laboratory Animal Use Institute for Laboratory Animal Research Division on Earth and Life Studies

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This project was supported by the American Veterinary Medical Association; Association of Primate Veterinar- ians; Baylor College of Medicine; Broad Institute; Charles River Laboratories; Emory University; Genentech; GlaxoSmithKline; Indiana University; Japan Agency for Medical Research and Development; Johns Hopkins University; Johnson & Johnson/Janssen Pharmaceuticals; Janssen Research & Development, LLC; Massachusetts General Hospital; Massachusetts Institute of Technology; Medical College of Wisconsin; MedImmune; Merck and Co., Inc.; MIT McGovern Institute; National Institutes of Health (Contract No HHSN263201800029I; Task Order HHSN26300016); National Primate Research Centers; Novartis; Pfizer Inc.; University of Miami; Univer- sity of Michigan; University of Pittsburgh; Wisconsin National Primate Research Center; and Yale University. Funding for this workshop was made possible, in part, by the U.S. Department of Agriculture through grant AP17AC000000G004 and the U.S. Food and Drug Administration through grant 5 R13 FD 005298-05. Views expressed in written workshop materials or publications and by speakers or moderators do not necessarily reflect the official policies of the U.S. Department of Health and Human Services; nor does any mention of trade names, commercial practices, or organizations imply endorsement by the U.S. government. This material is based on work supported by the National Science Foundation under Grant No. IOS-1639899. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. Any opinions, findings, conclusions, or recommendations ex- pressed in this publication do not necessarily reflect the views of any organization or agency that provided sup- port for the project. Digital Object Identifier: https://doi.org/10.17226/25356 Additional copies of this publication are available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2019 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Cover credit: Illustrations copyright 2013, Stephen D. Nash/IUCN SSC Primate Specialist Group. Used with permission. Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2019. Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing–Based Biomedical Research: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: https://doi.org/10.17226/25356. Prepublication Copy

The National Academy of Sciences was established in 1863 by an Act of Congress, signed by President Lincoln, as a private, nongovernmental institution to advise the nation on issues re- lated to science and technology. Members are elected by their peers for outstanding contribu- tions to research. Dr. Marcia McNutt is president. The National Academy of Engineering was established in 1964 under the charter of the National Academy of Sciences to bring the practices of engineering to advising the nation. Mem- bers are elected by their peers for extraordinary contributions to engineering. Dr. C. D. Mote, Jr., is president. The National Academy of Medicine (formerly the Institute of Medicine) was established in 1970 under the charter of the National Academy of Sciences to advise the nation on medical and health issues. Members are elected by their peers for distinguished contributions to medicine and health. Dr. Victor J. Dzau is president. The three Academies work together as the National Academies of Sciences, Engineering, and Medicine to provide independent, objective analysis and advice to the nation and conduct other activities to solve complex problems and inform public policy decisions. The National Academies also encourage education and research, recognize outstanding contributions to knowledge, and increase public understanding in matters of science, engineering, and medicine. Learn more about the National Academies of Sciences, Engineering, and Medicine at www. nationalacademies.org. Prepublication Copy

Consensus Study Reports published by the National Academies of Sciences, Engineering, and Medicine document the evidence-based consensus on the study’s statement of task by an au- thoring committee of experts. Reports typically include findings, conclusions, and recommen- dations based on information gathered by the committee and the committee’s deliberations. Each report has been subjected to a rigorous and independent peer-review process and it rep- resents the position of the National Academies on the statement of task. Proceedings published by the National Academies of Sciences, Engineering, and Medicine chronicle the presentations and discussions at a workshop, symposium, or other event convened by the National Academies. The statements and opinions contained in proceedings are those of the participants and are not endorsed by other participants, the planning committee, or the National Academies. For information about other products and activities of the National Academies, please visit www.nationalacademies.org/about/whatwedo. Prepublication Copy

PLANNING COMMITTEE ON CARE, USE, AND WELFARE OF MARMOSETS AS ANIMAL MODELS FOR GENE EDITING–BASED BIOMEDICAL RESEARCH: A WORKSHOP Members Saverio “Buddy” Capuano III, University of Wisconsin–Madison (Co-Chair) James G. Fox, Massachusetts Institute of Technology (Co-Chair) Jaco Bakker, Biomedical Primate Research Centre Marina Emborg, University of Wisconsin–Madison Eric Hutchinson, Johns Hopkins University School of Medicine James Pickel, National Institutes of Mental Health Erika Sasaki, Central Institute for Experimental Animals Suzette Tardif, Southwest National Primate Research Center Prepublication Copy v

