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      Control of paratuberculosis: who, why and how. A review of 48 countries

      review-article
      1 , , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 , 1 , 8 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 13 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 , 29 , 30 , 31 , 32 , 33 , 5 , 34 , 35 , 36 , 37 , 13 , 38 , 39 , 40 , 41 , 42 , 42 , 43 , 44 , 45 , 46 , 47 , 48 , 49 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 36 , 60 , 44 , 61 , 62 , 63 , 64 , 65 , 64 , 66 ,   67
      BMC Veterinary Research
      BioMed Central
      Paratuberculosis, Control, Review, Prevalence, Cattle, Sheep, Goat, Camelid, Deer, Wildlife

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          Abstract

          Paratuberculosis, a chronic disease affecting ruminant livestock, is caused by Mycobacterium avium subsp. paratuberculosis (MAP). It has direct and indirect economic costs, impacts animal welfare and arouses public health concerns. In a survey of 48 countries we found paratuberculosis to be very common in livestock. In about half the countries more than 20% of herds and flocks were infected with MAP. Most countries had large ruminant populations (millions), several types of farmed ruminants, multiple husbandry systems and tens of thousands of individual farms, creating challenges for disease control. In addition, numerous species of free-living wildlife were infected. Paratuberculosis was notifiable in most countries, but formal control programs were present in only 22 countries. Generally, these were the more highly developed countries with advanced veterinary services. Of the countries without a formal control program for paratuberculosis, 76% were in South and Central America, Asia and Africa while 20% were in Europe. Control programs were justified most commonly on animal health grounds, but protecting market access and public health were other factors. Prevalence reduction was the major objective in most countries, but Norway and Sweden aimed to eradicate the disease, so surveillance and response were their major objectives. Government funding was involved in about two thirds of countries, but operations tended to be funded by farmers and their organizations and not by government alone. The majority of countries (60%) had voluntary control programs. Generally, programs were supported by incentives for joining, financial compensation and/or penalties for non-participation. Performance indicators, structure, leadership, practices and tools used in control programs are also presented. Securing funding for long-term control activities was a widespread problem. Control programs were reported to be successful in 16 (73%) of the 22 countries. Recommendations are made for future control programs, including a primary goal of establishing an international code for paratuberculosis, leading to universal acknowledgment of the principles and methods of control in relation to endemic and transboundary disease. An holistic approach across all ruminant livestock industries and long-term commitment is required for control of paratuberculosis.

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          The online version of this article (10.1186/s12917-019-1943-4) contains supplementary material, which is available to authorized users.

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          Most cited references166

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          Herd-level economic losses associated with Johne's disease on US dairy operations.

          Johne's disease ('paratuberculosis') is a chronic, infectious, wasting disease that affects dairy cattle. Estimation of its impact on herd productivity and corresponding economic loss on US dairy operations was part of the USDA National Animal Health Monitoring System's (NAHMS) 1996 national dairy study. Johne's-positive herds experience an economic loss of almost US\(100 per cow when compared to Johne's-negative herds due to reduced milk production and increased cow-replacement costs. For Johne's-positive herds that reported at least 10% of their cull cows as having clinical signs consistent with Johne's disease, economic losses were over US\) 200 per cow. These high-prevalence herds experienced reduced milk production of over 700 kg per cow, culled more cows but had lower cull-cow revenues, and had greater cow mortality than Johne's-negative herds. Averaged across all herds, Johne's disease costs the US dairy industry, in reduced productivity, US\(22 to US\) 27 per cow or US\(200 to US\) 250 million annually.
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            Ante mortem diagnosis of paratuberculosis: a review of accuracies of ELISA, interferon-gamma assay and faecal culture techniques.

