DIAGNOSIS AND CONTROL OF JOHNE’S DISEASE

Committee on Diagnosis and Control of Johne’s Disease

Board on Agriculture and Natural Resources

Division on Earth and Life Studies

NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS
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DIAGNOSIS AND CONTROL OF JOHNE’S DISEASE Committee on Diagnosis and Control of Johne’s Disease Board on Agriculture and Natural Resources Division on Earth and Life Studies NATIONAL RESEARCH COUNCIL OF THE NATIONAL ACADEMIES THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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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 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. This study was supported by Agreement No. 02–9114–0523 and 00–9114–0523 between the National Academy of Sciences and the U.S. Department of Agriculture. Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. International Standard Book Number 0-309-08611-6 (Book) International Standard Book Number 0-309-50628-X (PDF) Library of Congress Control Number 2003109098 Additional copies of this report are available from the National Academies Press, 500 Fifth Street, N.W., Lockbox 285, Washington, D.C.20055; (800) 624–6242 or (202) 334–3313 (in the Washington metropolitan area); Internet, http://www.nap.edu Copyright 2003 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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THE NATIONAL ACADEMIES Advisers to the Nation on Science, Engineering, and 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 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 M.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. 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 responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V.Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of 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. Wm.A. Wulf are chairman and vice chairman, respectively, of the National Research Council.

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Committee on Diagnosis and Control of Johne’s Disease BRUCE A.RIDEOUT, Chair, Zoological Society of San Diego, San Diego, California SHELDON T.BROWN, Bronx Veterans Administration Medical Center, Bronx, New York WILLIAM C.DAVIS, Washington State University, Pullman JOHN M.GAY, Washington State University, Pullman RALPH A.GIANNELLA, University of Cincinnati College of Medicine, Cincinnati, Ohio MURRAY E.HINES II, University of Georgia, Tifton WILLIAM D.HUESTON, University of Minnesota, St. Paul LAWRENCE J.HUTCHINSON, Pennsylvania State University, University Park STAFF Tina I. Rouse, Study Director Tanja Pilzak, Research Assistant Kate Kelly, Editor Cindy Lochhead, Project Assistant

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Board on Agriculture and Natural Resources HARLEY W.MOON, Chair, Iowa State University, Ames SANDRA BARTHOLMEY, Crystal Lake, Illinois DEBORAH BLUM, University of Wisconsin, Madison ROBERT B.FRIDLEY, University of California, Davis BARBARA P.GLENN, Federation of Animal Science Societies, Bethesda, Maryland LINDA F.GOLODNER, National Consumers League, Washington, D.C. W.R. (REG) GOMES, University of California, Oakland PERRY R.HAGENSTEIN, Institute for Forest Analysis, Planning, and Policy, Wayland, Massachusetts CALESTOUS JUMA, Harvard University, Cambridge, Massachusetts JANET C.KING, University of California, Davis WHITNEY MACMILLAN, Cargill, Inc., Minneapolis, Minnesota TERRY L.MEDLEY, DuPont Biosolutions Enterprise, Wilmington, Delaware ALICE N.PELL, Cornell University, Ithaca, New York SHARRON S.QUISENBERRY, Montana State University, Bozeman NANCY J.RACHMAN, Exponent, Inc., Washington, D.C. SONYA B.SALAMON, University of Illinois at Urbana-Champaign, Urbana G.EDWARD SCHUH, University of Minnesota, Minneapolis BRIAN J.STASKAWICZ, University of California, Berkeley JACK WARD THOMAS, University of Montana, Missoula JAMES H.TUMLINSON, United States Department of Agriculture, Agricultural Research Service, Gainesville, Florida B.L.TURNER, Clarke University, Worcester, Massachusetts STAFF Charlotte Kirk Baer, Director Donna Lee Jameison, Administrative Assistant

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Acknowledgments This report represents the integrated efforts of many individuals. The committee thanks all those who shared their insight and knowledge to bring the document to fruition. We also thank all those who provided information at our public meetings and who participated in our public sessions. During the course of its deliberations, the committee sought assistance from several people who gave generously of their time to provide advice and information that were considered in its deliberations. Special thanks are due the following: John B.Adams, National Milk Producers Federation, Arlington, Virginia John P.Bannantine, United States Department of Agriculture, Ames, Iowa Michael Carter, United States Department of Agriculture, Beltsville, Maryland Michael T.Collins, University of Wisconsin, Madison William Hartmann, Minnesota Board of Animal Health, St. Paul Jeffrey Huse, New York State Department of Agriculture and Markets, Albany Dennis Lang, National Institutes of Health, Bethesda, Maryland Bill Layton, Marsh Veterinary Diagnostic Laboratory, Bozeman, Montana Brian J.McCluskey, United States Department of Agriculture, Fort Collins, Colorado

