BRUCELLOSIS IN THE GREATER YELLOWSTONE AREA

Norman F. Cheville, Principal Investigator

Dale R. McCullough, Principal Investigator

Lee R. Paulson, Project Director

Board on Agriculture

Board on Environmental Studies and Toxicology

Board on Agriculture

Commission on Life Sciences

Washington, D.C. 1998



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BRUCELLOSIS IN THE GREATER YELLOWSTONE AREA Norman F. Cheville, Principal Investigator Dale R. McCullough, Principal Investigator Lee R. Paulson, Project Director Board on Agriculture Board on Environmental Studies and Toxicology Board on Agriculture Commission on Life Sciences Washington, D.C. 1998

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NATIONAL ACADEMY PRESS 2101 Constitution Ave., N.W. Washington, D.C. 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 authors responsible for the report were chosen for their special competence 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 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. Bruce Alberts 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 achievements of engineers. Dr. William 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 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. Kenneth I. Shine 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. Bruce M. Alberts and Dr. William A. Wulf are chairman and vice chairman, respectively, of the National Research Council. The project was supported by the Department of the Interior Cooperative Agreement No. 1443CA000197005. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the organizations or agencies that provided support for this project. Library of Congress Catalog Card Number 97-80670 International Standard Book Number 0-309-05989-5 Cover photographs: Dale R. McCullough, Berkeley, California Copyright 1998 by the National Academy of Sciences. All rights reserved. National Academy Press (http:/www.nap.edu) 800-624-6242 202-334-3313 (in the Washington, D.C. metropolitan area) Printed in the United States of America

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BRUCELLOSIS IN THE GREATER YELLOWSTONE AREA NORMAN F. CHEVILLE, Principal Investigator, Iowa State University, Ames, Iowa DALE R. MCCULLOUGH, Principal Investigator, University of California, Berkeley, California LEE R. PAULSON, Project Director NORMAN GROSSBLATT, Editor KATHRINE IVERSON, Project Assistant/Information Specialist STEPHANIE PARKER, Project Assistant NORMAN F. CHEVILLE is Chair of the Department of Veterinary Pathology at Iowa State University. He received the DVM degree from Iowa State University (1959) and MS (1963) and Ph.D. (1964) from the University of Wisconsin. In 1968, he served a sabbatical year at the National Institute for Medical Research, London, studying under Anthony Allison. The honorary degree Doctor Honoris Causa was conferred by the University of Liège in 1986 for outstanding work in veterinary pathology. Dr. Cheville began his career at Army Biological Laboratory, Fort Detrick, Md., in the Veterinary Corps of the U.S. Army, 1959-61. After 3 years as research associate at the University of Wisconsin under Dr. Carl Olsen, he moved to the National Animal Disease Center as Chief of Pathology Research, 1964-89, and later as chief of the Brucellosis Research Unit, 1989-1995, during which he led the team that developed a new vaccine for bovine brucellosis. In 1995, he was appointed chair of the Department of Veterinary Pathology at Iowa State. Dr. Cheville has been Secretary-Treasurer and President of the American College of Veterinary Pathologists, President of the Conference of Research Workers in Animal Disease, and Editor of Veterinary Pathology. His honors include Outstanding Achievement Award, USDA, 1991; Distinguished Scientist Award, ARS, USDA, 1990; Alumni Merit Award, Iowa State University for "outstanding contributions to human welfare and professional accomplishment" in 1978. He has published more than 200 papers and 7 books. DALE R. MCCULLOUGH is Professor of Wildlife Biology in the Ecosystem Sciences Division of the Department of Environmental Science, Policy, and Management and Resource Conservation in the Museum of Vertebrate Zoology at the University of California, Berkeley, where he holds the A. Starker Leopold endowed chair. He received his BS in wildlife management from South Dakota State University (1957), MS in wildlife management from Oregon State University (1960), and Ph.D. in Zoology from University of California, Berkeley