            Infections with Mycobacterium avium subsp. paratuberculosis (MAP) can be latent for years without affecting the animal, but the animal may become infectious or clinical at some point. Diagnosis of paratuberculosis can be a challenge primarily in latent stages of the infection, and different diagnosis interpretations are usually required by the variety of decision makers. The objective of this paper was to provide a critical review of reported accuracies of ELISA tests, interferon-gamma assays (IFN-gamma) and faecal culture (FC) techniques used for diagnosis of three defined target conditions: MAP infected, MAP infectious and MAP affected animals. For each animal species, target condition and diagnostic test-type, sensitivities (Se) and specificities (Sp) were summarised based on a systematic, critical review of information in literature databases. The diagnostic test information often varied substantially for tests of the same type and make, particularly ELISA, which was the most frequently reported test-type. Comparison of the various tests accuracies was generally not possible, but stratification of test-evaluations by target condition improved the interpretation of the test accuracies. Infectious and affected animals can often be detected, but Se for infected animals is generally low. A main conclusion of the review was that the quality of design, implementation and reporting of evaluations of tests for paratuberculosis is generally poor. Particularly, there is a need for better correspondence between the study population and target population, i.e. the subjects chosen for test evaluation should reflect the distribution of animals in the population where the test is intended to be used.
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              Evidence for age susceptibility of cattle to Johne's disease.