ROUNDTABLE ON SCIENCE AND WELFARE IN LABORATORY ANIMAL USE Chair Robert C. Dysko, University of Michigan Liaison to ILAR Council Paul A. Locke, Johns Hopkins Bloomberg School of Public Health Members Jill Ascher, National Institutes of Health Szczepan Baran, Novartis Institutes for Biomedical Research, Inc. Bonnie V. Beaver, Texas A&M University Cindy Buckmaster, Baylor College of Medicine Saverio (Buddy) Capuano III, University of Wisconsin–Madison Carol Clarke, U.S. Department of Agriculture Michael DuVall, Janssen Pharmaceuticals James G. Fox, Massachusetts Institute of Technology Gloria J. Gaito, Pfizer Worldwide Research and Development Alema Galijatovic-Idrizbegovic, Merck & Co., Inc. Gail C. Golab, American Veterinary Medical Association Debra L. Hickman, Indiana University School of Medicine Michael Huerkamp, Emory University Donna Matthews Jarrell, Massachusetts General Hospital Bruce W. Kennedy, Chapman University David M. Kurtz, National Institute of Environmental Health Sciences Margaret S. Landi, GlaxoSmithKline Joseph T. Newsome, University of Pittsburgh Lori Palley, Massachusetts General Hospital Patricia Preisig, Yale University Brianna L. Skinner, U.S. Food and Drug Administration Edda (Floh) Thiels, National Science Foundation Joseph Thulin, Medical College of Wisconsin Patricia V. Turner, Charles River Laboratories Rhonda J. Wiler, Genentech Axel Wolff, National Institutes of Health Robert H. Wurtz, National Institutes of Health Julia Zaias, University of Miami Staff Lida Anestidou, Director, Roundtable on Science and Welfare in Laboratory Animal Use Teresa Sylvina, Director, Institute for Laboratory Animal Research Tamara Dawson, Senior Program Assistant, Board on Environmental Sciences and Toxicology (September-November 2018) Keiona Jones, Senior Program Assistant, Institute for Laboratory Animal Research (from December 2018) Consultant Anne Frances Johnson, Writer vi Prepublication Copy

INSTITUTE FOR LABORATORY ANIMAL RESEARCH Council Members Margaret S. Landi, Chief of Animal Welfare, Ethics and Strategy, GlaxoSmithKline (Chair) Karin Blumer, Scientific Affairs, Novartis International AG Cory Brayton, Associate Professor of Molecular and Comparative Pathobiology, Johns Hopkins University Joseph J. DeGeorge, Principal Partner, Bianca Holdings, LLC Michael DuVall, Scientific Director, Head of Toxicology and Laboratory Animal Medicine, Johnson & Johnson, Janssen Pharmaceuticals Lewis B. Kinter, Independent Consultant Paul A. Locke, Associate Professor, Department of Environmental Health and Engineering Director, DrPH Program in Environmental Health Sciences, Johns Hopkins Bloomberg School of Public Health James A. Roth, Clarence Hartley Covault Distinguished Professor, Director, Center for Food Security and Public Health, College of Veterinary Medicine, Iowa State University Lawrence B. Schook, Edward William and Jane Marr Gutsgell Professor of Animal Sciences and Radiology, University of Illinois at Urbana-Champaign Staff Teresa Sylvina, Director Lida Anestidou, Senior Program Officer Keiona Jones, Senior Program Assistant Prepublication Copy vii