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Cheryl Miller, Paratuberculosis Awareness and Research Association, Temple Terrace, Florida Charlotte F.Quist, Wildlife Health Associates, Inc., Dillon, Montana Ralph Slaughter, Biocor Animal Health, Omaha, Nebraska Judith R.Stabel, United States Department of Agriculture, Ames, Iowa Susan M.Stehmen, Cornell University, Ithaca, New York Gary M.Weber, National Cattlemen’s Beef Association, Washington, D.C. Scott J.Wells, University of Minnesota, St. Paul Robert H.Whitlock, University of Pennsylvania, Kennett Square The committee is grateful to members of the National Research Council (NRC) staff who worked diligently to maintain progress and quality in its work. This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’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 integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Raúl G.Barletta, University of Nebraska, Lincoln Michael T.Collins, University of Wisconsin, Madison Charles J.Czuprynski, University of Wisconsin, Madison Donald E.Hansen, Oregon State University, Corvallis Norman Pace, University of Colorado, Boulder J.Marc Rhoads, University of North Carolina, Chapel Hill Christine Rossiter, Poulin Grain, Inc., Newport, Vermont Elizabeth S.Williams, University of Wyoming, Laramie Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by Dr. Norman Cheville. Appointed by the National Research Council, he was responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution.

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Preface Control or eradication of important livestock diseases has been a top priority for the United States Department of Agriculture (USDA) throughout much of the previous century. Most efforts have involved mandatory national eradication programs. But mandatory programs bring a host of difficulties: they require a large program infrastructure, administration of indemnity programs, and constant scrutiny to uncover and eliminate loopholes. As most eradication programs near completion, attention is turning to other diseases that previously were not of sufficiently high priority to warrant mandatory control. These other diseases pose new challenges and may require novel approaches for control. Johne’s disease (JD) is one such disease. Although its significance as an animal health and economic problem has been recognized for years, it is only now beginning to receive attention and prioritization for control. The United States Animal Health Association’s National Johne’s Disease Working Group has been leading the effort to provide national coordination and minimum standards for voluntary control, and USDA recently stepped in with the appointment of a national JD coordinator. Some of this recent attention is being driven by concern over the potential role of Mycobacterium avium subsp. paratuberculosis (Map), the causative agent of JD, in Crohn’s disease in humans. This issue warrants concern because it could affect the diagnosis and

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treatment of Crohn’s disease and because it could change strategies for control of JD in livestock. The USDA saw an opportunity to address this important issue and to facilitate progress in the control of JD in livestock. In August 2001, the Board on Agriculture and Natural Resources was asked to convene the Committee on the Diagnosis and Control of Johne’s Disease. The committee’s task was to review and synthesize the state of knowledge of JD in livestock, to evaluate current control plans, to critically assess the evidence for and against a causal relationship between Map and Crohn’s disease, and to provide recommendations for control and research. The committee had a relatively short period in which to accomplish these ambitious goals, but I am pleased that its members approached the task with great enthusiasm and determination. The committee met twice in Washington D.C., and once in Hershey, Pennsylvania in conjunction with the annual meeting of the United States Animal Health Association. The latter meeting included a public workshop, where committee members heard from experts on JD and from a leading Crohn’s disease patient advocacy group. At its final meeting, the committee received an update on research into the link between Map and Crohn’s disease and a progress report on the Map genome project at the National Animal Disease Laboratory. This report represents the outcome of many hours of hard work and spirited debate by committee members. I am grateful for their talent, dedication, intellectual integrity, and perseverance in the face of many challenges posed by our schedule and task. I am also very grateful to the Board on Agriculture and Natural Resources for the great care they took in assembling such a distinguished panel and for the opportunity to serve with them on this important committee. Finally, on behalf of the committee I would like to thank and acknowledge study director Tina Rouse and project assistant Cindy Lochhead for their outstanding dedication and persistence. Without their expertise, organizational skills, resilience, and resourcefulness, we could not have completed the task. BRUCE A.RIDEOUT, Chair Committee on Diagnosis and Control of Johne’s Disease

