American College of Laboratory Animal Medicine Series StevenH.Weisbroth,Ronald E. Flatt, and Alan L. Kraus, eds.: The Biology ofthe LaboratoryRabbit, 1974 JosephE. Wagner andPatrickJ.Manning, eds.: The Biology ofthe Guinea Pig,1976 Edwin J. Andrews, Billy C. Ward, and Norman H.Altman, eds.: Spontaneous AnimalModels ofHuman Disease, Volume 1,1979;Volume II, 1979 Henry J.Baker, J.RussellLindsey,and StevenH.Weisbroth,eds.: The LaboratoryRat, Volume I:Biologyand Diseases,1979; Volume II: ResearchApplications, 1980 Henry L. Foster,J. DavidSmall,and James G.Fox, eds.: The Mouse inBiomedical Research,Volume I:History, Genetics,andWild Mice, 1981; Volume II: Diseases,1982; VolumeIll:NormativeBiology,Immunology,andHusbandry,1983;VolumeIV:ExperimentalBiologyandOncology, 1982 James G.Fox, BennettJ. Cohen, andFranklinM. Loew,eds.: LaboratoryAnimal Medicine, 1984 G.L. Van Hoosier, Jr., and Charles W.McPherson, eds.: LaboratoryHamsters, 1987 Patrick J.Manning,DanielH. Ringler, and Christian E. Newcomer, eds.: The Biology ofthe LaboratoryRabbit, 2ndEdition, 1994 B. TaylorBennett, ChristianR. Abee, andRoy Henrickson, eds.: Nonhuman PrimatesinBiomedical Research,Volume I:Biology and Management, 1995; VolumeII: Diseases,1998 Dennis F. Kohn, SallyK. Wixson,William J. White, and G.John Benson, eds.: AnesthesiaandAnalgesia inLaboratoryAnimals,1997 James G.Fox, Lynn C. Anderson, Franklin M.Loewand Fred W. Quimby,eds.: LaboratoryAnimal Medicine, 2nd Edition,2002 Mark A.Suckow,StevenH.Weisbroth andCraigL. Franklin,eds.: The LaboratoryRat, 2ndEdition, 2006 James G.Fox, Muriel T.Davisson, Fred W. Quimby, StephenW.Barthold, ChristianE. Newcomerand Abigail L. Smith,eds.: The Mouse inBiomedical Research,2nd Edition,Volume I:History, WildMice, and Genetics, 2007; Volume II: Diseases, 2007; Volume III:Normative Biology, Husbandry,andModels, 2007; Volume IV:Immunology,2007 RichardE. Fish, Marilyn J.Brown, PeggyJ. Dannemanand Alicia Z. Karas, eds.: AnesthesiaandAnalgesia inLaboratoryAnimals,2nd Edition, 2008 Jack R. Hesslerand Noel D.M. Lehner, eds.: Planning and DesigningAnimal ResearchFacilities,2009 Mark A.Suckow,Karla A. Stevens,and Ronald P. Wilson,eds.: The LaboratoryRabbit,Guinea Pig,HamsterandotherRodents, 2011 Christian R. Abee,Keith Mansfield, Suzette Tardif and Timothy Morris,eds.: Nonhuman PrimatesinBiomedical Research,2nd Edition,Volume I:Biology and Management, 2012; Volume II: Diseases, 2012 KathrynBayneand Patricia V. Turner, eds.: LaboratoryAnimal Welfare, 2012 Nonhuman Primates in Biomedical Research Volume 1: Biology and Management Second Edition Edited by Christian R. Abee University of Texas, MDAnderson Cancer Center, Michale E. Keeling Center for Comparative Medicine and Research, Bastrop, Texas Keith Mansfield Novartis Institutes for Biomedical Research, Cambridge, Massachusetts Suzette Tardif University of Texas Health Science Center, Barshop Institute of Longevity & Aging Studies, San Antonio, Texas Timothy Morris School of Veterinary Medicine and Science, University of Nottingham, United Kingdom AMSTERDAMlBOSTONlHEIDELBERGlLONDONlNEWYORKlOXFORDlPARIS SANDIEGOlSANFRANCISCOlSINGAPORElSYDNEYlTOKYO AcademicPressisanImprintofElsevier AcademicPressisanimprintofElsevier 32JamestownRoad,LondonNW17BY,UK 225WymanStreet,Waltham,MA02451,USA 525BStreet,Suite1800,SanDiego,CA92101-4495,USA Firstedition1995 Secondedition2012 Copyright(cid:1)2012ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproduced,storedinaretrievalsystemortransmittedinanyformorbyanymeanselectronic, mechanical,photocopying,recordingorotherwisewithoutthepriorwrittenpermissionofthepublisher