              Calf rearing programs for the control of bovine Johne's disease (BJD) in dairy farms have been widely adopted globally and are based on evidence that the most significant risk factor for developing the disease is exposure of young calves to infectious doses of the causative organism Mycobacterium avium subsp. paratuberculosis (Mptb). Hygienic calf rearing practices aim to break the transmission cycle of Mptb by removing neonatal calves from their dams within 12h of birth and segregating replacement heifers from the herd until they are 12 months of age. But compliance with these interventions is difficult for many producers and delaying the removal of calves from their dams and earlier return of heifers to the herd are common practices. However, would changing these practices increase the risk of animals contracting BJD? Evidence for age susceptibility of calves and young adults to Mptb is reviewed. The experimental studies selected for inclusion in an analysis of the evidence were those designed specifically to address the issue and were confined to examination of 140 cattle in experiments conducted by eight groups of workers between the years 1938 and 2006. Approximately 75% of calves 12 months old developed lesions indicative of BJD infection when exposed to any of the tested routes of Mptb infection. No direct evidence was found to support the commonly held view that calf removal from the dam for a maximum period of 12h is preferable to 24h. However the studies did show that if exposure to infection occurs at birth, then the risk of infection progressing to BJD is high, particularly in a highly contaminated environment or if the dam is infected. Copyright 2009 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                02 9351 1619 , richard.whittington@sydney.edu.au
                kdonat@thueringertierseuchenkasse.de
                m.weber@gdanimalhealth.com
                dkelton@uoguelph.ca
                saxmose@sund.ku.dk
                Eisenberg@ndstsk.de
                norma.arrigoni@izsler.it
                rajuste@serida.org
                jsaezllo@mapama.es
                navneet.dhand@sydney.edu.au
                annalisa.santi@izsler.it
                anita.michel@up.ac.za
                barkema@ucalgary.ca
                kralik@vri.cz
                pkost@vet.uth.gr
                lciter@animalhealthireland.ie
                frank.griffin@otagoinnovation.com
                rbarwell@animalhealthaustralia.com.au
                masm@ufv.br
                slana@vri.cz
                Heike.Koehler@fli.de
                shoorvir_singh@rediffmail.com
                yoohs@snu.ac.kr
                gris@unam.mx
                agoodridge@indicasat.org.pa
                Matjaz.Ocepek@vf.uni-lj.si
                jgarrido@neiker.eus
                Karen.Stevenson@moredun.ac.uk
                michael.t.collins@wisc.edu
                balonso@senasa.gov.ar
                cirone.karina@inta.gob.ar
                paolicchi.fernando@inta.gob.ar
                Lawrence.Gavey@daf.qld.gov.au
                tanvirahman@bau.edu.bd
                emmanuelle.demarchin@arsia.be
                Willem.VanPraet@dgz.be
                cbauman@uoguelph.ca
                gilles.fecteau@umontreal.ca
                slmckenna@upei.ca
                miguelsalgado@uach.cl
                jorge.fernandez@udea.edu.co
                dziedzinska@vri.cz
                gustavo_echeverria@live.com
                jaana.seppanen@foodauthority.fi
                virginie.thibault.reseaugds@anses.fr
                valaf@hi.is
                drkhshnd77@gmail.com
                mhaghkha@shirazu.ac.ir
                l.ruocco@sanita.it
                skawaji@affrc.go.jp
                eiichimomotani@gmail.com
                C.Heuer@massey.ac.nz
                solis.norton@deerpro.org.nz
                Simeonc5@gmail.com
                angelika.agdestein@vetinst.no
                annette.kampen@vetinst.no
                szteyn@uwm.edu.pl
                jenny.frossling@sva.se
                ebba.schwan@gardochdjurhalsan.se
                George.Caldow@sac.co.uk
                sam.strain@animalhealthni.com
                Michael.A.Carter@aphis.usda.gov
                wells023@umn.edu
                Mussomunyeme@gmail.com
                robert.wolf@stmk.gv.at
                rgur1038@uni.sydney.edu.au
                cristobal.verdugo@uach.cl
                christine.fourichon@oniris-nantes.fr
                mtbook@affrc.go.jp
                sharuchanafu@gmail.com
                elena.dilabio@blv.admin.ch
                monayae@gmail.com
                adgr@fvet.edu.uy
                alnunez@adinet.com.uy
                jose.piaggio@gmail.com
                alesuanes@gmail.com
                jacobusdeward@gmail.com
                Journal
                BMC Vet Res
                BMC Vet. Res
                BMC Veterinary Research
                BioMed Central (London )