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(1966). He was a Professor of Resource Ecology in the School of Natural Resources at the University of Michigan, Ann Arbor from 1966 to 1979, and in 1980 he moved to his present position at the University of California. His research interests concern the behavior, ecology, conservation, and management of large mammals, in which he has endeavored to integrate new areas of conservation biology into traditional wildlife management approaches. He has spent sabbatical leaves in the outback of Australia studying three co-occurring species of kangaroos, and in Taiwan studying the elusive Reeves' muntjac, a small forest deer. He has served previously on three NAS/NRC committees reviewing wildlife management issues. He has published more than 100 papers and five books. Among his honors are three outstanding book of the year awards from the Wildlife Society and being named a distinguished alumnus by South Dakota State University and Oregon State University. LEE R. PAULSON is Program Director for Resource Management in the Board on Environmental Sciences and Toxicology. She has served as project director or senior staff officer for numerous National Research Council studies, including Setting Priorities for Land Conservation, Hazardous Materials on the Public Lands, Animals as Sentinels of Environmental Health Hazards, The Evaluation of Forensic DNA Evidence, and Monitoring Human Tissues for Toxic Substances.

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BOARD ON AGRICULTURE DALE E. BAUMAN, Chair, Cornell University, Ithaca, New York JOHN M. ANTLE, Montana State University, Bozeman, Montana SANDRA S. BATIE, Michigan State University, East Lansing, Michigan MAY R. BERENBAUM, University of Illinois, Urbana, Illinois LEONARD S. BULL, North Carolina State University, Raleigh, North Carolina WILLIAM B. DELAUDER, Delaware State University, Dover, Delaware ANTHONY S. EARL, Quarles & Brady, Madison, Wisconsin ESSEX E. FINNEY JR., U.S. Department of Agriculture, Mitchellville, Maryland CORNELIA FLORA, Iowa State University, Ames, Iowa GEORGE R. HALLBERG, The Cadmus Group, Boston, Massachusetts RICHARD R. HARWOOD, Michigan State University, East Lansing, Michigan T. KENT KIRK, University of Wisconsin, Madison, Wisconsin HARLEY W. MOON, Iowa State University, Ames, Iowa WILLIAM L. OGREN, Hilton Head, South Carolina GEORGE E. SEIDEL JR., Colorado State University, Fort Collins, Colorado JOHN W. SUTTIE, University of Wisconsin, Madison, Wisconsin JAMES J. ZUICHES, Washington State University, Pullman, Washington PAUL GILMAN, Executive Director MICHAEL J. PHILLIPS, Director SHIRLEY B. THATCHER, Administrative Assistant

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BOARD ON ENVIRONMENTAL STUDIES AND TOXICOLOGY GORDON ORIANS, (Chair), University of Washington, Seattle, Washington DONALD MATTISON, (Vice Chair), University of Pittsburgh, Pittsburgh, Pennsylvania MAY R. BERENBAUM, University of Illinois, Urbana, Illinois EULA BINGHAM, University of Cincinnati, Cincinnati, Ohio PAUL BUSCH, Malcolm Pirnie, Inc., White Plains, New York GEORGE P. DASTON, The Procter & Gamble Co., Cincinnati, Ohio PETER L. DEFUR, Virginia Commonwealth University, Richmond, Virginia DAVID L. EATON, University of Washington, Seattle, Washington DIANA FRECKMAN, Colorado State University, Ft. Collins, Colorado ROBERT A. FROSCH, Harvard University, Cambridge, Massachusetts MARK HARWELL, University of Miami, Miami, Florida BARBARA HULKA, University of North Carolina, Chapel Hill, North Carolina DANIEL KREWSKI, Health & Welfare Canada, Ottawa, Ontario RAYMOND C. LOEHR, The University of Texas, Austin, Texas JAMES A. MACMAHON, Utah State University, Logan, Utah MARIO J. MOLINA, Massachusetts Institute of Technology, Cambridge, Massachusetts WARREN MUIR, Hampshire Research Institute, Alexandria, Virginia GEOFFREY PLACE, Hilton Head, South Carolina MARGARET STRAND, Bayh, Connaughton and Malone, Washington, D.C. BAILUS WALKER, JR., Howard University, Washington, D.C. GERALD N. WOGAN, Massachusetts Institute of Technology, Cambridge, Massachusetts TERRY F. YOSIE, Ruder Finn Inc., Washington, D.C. Senior Staff JAMES J. REISA, Director DAVID J. POLICANSKY, Associate Director and Program Director for Applied Ecology CAROL A. MACZKA, Program Director for Toxicology and Risk Assessment LEE R. PAULSON, Program Director for Resource Management RAYMOND A. WASSEL, Program Director for Environmental Sciences and Engineering KULBIR BAKSHI, Program Director for the Committee on Toxicology