PermissionsmaybesoughtdirectlyfromElsevier’sScience&TechnologyRightsDepartmentinOxford,UK:phone(+44)(0)1865 843830;fax(+44)(0)1865853333;email:[email protected],visittheScienceandTechnologyBookswebsiteat www.elsevierdirect.com/rightsforfurtherinformation Notice Noresponsibilityisassumedbythepublisherforanyinjuryand/ordamagetopersonsorpropertyasamatterofproductsliability, negligenceorotherwise,orfromanyuseoroperationofanymethods,products,instructionsorideascontainedinthematerial herein.Becauseofrapidadvancesinthemedicalsciences,inparticular,independentverificationofdiagnosesanddrugdosages shouldbemade BritishLibraryCataloguing-in-PublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress ISBN:978-0-12-415833-7set ISBN:978-0-12-381365-7volume1 ISBN:978-0-12-381366-4volume2 ForinformationonallAcademicPresspublicationsvisit ourwebsiteatwww.elsevierdirect.com TypesetbyTNQBooksandJournals PrintedandboundinCanada 12131415 10987654321 Preface Biomedicalresearchusingnonhumanprimatescontinuesto usesofnonhumanprimates.Planningforthesecondedition provide important insights into the pathogenesis and treat- began with the return of Christian Abee as an editor mentofdiseasesthatimpacthumanhealth.Inrecentyears, followed by Keith Mansfield, Suzette Tardif, and Timothy translational research has become an increasingly empha- Morrisasco-editors. sized area in biomedical research.This emphasison trans- Theeditorsreviewedthefirsteditiontodeterminethose lating discoveries made in basic research into treatments chapters that should be repeated with careful attention to thatareusefultopatientsrequiresanimalmodelsthatallow chapters that required major revisions and those that scientists to predict human responses. Nonhuman primates required less extensive updating. The editors agreed that have long been recognized as important models for trans- the text should have a more international perspective and lational research due to their phylogenetic proximity to chapters should be added that describe research areas in humanbeingsandtheirsimilarityinresponsestotreatment which nonhuman primates play a critical role. Therefore, and pathogenesis of disease when compared to patients thissecondeditionhasaddedchaptersthatprovideamore subsequently observed in clinical trials. For these reasons, internationalperspectiveonregulatoryoversightofthecare the American College of Laboratory Animal Medicine and use of nonhuman primates and chapters that describe (ACLAM)recognizedtheneedforanauthoritativetextbook important model systems and research areas. High-resolu- on the biology, management, and diseases of nonhuman tion color images have been included in this edition that primatesusedinbiomedicalresearch. illustrate gross and microscopic lesions characteristic of ThefirsteditionofNonhumanPrimatesinBiomedical diseases of nonhuman primates. Color illustrations have Research was edited by B. Taylor Bennett, Christian R. alsobeenincludedofimagingtechniquesthatcanbeused Abee,andRoyV.Henricksonaspartofthetextbookseries in both clinical veterinary medical care and research sponsoredbytheAmericanCollegeofLaboratoryAnimal applications. Medicine. It was published in two volumes, Biology and Theeditorsassembledanoutstandinggroupofchapter Management(1995)andDiseases(1998).Thecompletion contributors with many chapter authors from the first of the first edition required more than 10 years to plan, editioncontributingonceagain.Chaptermanuscriptswere develop,edit,andpublish.Ithasservedasaseminaltextin peer reviewed by experts