                1746-6148
                13 June 2019
                13 June 2019
                2019
                : 15
                : 198
                Affiliations
                [1 ]ISNI 0000 0004 1936 834X, GRID grid.1013.3, School of Veterinary Science, Faculty of Science, , University of Sydney, ; 425 Werombi Road, Camden, NSW 2570 Australia
                [2 ]Animal Health Service, Thuringian Animal Diseases Fund, 07745 Jena, Germany
                [3 ]ISNI 0000 0001 2165 8627, GRID grid.8664.c, Clinic for Obstetrics, Gynecology and Andrology with Veterinary Ambulance, , Justus-Liebig-University Giessen, ; 35392 Giessen, Germany
                [4 ]ISNI 0000 0000 9730 5476, GRID grid.413764.3, GD Animal Health, ; 7400 AA Deventer, The Netherlands
                [5 ]ISNI 0000 0004 1936 8198, GRID grid.34429.38, Department of Population Medicine, , University of Guelph, ; Guelph, Ontario N1G 2W1 Canada
                [6 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Department of Veterinary and Animal Sciences, , University of Copenhagen, ; DK-1870 Frederiksberg C, Denmark
                [7 ]Niedersächsische Tierseuchenkasse, 30169 Hannover, Germany
                [8 ]Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna, 29027 Podenzano, Italy
                [9 ]ISNI 0000 0004 0625 911X, GRID grid.419063.9, Servicio Regional de Investigación y Desarrollo Agroalimentario (SERIDA), ; 33300 Villaviciosa, Asturias Spain
                [10 ]Ministry of Agriculture and Fisheries, Food and Environment, ES-28071 Madrid, Spain
                [11 ]ISNI 0000 0001 2107 2298, GRID grid.49697.35, Faculty of Veterinary Science, , University of Pretoria, ; Onderstepoort, 0110 South Africa
                [12 ]ISNI 0000 0004 1936 7697, GRID grid.22072.35, Faculty of Veterinary Medicine, , University of Calgary, ; Calgary, Alberta T2N 4N1 Canada
                [13 ]ISNI 0000 0001 2285 286X, GRID grid.426567.4, Veterinary Research Institute, ; 621 00 Brno, Czech Republic
                [14 ]ISNI 0000 0001 0035 6670, GRID grid.410558.d, Faculty of Veterinary Medicine, , University of Thessaly, ; 43100 Karditsa, Greece
                [15 ]GRID grid.496876.2, Animal Health Ireland, ; Carrick on Shannon, Co. Leitrim, N41 WN27 Republic of Ireland
                [16 ]ISNI 0000 0001 2110 5328, GRID grid.417738.e, Disease Research Limited, Invermay Agricultural Centre, ; Mosgiel, 9092 New Zealand
                [17 ]Animal Health Australia, Turner, ACT 2612 Australia
                [18 ]ISNI 0000 0000 8338 6359, GRID grid.12799.34, Veterinary Department, , Universidade Federal de Viçosa, ; Viçosa, Minas Gerais 365700-900 Brazil
                [19 ]Friedrich-Loeffler-Institut, Federal Research Institute of Animal Health, 07743 Jena, Germany
                [20 ]GRID grid.448881.9, Deparment of Biotechnology, , GLA University, ; Mathura, Uttar Pradesh 281 406 India
                [21 ]ISNI 0000 0004 0470 5905, GRID grid.31501.36, Department of Infectious Diseases, College of Veterinary Medicine, , Seoul National University, ; Seoul, 08826 South Korea
                [22 ]ISNI 0000 0001 2159 0001, GRID grid.9486.3, Facultad de Medicina Veterinaria y Zootecnia, , Universidad Nacional Autonoma de México, ; 76750 Tequisquiapan, Queretaro, Mexico
                [23 ]ISNI 0000 0004 0601 8631, GRID grid.501516.6, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología, , City of Knowledge, ; Panama City, 0843-01103 Panama
                [24 ]ISNI 0000 0001 0721 6013, GRID grid.8954.0, National Veterinary Institute, Veterinary Faculty, , University of Ljubljana, ; 1000 Ljubljana, Slovenia
                [25 ]Instituto Vasco de Investigacion y Desarrollo Agrario-NEIKER, 48160 Derio, Bizkaia Spain
                [26 ]ISNI 0000 0001 2186 0964, GRID grid.420013.4, Moredun Research Institute, ; Midlothian, EH26 0PZ UK
                [27 ]ISNI 0000 0001 2167 3675, GRID grid.14003.36, School of Veterinary Medicine, , University of Wisconsin-Madison, ; Wisconsin, 53706-1102 USA
                [28 ]DILAB – SENASA, Martínez, 1640 Buenos Aires, Argentina
                [29 ]ISNI 0000 0001 2167 7174, GRID grid.419231.c, Instituto Nacional de Tecnologia Agropecuaria, ; 7620 Balcarce, Argentina
                [30 ]Biosecurity Queensland, Department of Agriculture and Fisheries, Toowoomba, Queensland 4350 Australia
                [31 ]ISNI 0000 0001 2179 3896, GRID grid.411511.1, Faculty of Veterinary Science, , Bangladesh Agricultural University, ; Mymensingh, 2202 Bangladesh
                [32 ]Regional Association for Animal Identification and Health, 5590 Ciney, Belgium
                [33 ]Animal Health Care Flanders, 2500 Lier, Belgium
                [34 ]ISNI 0000 0001 2292 3357, GRID grid.14848.31, Faculté de Médecine Vétérinaire, , University of Montreal, ; Quebec, J2S 6Z9 Canada
                [35 ]ISNI 0000 0001 2167 8433, GRID grid.139596.1, Atlantic Veterinary College, ; Charlottetown, Prince Edward Island C1A 4P3 Canada