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COMMISSION ON LIFE SCIENCES THOMAS D. POLLARD, (Chair), The Salk Institute, La Jolla, California FREDERICK R. ANDERSON, Cadwalader, Wickersham & Taft, Washington, D.C. JOHN C. BAILAR III, University of Chicago, Chicago, Illinois PAUL BERG, Stanford University School of Medicine, Stanford, California JOANNA BURGER, Rutgers University, Piscataway, New Jersey SHARON L. DUNWOODY, University of Wisconsin, Madison, Wisconsin JOHN EMMERSON, Portland, Oregon NEAL FIRST, University of Wisconsin, Madison, Wisconsin URSULA GOODENOUGH, Washington University, St. Louis, Missouri HENRY HEIKKINEN, University of Northern Colorado, Greeley, Colorado HANS J. KENDE, Michigan State University, East Lansing, Michigan CYNTHIA KENYON, University of California, San Francisco, California DAVID LIVINGSTON, Dana-Farber Cancer Institute, Boston, Massachusetts THOMAS E. LOVEJOY, Smithsonian Institution, Washington, D.C. DONALD R. MATTISON, University of Pittsburgh, Pittsburgh, Pennsylvania JOSEPH E. MURRAY, Wellesley Hills, Massachusetts EDWARD E. PENHOET, Chiron Corporation, Emeryville, California MALCOLM C. PIKE, University of Southern California, Los Angeles, California JONATHAN M. SAMET, The Johns Hopkins University, Baltimore, Maryland CHARLES F. STEVENS, The Salk Institute, La Jolla, California JOHN L. VANDEBERG, Southwest Foundation for Biomedical Research, San Antonio, Texas PAUL GLIMAN, Executive Director

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PREFACE AND ACKNOWLEDGMENTS Brucellosis in the Greater Yellowstone Area (GYA) has been the subject of much debate and national attention. In the conduct of this study, we had the opportunity to hear many views and deeply held convictions. But at the heart of the controversy over bison management is the need for a solid scientific underpinning. To that end, we directed our efforts to identifying current research and reviewing previous research. We made every effort to represent accurately consensus views of researchers and other experts. It is our hope that this report will provide a basis for future endeavors related to managing brucellosis in the GYA and that science can be melded with policy to resolve many of the difficult issues faced by the governmental parties involved in brucellosis management. Each entity has been faced with pressures to act in the best interests of their commercial or recreational users. We further hope that this report will provide a beginning for use of emerging technology to develop a plan appropriate to the task, and one that is in best interests of the nation. We are deeply grateful to the many colleagues who have contributed data for the manuscript during its development. A great many people have been most generous in providing us with much data, information, and observations on brucellosis, on the Greater Yellowstone Area, and on a wide variety of animals and their behavior. We wish to acknowledge in particular Drs. Steven Olsen (USDA), Mitchell Palmer, Jack Rhyan (USDA), and Beth Williams (University of Wyoming) for contributing data, graphs, and photographs of brucellosis in bison. The perspective of Mary Meagher, who has spent a lifetime with bison, was invaluable. Tom Thorne and Terry Kreeger, of the Wyoming Game and Fish Department, whose studies of diseases of wildlife and initiative in organizing the Greater Yellowstone Interagency Brucellosis Commission, were responsible for much of our practical understanding of brucellosis in elk of the Greater Yellowstone Ecosystem. The work of the Greater Yellowstone Interagency Brucellosis Committee, particularly under the influence of Drs. Dan Huff and Bob Hillman, was crucial to our understanding of the cooperation and compromise that will be required to solve this brucellosis dilemma. Data obtained from the current bison study in the YNP by Keith Aune (Montana Department of Fish, Wildlife and