in the respective subject areas. the field because it provided readers with the collective The reviewers of chapters provided a very important knowledge of experts in veterinary medicine, laboratory contributionbyhelpingtomakecertainthatchapterswere animalmedicine, comparativemedicine,and primatology accurate and fair in their review of the subject areas. as these disciplines are applied to the care and use of Reviewersarelistedineachrespectivevolume,butarenot nonhuman primates in biomedical research. The first identified with the specific chapter they reviewed. editionisnolongerinprintandusedcopieshavebecome Nonhuman Primates in Biomedical Research 2nd collector’s items selling for more than the original editionprovidesacomprehensiveandcurrentreviewofthe purchaseprice.ThisprovidedthePublicationsCommittee collective knowledge of the biology, management, of the American College of Laboratory Animal Medicine diseases, and research uses of nonhuman primates. The withstrongjustificationtoapprovethedevelopmentofthis information in these volumes will be useful to clinical second edition of this important text. veterinarians, veterinary pathologists, primate caregivers PlanningforthesecondeditionofNonhumanPrimates andcolonymanagers,scientistswhoworkwithnonhuman inBiomedicalResearchbeganin2006.Althoughmuchof primates, and others who wish to know more about the information in the first edition remains useful, there nonhuman primates. have been major advances in our understanding of the Chris Abee, Keith Mansfield, Suzette Tardif, and biology, veterinary medical care, pathology, and research Timothy Morris vii Acknowledgments There are many people deserving of recognition for their copyediting by Elsevier. The editors want to give special many hours of dedicated service in planning, developing, thankstoMaryPreapatElsevierforhergentlepressureto and editing Nonhuman Primates in Biomedical Research keep us as close as possible to our deadlines and her 2nd edition. The editors wish to thank Laura Zapalac and timely responses to the book editors’ questions and Jennifer Kurtz at the Michale E. Keeling Center for requests. And finally, I would like to thank my co-editors, Comparative Medicine and Research of the University of Keith Mansfield, Suzette Tardif, and Tim Morris for their Texas MD Anderson Cancer Center for the many hours tireless efforts to make certain that this second edition of they devoted to scheduling editors’ conference calls, Nonhuman PrimatesinBiomedical Researchmet the high maintaining spreadsheets that allowed the editors to standard expected of the American College of Laboratory follow the progress of each chapter through the arduous Animal Medicine “Blue Book” series. The completion of processofcomposition,chapterreview,authors’revisions, this second edition was truly a team effort and a team first copyedit, and finally, submission of each chapter to accomplishment of the chapter contributors, the chapter Elsevier. We are also grateful to Rachel Tardif for her reviewers, the book editors, administrative staff, and the outstanding efforts in the initial copyedit of most of the staff at Elsevier. chapters. Her work allowed the editors to identify and Chris Abee correct mistakes in chapter manuscripts prior to final ix Reviewers Karyn L. Armstrong Covance Research Products, Inc., Jeffrey D. Fortman University of Illinois at Chicago, Alice, TX Biologic Resources Laboratory, Chicago, IL Lynne M. Ausmann Tufts University, Jean Mayer USDA Margaret H. Gilbert Tulane University, Tulane National Human Nutrition