                [36 ]ISNI 0000 0004 0487 459X, GRID grid.7119.e, Facultad de Ciencias Veterinarias, , Universidad Austral de Chile, ; 5090000 Valdivia, Chile
                [37 ]ISNI 0000 0000 8882 5269, GRID grid.412881.6, Escuela de Medicina Veterinaria, , Universidad de Antioquia, ; Medellín, Antioquia 050034076 Colombia
                [38 ]GRID grid.7898.e, Instituto de Investigación en Salud Pública y Zoonosis, , Universidad Central del Ecuador, ; 17-03-100 Quito, Ecuador
                [39 ]Finnish Food Authority, Mustialankatu 3, 00790 Helsinki, Finland
                [40 ]ANSES Laboratoire de Ploufragan-Plouzané-Niort and GDS France, CS 28440, 79024 Niort Cedex, France
                [41 ]ISNI 0000 0004 0640 0021, GRID grid.14013.37, Institute for Experimental Pathology at Keldur, University of Iceland, ; IS-112 Reykjavík, Iceland
                [42 ]ISNI 0000 0001 0745 1259, GRID grid.412573.6, School of Veterinary Medicine, , Shiraz University, ; Shiraz, 71441-69155 Iran
                [43 ]ISNI 0000 0004 1756 9674, GRID grid.415788.7, Ministry of Health, General Directorate of Animal Health and Veterinary Medicines, ; 00144 Rome, Italy
                [44 ]ISNI 0000 0004 0530 9488, GRID grid.416882.1, National Institute of Animal Health, National Agriculture and Food Research Organization, ; Tsukuba, Ibaraki, 305-0856 Japan
                [45 ]Comparative Medical Research Institute, Tsukuba, Ibaraki 305-0856 Japan
                [46 ]ISNI 0000 0001 0696 9806, GRID grid.148374.d, School of Veterinary Sciences, , Massey University, ; Palmerston North, 4441 New Zealand
                [47 ]DeerPRO, Dunedin, 9016 New Zealand
                [48 ]ISNI 0000 0004 1794 5983, GRID grid.9582.6, Department of Veterinary Public Health and Preventive Medicine, , University of Ibadan, ; Ibadan, Nigeria
                [49 ]ISNI 0000 0000 9542 2193, GRID grid.410549.d, Norwegian Veterinary Institute, ; N-0106 Oslo, Norway
                [50 ]ISNI 0000 0001 2149 6795, GRID grid.412607.6, Faculty of Veterinary Medicine, , University of Warmia and Mazury, ; 10-718 Olsztyn, Poland
                [51 ]ISNI 0000 0001 2166 9211, GRID grid.419788.b, National Veterinary Institute, ; SE-751 89 Uppsala, Sweden
                [52 ]Swedish Farm and Animal Health, 62254 Romakloster, Sweden
                [53 ]ISNI 0000 0001 0170 6644, GRID grid.426884.4, Scotland’s Rural College, ; Edinburgh, EH9 3JG UK
                [54 ]Animal Health and Welfare Northern Ireland, Dungannon Enterprise Centre, Dungannon, BT71 6JT UK
                [55 ]ISNI 0000 0001 0725 8379, GRID grid.413759.d, USDA-APHIS-Veterinary Services, ; Riverdale, MD 20737 USA
                [56 ]ISNI 0000000419368657, GRID grid.17635.36, College of Veterinary Medicine, , University of Minnesota, ; St. Paul, MN 55108 USA
                [57 ]ISNI 0000 0000 8914 5257, GRID grid.12984.36, School of Veterinary Medicine, , The University of Zambia, ; 10101 Lusaka, Zambia
                [58 ]Fachabteilung Gesundheit und Pflegemanagement, 8010 Graz, Austria
                [59 ]National Centre for Animal Health, Serbithang, Bhutan
                [60 ]Oniris – INRA, Department Farm Animal Health and Public Health, 44307 Nantes cedex 3, France
                [61 ]GRID grid.460993.1, Faculty of Animal Science, Veterinary Science and Fisheries, , Agriculture and Forestry University, ; Rampur, Chitwan Nepal
                [62 ]GRID grid.438536.f, Federal Food Safety and Veterinary Office, ; 3003 Bern, Switzerland
                [63 ]National Institute of Animal Health, Chatuchak, Bangkok, 10900 Thailand
                [64 ]ISNI 0000000121657640, GRID grid.11630.35, Facultad de Veterinaria, ; Lasplaces 1620, CP 11600 Montevideo, Uruguay
                [65 ]Ministry of Livestock Agriculture and Fisheries, CP 11400 Montevideo, Uruguay
                [66 ]Ministry of Livestock Agriculture and Fisheries of Uruguay, CP 11300 Montevideo, Uruguay
                [67 ]ISNI 0000 0001 2155 0982, GRID grid.8171.f, Servicio Autonomo Instituto de Biomedicina, , Universidad Central de Venezuela, ; Caracas, Venezuela
                Author information
                http://orcid.org/0000-0003-3982-611X
                Article
                1943
                10.1186/s12917-019-1943-4
                6567393
                31196162
                e76644f9-b92b-4a17-ac74-96c482a6e631
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 9 December 2018
                : 31 May 2019
                Categories
                Review
                Custom metadata
                © The Author(s) 2019

                Veterinary medicine
                paratuberculosis,control,review,prevalence,cattle,sheep,goat,camelid,deer,wildlife
                Veterinary medicine
                paratuberculosis, control, review, prevalence, cattle, sheep, goat, camelid, deer, wildlife

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