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Parks), Peter Gogan (U.S. Geological Survey Biological Resources Division), Jack Rhyan, Tom Roffe (USGS, BRD), and Mark Taper (Montana State University, Bozeman) gave great insight into where we are going with brucellosis in Bison bison. Additional thanks and appreciation are due to Joel Berger, University of Nevada, Reno; Mark Boyce, University of Wisconsin, Stevens Point; Wayne Brewster, Yellowstone National Park; Steve Cain, Grand Teton National Park; Franz Camenzind, Jackson Hole Conservation Alliance, Wyoming; Andrew Clark, State Veterinarian, Oregon; Ron Cole, Hart Mountain National Antelope Refuge, Oregon; Walt Cook, University of Wyoming; Lynette Corbeil, University of California San Diego; Don Davis and James Derr, Texas A & M University; Phil Elzer and Fred Enright, Louisiana State University; Darla Ewalt, USDA, APHIS; Phillip Farnes, Snowcap Hydrology, Bozeman, Montana; Elmer Finck, Emporia State University, Kansas; Robert Garrott, Montana State University, Bozeman; Eric Gese, National Wildlife Research Center, Fort Collins, Colorado; Mike Gilsdorf, USDA, APHIS; Scott Grothe, Montana State University, Bozeman; Sam Holland, State Veterinarian, South Dakota; Tom Lemke, Montana Department of Fish, Wildlife and Parks; John Linnell, Norwegian Institute for Nature Research; Paul Nicoletti, Florida State University; Richard Ockenfels, Arizona Game and Fish Department; Rolf Peterson, Michigan Technological University, Houghton; Paul Rebich, Bigsky Beefalo, Montana; David Sands, Montana State University; D. J. Schubert, The Fund for Animals, Meyer & Glitzenstein, Washington, D. C.; Steve Sheffield, Clemson University; Bruce Smith, National Elk Refuge, Wyoming; Scott Smith, Wyoming Game and Fish Department; M. Stewart, USDA, APHIS; Ken Taylor, Alaska Department of Fish and Game; John Weaver, Wildlife Conservation Society; and Randall Zarnke, Alaska Department of Game and Fish, Fairbanks. Several persons gave their of their time and expertise to review this document, and we thank them for their critical input: Beverly Byrum, Ohio Department of Agriculture, Reynoldsburg; Franz Camenzind, Jackson Hole Conservation Alliance, Wyoming; Robert Ehlenfeldt, Wisconsin Department of Agriculture, Madison; Will Garner, Logan, Utah; Burke Healey, State of Oklahoma, Oklahoma City; Daniel Jarboe, Ft. Detrick, Maryland; R. Langford, Walter Reed Army Medical Center, Washington, D.C.; Robert Mead, Washington Department of Agriculture, Olympia; Gordon Orians, Seattle, Washington; David Pascual, Montana State University, Bozeman; Duncan Patten, Bozeman, Montana; George Seidel, Colorado State, Ft. Collins; Morton Swartz, Massachusetts General Hospital, Boston; Steve Torbit, National Wildlife Federation Rocky Mountain Natural Resources Center, Boulder; Fred Wagner, Utah State. We are also grateful to Secretary of the Interior Bruce Babbitt for making this work possible, as well as administrators and scientists within the National Park System of the U. S. Department of Interior, and in the Animal and Plant Health Inspection Service of the U. S. Department of Agriculture. Special thanks are owed to Margaret Jaeger and Thomas Kucera for their dedicated work in gathering information from scattered sources and preparation of the manuscript. Special thanks also are due to Kathy lverson for arranging meetings,

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logistics, and travel and to Stephanie Parker, who designed and crafted the web page to keep the public informed of project progress. And finally, it has been our good fortune to work with Lee Paulson as project director—incisive, enthusiastic, highly literate, and up-front, she brought to the project the capacity to shift rapidly through conflicting opinions to identify and focus on essential items. Norman F. Cheville Dale R. McCullough

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CONTENTS Executive Summary   1 Introduction   10     Background   13     Structure of This Study   14 Part I: The Disease and Transmission   16     Bison and Cattle   16     B. Abortus Infection and Transmission   17     Persistence in Pregnancy   20     Periodic Bacteremia in Chronic Infection   21     Transmission to Scavengers and Predators   21     Shedding in Mammary Glands and Milk   23     Shedding in Feces   24     Infection in Males   25     Detecting Infected Animals   27     Serology   27     The False-Negative Serologic Test   29     The False-Positive Serologic Test   29     Bacterial Culture   29     Correlation of Serology with Bacterial Culture   31     Immunity   33     Likelihood of Infectiousness   33     Minimum Infectious Dose   34     True Prevalence of B. Abortus in GYA Bison and Elk   35     Bison   36     Elk   37     Infection in Other Mammals in the GYA   38     Canids   38     Moose   39     Horse   40     Bear, Deer, and Other Big Game   40 Part II: Transmission Among and Between Species   42