Research Center on Aging, Boston, Primate Research Center, Covington, LA MA Colin Groves Australian National University, Canberra, Michael B. Ballinger Amgen, Inc., Thousand Oaks, CA ACT, Australia Kathryn Bayne Association for Assessment and Patrick W. Hanley The University of Texas MD Accreditation of Laboratory Animal Care (AAALAC) Anderson Cancer Center, Michale E. Keeling International, Frederick, MD Center for Comparative Medicine and Research, Bastrop, TX Mollie Bloomsmith Emory University, Yerkes National Primate Research Center, Atlanta, GA Robert F. Hoyt National Institutes of Health, National Heart, Lung and Blood Institute, Bethesda, MD Rudolf P. Bohm, Jr. Tulane University, Tulane National Primate Research Center, Covington, LA Denis Lambrights GlaxoSmithKline (GSK) Biologicals, Rixensart, Belgium Kathleen M. Brasky Southwest National Primate Research Center, Texas Biomedical Research Judy MacArthur-Clark Animals in Science Regulation Institute, San Antonio, TX Unit, Home Office, London, UK William E. Britz, Jr. Britz & Company, Wheatland, WY Christopher L. Medina Abbott Laboratories, Comparative Medicine, Abbott Park, IL Hannah Buchannan-Smith University of Stirling, Psychology, School of Natural Sciences, Scotland, UK Yasmina A. Paramastri Vanderbilt University Medical Center, Department of Pathology, Microbiology and Thomas M. Butler Retired, Fair Oaks Ranch, TX Immunology, Nashville, TN John Capitanio University of California, Davis, SulliJ.PopilskisNewYorkMedicalCollege,Department Department of Psychology, Davis CA of Comparative Medicine, Valhalla, NY William Cole Retired, Lansdale, PA Wendy Saltzman University of California at Riverside, Lita Drobatz GlaxoSmithKline (GSK) Pharmaceuticals, Department of Biology, Riverside, CA King of Prussia, PA Michael Schillaci University of Toronto, Department of Bennett Dyke Retired, San Antonio, TX Anthropology, Toronto, Ontario, Canada Marisa Elkins St. Claire National Institutes of Health, Ma˚rten K.J. Schneider University Hospital of Zurich, National Institute of Allergy and Infectious Diseases, Laboratory of Vascular Immunology, Division of Rockville, MD Internal Medicine, Zurich, Switzerland James J. Elliott Texas A&M University, Comparative Mary Schneider University of Wisconsin-Madison, Medicine Program, College Station, TX Departments of Kinesiology (Occupational Therapy Lynn Fairbanks University of California at Los Angeles, Program) and Psychology, Madison, WI Semel Institute, Los Angeles, CA M. Michael Swindle Medical University of South John Finch Charles River Laboratories, Edinburgh, Carolina, Department of Comparative Medicine, UK Charleston, SC John Fleagle Stony Brook University, Department of Maureen Thompson Emory University, Yerkes National Anatomical Sciences, Stony Brook, NY Primate Research Center, Atlanta, GA xi xii Reviewers Duane Ullrey Michigan State University, Departments of Lawrence E. Williams The University of Texas MD Animal Science and Fisheries & Wildlife, East Anderson Cancer Center, Michale E. Keeling Center Lansing, MI for Comparative Medicine and Research, Bastrop, TX Gary L. White The University of Oklahoma Health Roman F. Wolf The University of Oklahoma Health Sciences Center, Comparative Medicine, Oklahoma Sciences Center, Comparative Medicine, Oklahoma City, OK City, OK Gregory K. Wilkerson The University of Texas MD Simon Young AstraZeneca, Alderley Park, Cheshire, UK Anderson Cancer Center, Michale E. Keeling Marcus Young Owl California State University, Long Center for Comparative Medicine and