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Contents     EXECUTIVE SUMMARY   1     The Task   2     Conclusions   3     Disease Control   4     Education and Training   7     Research   7 1   INTRODUCTION   13     The Committee’s Task   15 2   JOHNE’S DISEASE IN DOMESTICATED AND WILD ANIMALS   16     Spectrum of Disease in Domesticated Animals   18     Spectrum of Disease in Other Animals   20     Pathology   21     Epidemiology   24     Modes of Transmission   27     Pathogenesis in Cattle   37 3   DIAGNOSTICS   45     Testing of Domesticated Animals   45

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    Molecular Methods   59     Epidemiologic Tools   62 4   CONTROL PRINCIPLES AND PROGRAMS   66     Control Principles   66     Current Control Programs   78     Principles of Control Implementation   97 5   ECONOMIC IMPLICATIONS OF JOHNE’S DISEASE   99     Trade   100 6   JOHNE’S DISEASE AND CROHN’S DISEASE   104     Crohn’s Disease   105     Implications of the Link   107     Conclusions   119 7   CONCLUSIONS AND RECOMMENDATIONS   121     Control Programs   122     Control Recommendations   124     Education and Training Recommendations   126     Research Recommendations   127     REFERENCES   133     APPENDIXES     A   Interpretation of Diagnostic Results   175 B   USAHA Voluntary Johne’s Disease Herd Status Program for Cattle   179 C   USDA/APHIS Draft Johne’s Disease Control Program   194     ABOUT THE AUTHORS   221     BOARD ON AGRICULTURE AND NATURAL RESOURCES PUBLICATIONS   226

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Tables, Boxes, and Figures TABLES 2–1   Species Infected with Mycobacterium avium subsp. paratuberculosis   16 2–2   Clinical Stages of Johne’s Disease in Cattle   20 2–3   Global Seroprevalence of Johne’s Disease in Dairy Cattle   25 2–4   Seroprevalence of Johne’s Disease in U.S. Dairy Cattle in 1996   26 2–5   Environmental Factors Associated with Mycobacterium avium subsp. paratuberculosis   32 2–6   Mycobacterium avium subsp. paratuberculosis Response to Heat Treatment, Pasteurization, and Other Processes   35 3–1   Detectability of Johne’s Disease at Varying Clinical Stages   46 3–2   Comparison of Diagnostic Tests for Johne’s Disease   47 3–3   Utility of Diagnostic Tests in Clinical Stages of Johne’s Disease   47 4–1   Standard-Track Certification from the U.S. Voluntary Johne’s Disease Herd Status Program for Cattle   81 4–2   Fast-Track Certification from the U.S. Voluntary Johne’s Disease Herd Status Program for Cattle   81 4–3   Test-Positive Requirements from the Uniform Program Standards   84

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    for the Voluntary Bovine Johne’s Disease Control Program   84 4–4   Standard-Track Test-Negative Components from the Uniform Program Standards for the Voluntary Bovine Johne’s Disease Control Program   84 4–5   Fast-Track Test-Negative Components from the Uniform Program Standards for the Voluntary Bovine Johne’s Disease Control Program   85 4–6   National Veterinary Services Laboratory Approved Johne’s Disease Tests   87 4–7   Canadian and U.S. National Veterinary Services Laboratory Approved Laboratories for Johne’s Disease   87 4–8   Components of State Johne’s Disease Herd Status/Control Programs   96 4–9   Components of Nationwide Johne’s Disease Herd Status/Control Programs   97 6–1   Clinical Features of Crohn’s Disease and Johne’s Disease   111 6–2   Pathologic Features of Crohn’s Disease and Johne’s Disease   112 6–3   Antimycobacterial Therapy Studies for Crohn’s Disease   113 BOXES ES-1   Components of a Coordinated Industry/Government JD Control Program   5 4–1   Approval Process for Laboratories Performing Official Johne’s Disease Tests   86 4–2   Approval Process for Laboratories Performing Johne’s Disease Screening Tests (Serology Tests)   86 7–1   Components of a Coordinated Industry/Government JD Control Program   125 FIGURES 4–1   Johne’s Disease State Control Programs, January 2002   92 4–2   Johne’s Disease State Certification and Status Programs, January 2002   93 4–3   Johne’s Disease State Advisory Committees, January 2002   93