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    Bison, Elk, and Cattle   42     Epidemiologic Evidence of Transmission from Wildlife to Cattle   44     Bison and Elk Behavior and Transmission   45     Transmission by Other Species of Ungulates   49     Potential Role of Carnivores in Transmission   50     Role of Other Wildlife Species   56     Bison Movement Out of Yellowstone National Park   56     Weather and Bison   56     Natural Regulation in YNP Bison   63     Influences of Plowing and Grooming Snow   68     Bison in Grand Teton National Park and the National Elk Refuge   70     Elk in the Greater Yellowstone Area   71     Northern Elk Herd Movements Out of Yellowstone National Park   72     Other Elk Herds in the GYA   76     Effects on Reproductive Potential   78     Risk of Transmission   79     Bison to Cattle   80     Elk to Cattle   81     Elk to Bison   81     Bison to Elk   82     Elk as a Reinfection Pathway for Bison   82     Other GYA Wildlife to Cattle   86     Transmission to Humans in the GYA   86     Other Species of Brucella and Brucellosis in Wildlife   87 Part III: Vaccines   89     Existing Vaccines   89     Strain 19   90     S19 in Bison   90     S19 in Elk   92     Strain RB51   92     Other Vaccines   96     Efficacy   96     Strain Survival   96     Route   97     Parenteral Injection   97     Biobullet   97     Oral   97     Dose   98     Age   98

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    Other Factors to Consider   98     Duration of Immunity   99     Serologic Responses   99     Biosafety of Vaccines   101     Clinical Signs of Disease   101     Bacteria in Body Secretions   101     Bacteria in the Bloodstream   102     Persistence in Regional Lymph Nodes   102     Immune Response   102     Absence of Inflammation or Chronic Tissue Injury   103     Capacity to Induce Abortion   103     Experimental Recrudescence   104     Genetic Stability   105     Vaccination Program Success   105 Part IV: Reducing the Risk of Transmission from Wildlife to Cattle   107     Previous Bison-Vaccination Programs in National and State Parks   107     Approaches to Controlling or Eliminating Brucellosis in YNP   109     Field Delivery of a Vaccination Program for YNP Bison   112     Vaccine Delivery in Food or via Injection   113     Venereal Immunization   114     Vaccination of Cattle   115     Limiting Cattle Near Park Borders to Steers   115     Effects of Test-and-Slaughter Programs on Genetic Diversity   116     Natural Regulation and Brucellosis Control   117     Adaptive Management   122 References   124 Appendix A: Questions Addressed by the NRC Study   144 Appendix B: Meeting Agendas and Presentations   146     Agenda, 24-26 July 1997, Bozeman, MT   146     Agenda, 4 August 1997, Jackson, WY   149     Evaluation of Brucella abortus Vaccine Strain RB51 in Bison, Philip H. Elzer and Donald S. Davis   151     Evaluation of the Vaccine Efficacy of RB51 Administered Orally in Elk, Philip H. Elzer, Gerhardt G. Schurig, Fred M. Enright, and Donald S. Davis   157     Issues in Vaccination for Brucellosis, Fred M. Enright   161

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    Oral RB51 Vaccination of Elk: Tissue Colonization and Immune Response, Wyoming Game and Fish Department with Louisiana State University and Virginia Polytechnic Institute   168     RB51 Vaccination of Elk: Safety and Efficacy, Wyoming Game and Fish Department with University of Wyoming, Louisiana State University and Virginia Polytechnic Institute   169     Brucellosis in the Greater Yellowstone Area: What is the Problem?, Paul Nicoletti   170     Safety and Efficacy of Existing Vaccines to Prevent Brucellosis in Bison, Steven Olsen   173     Lesions and Sites of Tissue Localization of Brucella abortus in Female Bison from Yellowstone National Park: Preliminary Results, Jack C. Rhyan, Keith Aune, Thomas J. Roffe, Thomas Gidlewski, Darla R. Ewalt, and Michael Philo   177 Appendix C: Other Diseases in GYA Wildlife   181

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BRUCELLOSIS IN THE GREATER YELLOWSTONE AREA

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