Acknowledgments This Proceedings of a Workshop was reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and crit- ical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published proceedings as sound as possible and to ensure that it meets the institutional standards for quality, objectivity, evidence, and responsiveness to the charge. The review comments and draft manuscript remain confidential to protect the integrity of the process. We thank the following individuals for their review of this proceedings: Lynn C. Anderson, Consultant Tamara Berdyyeva, Janssen R&D US Kent Lloyd, University of California, Davis Suzette D. Tardif, Southwest National Primate Research Center Robert Wurtz, National Eye Institute Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the content of the proceedings nor did they see the final draft before its release. The review of this proceedings was overseen by Jeff Everitt, Duke University, and Stephen Barthold, University of California, Davis (emeritus). They were responsible for making certain that an independent examination of this proceedings was carried out in accordance with standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the rapporteurs and the National Academies. The support of the Roundtable on Science and Welfare in Laboratory Animal Use was vital to the planning and conduct of the workshop on Care, Use, and Welfare of Marmosets as Animal Models for Gene Editing–Based Biomedical Research. Federal sponsors are the National Science Foundation, the U.S. De- partment of Agriculture, and the U.S. Food and Drug Administration. Nonfederal sponsorship was provided by the American Veterinary Medical Association; Baylor College of Medicine; Charles River Laboratories; Emory University; Genentech; GlaxoSmithKline; Indiana University; Johns Hopkins University; Johnson & Johnson/Janssen Pharmaceuticals; Massachusetts General Hospital; Massachusetts Institute of Technol- ogy; Medical College of Wisconsin; MedImmune; Merck and Co., Inc.; National Primate Research Centers; Novartis; Pfizer Inc.; University of Miami; University of Michigan; University of Pittsburgh; and Yale University. The Roundtable on Science and Welfare in Laboratory Animal Use expresses deep gratitude to the members of the planning committee for developing an expansive and multifaceted workshop agenda and to the expert speakers who took part in the workshop’s discussions. Prepublication Copy ix

 

Contents 1 INTRODUCTION........................................................................................................................................ 1 Workshop Statement of Task, 1 2 CONTEXT FOR THE USE OF MARMOSETS AS ANIMAL MODELS ............................................. 3 History, 3 Current Use and Key Advantages, 3 Key Challenges, 5 References, 5 3 ETHICAL CONSIDERATIONS ............................................................................................................. 6 Theoretical Considerations, 6 Practical Considerations, 9 Discussion, 10 References, 12 4 CURRENT RESEARCH APPLICATIONS ........................................................................................ 14 Neuroscience, 14 Aging, 19 Infectious Disease, 22 Gene Editing and Transgenic Animals, 24 Discussion, 25 References, 25 5 MARMOSET GENOMICS AND GENETIC DIVERSITY .............................................................. 27 Characterizing the Marmoset Genome, 27 Genetic Diversity in Marmosets, 29 References, 32 6 MARMOSET SUPPLY AND AVAILABILITY ................................................................................. 34 Marmosets in the Wild, 34 Breeding and Transportation, 36 References, 40 7 MARMOSET CARE AND MANAGEMENT ..................................................................................... 41 Routine Care, 41 Diet, 43 Habits and Environment, 45 Reproduction, 46 Disease Prevention and Management, 48 Pain Prevention and Management, 51 Discussion, 53 References, 53 8 FINAL REMARKS .................................................................................................................................. 56 Prepublication Copy xi

Contents APPENDIXES A WORKSHOP AGENDA ......................................................................................................................... 58 B PROFESSIONAL BIOSKETCHES ...................................................................................................... 63 FIGURES 2-1 Areas of focus for research using tamarins and marmosets over the decades, 4 2-2 Number of citations on PubMed that include the term marmosets, 1960 to the present, 4 4-1 Comparison of brain characteristics of humans, macaques, marmosets, and mice, 15 4-2 Anatomical in vivo T1w-MPRAGE 150 µm3 MRI of the normal marmoset brain, 16 4-3 Schematic of cradle setup for performing fMRI on conscious awake marmosets, 16 4-4 Test methods and biomarkers for the progression of Parkinson’s disease in marmosets, 18 4-5 Causes of death in marmosets older than 6 years of age and younger than 6 years of age at Southwest National Primate Research Center, 20 5-1 Genetic analyses show clusters of genetic similarity within each research center, 31 6-1 Marmoset genera Callithrix and Mico, 35 6-2 Legal protections for captive primates in Latin America, 37 6-3 U.S. imports of macaques and marmosets, 2010-2017, 38 xii Prepublication Copy

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The marmoset, a type of small monkey native to South America, is a research model of increasing importance for biomedical research in the United States and globally. Marmosets offer a range of advantages as animal models in neuroscience, aging, infectious diseases, and other fields of study. They may be particularly useful for the development of new disease models using genetic engineering and assisted reproductive technologies. However, concerns have been voiced with respect to the development of new marmoset-based models of disease, ethical considerations for their use, the supply of marmosets available for research, and gaps in guidance for their care and management.

To explore and address these concerns, the Roundtable on Science and Welfare in Laboratory Animal Use hosted a public workshop on October 22-23, 2018, in Washington, DC. The workshop focused on the availability of marmosets in the United States and abroad; animal welfare and ethical considerations stemming from the use of wildtype and genetically modified marmosets; and standards of housing and care, dietary needs, and feeding requirements for marmosets in captivity. This publication summarizes the presentations and discussions from the workshop.

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