Research, Beach, Department of Anthropology and Biological Bastrop, TX Sciences, Long Beach, CA Contributors Mark G. Baxter Friedman Brain Institute, Mount Sinai DavidK.JohnsonCascadeBiosciencesConsultants,Inc., School of Medicine, New York, USA Sisters, OR Kathryn Bayne AAALAC International, Frederick, MD Stephen T. Kelley Department of Comparative Medicine, University of Washington, Seattle, WA IrwinS.BernsteinDepartmentofPsychology,University of Georgia, Athens, GA BrianJ.KellyBehavioralSciencesDepartment,Fitchburg State University, Fitchburg, MA James L. Blanchard Comparative Medicine Program, Tulane University, Covington, LA Liz Koutsos Mazuri Exotic Animal Nutrition, PMI Nutrition International LLC, St Louis, MO Mollie A.Bloomsmith YerkesNationalPrimateResearch Center, Atlanta, GA Joshua A. Kramer New England Primate Research Center, Harvard Medical School, Southborough, MA Rudolf P. Bohm, Jr Division of Veterinary Medicine, Tulane National Primate Research Center, Covington, Vince Meador Anatomic and Clinical Pathology, LA Integrated Science and Innovation, Covance Laboratories Inc., WI Saverio Capuano Wisconsin National Primate Research Center, Madison, WI Jerrold S. Meyer Department of Psychology, University of Massachusetts, Amherst, MA Angela Carville New England Primate Research Center, Southborough, MA Nancy Minugh-Purvis Department of Pathology and Laboratory Medicine and Office of Professional Donna J. Clemons Abbott Laboratories, Comparative Studies in the Health Sciences, Drexel University Medicine, Abbott Park, IL College of Medicine, Philadelphia, PA Kristine Coleman Oregon National Primate Research Kathy L. Murphy Friedman Brain Institute, Mount Sinai Center, Beaverton, OR School of Medicine, New York, USA David K.C. Cooper Thomas E. Starzl Transplantation Timothy H. Morris The School of Veterinary Medicine Institute, Department of Surgery, University of and Science, The University of Nottingham, Pittsburgh, Pittsburgh, PA Leicestershire, UK Carolyn M. Crockett National Primate Research Center, MarekA. NiekraszAnimal Resources Center, University University of Washington, Seattle, WA of Chicago, Chicago, IL DavidElmoreCharlesRiversLaboratories,SanDiego,CA MelindaA.NovakDepartmentofPsychology,University Paul A. Flecknell Comparative Biology Centre, The of Massachusetts, Amherst, MA Medical School, The University of Newcastle, Michael L. Power Nutrition Laboratory, Smithsonian Newcastle-upon-Tyne, UK Conservation Biology Institute, National Zoological Elizabeth W. Ford The Scripps Research Institute, Park, Washington, DC LaJolla, CA KarenRiceSouthwestNationalPrimateResearchCenter, Margaret H. Gilbert Division of Veterinary Medicine, Texas Biomedical Research Institute, San Antonio, Tulane National Primate Research Center, TX Covington, LA Kasi E. Russell-Lodrigue Division of Veterinary James C. Ha National Primate Research Center, Medicine, Tulane National Primate Research Center, Department of Psychology, University of Washington, Covington, LA Seattle, WA StevenJ.SchapiroTheUniversityofTexasMDAnderson Dennis O. Johnsen Port Townsend, WA Cancer Center, Bastrop, TX xiii xiv Contributors David Glenn Smith Department of Anthropology and Gerhard F. Weinbauer Developmental and Reproductive California National Primate Research Center, Toxicology, Covance Laboratories, Kesselfeld, University of California, Davis, CA Muenster, Germany Suzette Tardif Barshop Institute of Longevity & Aging Gary L. White The University of Oklahoma Health Studies, University of Texas Health Science Center, Sciences Center, Comparative Medicine, Oklahoma San Antonio, TX City, OK Barbara Toddes Philadelphia Zoo, Philadelphia, PA RobertA.Whitney,Jr.RADM(0e8Retired),USPublic Health Service, Steilacoom, WA Jean E. Turnquist Department of Anatomy and Neurobiology, University of Puerto Rico Medical Lawrence E. Williams Michale E. Keeling Center School, San Juan, Puerto Rico for Comparative Medicine and Research, Department of Veterinary Sciences, The University of Texas MD RobertWagnerDivisionofLaboratoryAnimalResources, Anderson Cancer Center, Bastrop, TX University of Pittsburgh, Pittsburgh, PA, USA Roman F. Wolf The University of Oklahoma Health AlexWakefieldCovanceLaboratoriesInc.,Greenfield,IN Sciences Center, Comparative Medicine, Oklahoma Craig L. Wardrip Animal Resources Center, University City, OK of Chicago, Chicago, IL James L. Weed Division of Veterinary Resources, National Institutes of Health, Bethesda, MD Chapter 1 History of the Use of Nonhuman Primates in Biomedical Research Dennis O. Johnsen*, David K. Johnsony and Robert A. Whitney, Jrz *PortTownsend,WA,yCascadeBiosciencesConsultants,Inc.,Sisters,OR,zRADM(0e8Retired),USPublicHealthService,Steilacoom,WA Chapter Outline HumanandNonhumanPrimatesto1960 2 Constraints 13 RootsofModernPrimatology 2 Regulation 13 FirstPrimateCenters 2 1978IndianBanonMonkeyExports 13 SovietInstituteofExperimentalPathologyandTherapy 2 SimilarActionsinOtherCountries 14 RobertYerkesandthePrimateLaboratoryoftheYale RespondingtotheConstraints 14 InstituteofPsychobiology 3 RiseofDomesticBreeding 14 CayoSantiagoandtheCaribbeanPrimateResearch InteragencyPrimateSteeringCommittee 15 Center 3 OtherConservationActivities 15 VirologicalResearchinNonhumanPrimates 4 Non-GovernmentalOrganizations 15 General 4 Transitiontothe1980s 16 Polio 4 PatternsofUsage 16 Kuru 5 RetroviralDisease 17 Virus(HerpesBVirusorMacacineHerpesvirus1) 5 1980Sand1990S:ProgressPayingoffintheFaceofSerious OtherContributions 6 Challenges 17 TheWorkofHarryHarlow 6 ANobelPrize 17 BreedingandReproductivePhysiology 6 RetroviralDiseaseandSimianImmunodeficiencyVirus EstablishmentoftheNationalInstitutesofHealth’sNational (SIV) 17 PrimateResearchCentersProgramintheUSA:Crossingthe EmergenceandImpactoftheAnimalRightsMovement 18 Threshold 6 PeoplefortheEthicalTreatmentofAnimals 18 InitialActivity 6 1985AmendmentoftheAnimalWelfareAct 19 DevelopingtheConcept 6 OtherEffectsofAIDSResearch 19 LaunchingtheNewProgram 7 ChimpanzeeBreedingandResearchProgram 19 NationalPrimateResearchCentersProgramToday 8 Virus,ZoonoticDiseases,andAIDSProvidethe 1960e1980:PeriodofGrowthinaWorldofIncreasing StimulusforSpecificPathogenFreeBreeding 20 Constraints 8 EbolaVirusandInterruptionofImports 21 EmulationoftheCenterConcept 8 CaptiveBreedingGoesGlobal 22 General 8 PrimateResearchBeyondtheYear2000 22 SouthwestFoundationforResearchandEducation 8 SignificantScientificAdvances 22 WakeForestUniversityPrimateCenter 9 MappingtheChimpanzeeandRhesusMonkey DukePrimateCenter 9 Genome 22 LaboratoryforExperimentalMedicineandSurgeryin GenomicResearch 22 Primates 9 InfectiousDisease 23 MichaleE.KeelingCenterforComparativeMedicine GrowthintheUseofNonhumanPrimates 23 andResearch 10 General 23 CaribbeanPrimateResearchCenter 10 TheNPRCProgram 24 DepartmentofDefense,DepartmentofHealthand CDCImportData,CRO,andPharmaceutical HumanServices’PublicHealthService,andotherUS Activity 24 GovernmentLaboratories 11 International 24 ActivitiesAbroad 11 RegulationandReview 25 1 NonhumanPrimatesinBiomedicalResearch.DOI:10.1016/B978-0-12-381365-7.00001-7 Copyright(cid:1)2012ElsevierInc.Allrightsreserved.