Bovine viral diarrhea virus in free-ranging wild ruminants in Switzerland: low prevalence of infection despite regular interactions with domestic livestock

BMC Veterinary Research

Marie-Pierre Ryser-Degiorgis¹  Corinne Hug²  Hanspeter Stalder²  Hans-Rudolf Vogt²  Julien Casaubon¹ 

[1] Centre for Fish and Wildlife Health (FIWI), Vetsuisse Faculty, University of Bern, Bern, Switzerland;Institute of Veterinary Virology (IVV), Vetsuisse Faculty, University of Bern, Bern, Switzerland

关键词: Wild ruminants;    Switzerland;    Seroprevalence;    Livestock;    Interactions;    Epidemiology;    Bovine viral diarrhea virus;   

Others  :  1119683
DOI  :  10.1186/1746-6148-8-204

 received in 2012-04-07, accepted in 2012-10-10,  发布年份 2012

【 摘 要 】

Background

In the frame of an eradication program for bovine viral diarrhea (BVD) in Swiss livestock, the question was raised whether free-ranging wildlife could threaten the success of this sanitary measure. Therefore, we conducted serological and virological investigations on BVD virus (BVDV) infections in the four indigenous wild ruminant species (roe deer, red deer, Alpine chamois and Alpine ibex) from 2009 to 2011, and gathered information on interactions between wild and domestic ruminants in an alpine environment by questionnaire survey.

Results

Thirty-two sera out of 1’877 (1.7%, 95% confidence interval [CI] 1.2-2.4) were seropositive for BVDV, and a BVDV1 sub genotype h virus was found in a seropositive chamois (0.05%, 95% CI 0.001-0.3). The seropositive animals originated from sub-alpine or alpine regions and significantly more seropositive red deer, chamois and ibex than roe deer were found. There were no statistically significant differences between sampling units, age classes, genders, and sampling years. The obtained prevalences were significantly lower than those documented in livestock, and most positive wild ruminants were found in proximity of domestic outbreaks. Additionally, BVDV seroprevalence in ibex was significantly lower than previously reported from Switzerland. The survey on interspecific interactions revealed that interactions expected to allow BVDV transmission, from physical contacts to non-simultaneous use of the same areas, regularly occur on pastures among all investigated ruminant species. Interactions involving cervids were more often observed with cattle than with small ruminants, chamois were observed with all three domestic species, and ibex interacted mostly with small ruminants. Interactions related to the use of anthropogenic food sources were frequently observed, especially between red deer and cattle in wintertime.

Conclusions

To our knowledge, this is the first report of BVDV RNA isolated from an Alpine chamois. Nevertheless, our results suggest that BVDV infections are only sporadic in Swiss wild ruminants, despite regular occurrence of interactions with potentially infected livestock. Overall, serological, virological and ethological data indicate that wildlife is currently an incidental spill-over host and not a reservoir for BVDV in Switzerland.

【 授权许可】

   
2012 Casaubon et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Bengis RG, Kock RA, Fischer J: Infectious animal diseases: the wildlife/livestock interface. Rev Sci Tech OIE 2002, 21:53-65.
• [2]Rhyan JC, Spraker TR: Emergence of diseases from wildlife reservoirs. Vet Pathol 2010, 47:34-39.
• [3]Fourichon C, Beaudeau F, Bareille N, Seegers H: Quantification of economic losses consecutive to infection of a dairy herd with bovine viral diarrhoea virus. Prev Vet Med 2005, 72:177-181. discussion 215–219
• [4]Lindberg A, Houe H: Characteristics in the epidemiology of bovine viral diarrhea virus (BVDV) of relevance to control. Prev Vet Med 2005, 72:55-73.
• [5]Bachofen C, Stalder H, Braun U, Hilbe M, Ehrensperger F, Peterhans E: Co-existence of genetically and antigenically diverse bovine viral diarrhoea viruses in an endemic situation. Vet Microbiol 2008, 131:93-102.
• [6]Frölich K, Thiede S, Kozikowski T, Jakob W: A review of mutual transmission of important infectious diseases between livestock and wildlife in Europe. Ann N Y Acad Sci 2002, 969:4-13.
• [7]Vilcek S, Nettleton PF: Pestiviruses in wild animals. Vet Microbiol 2006, 116:1-12.
• [8]Presi P, Heim D: BVD eradication in Switzerland – a new approach. Vet Microbiol 2010, 142:137-142.
• [9]Rüfenacht J, Schaller P, Audigé L, Strasser M, Peterhans E: Prevalence of cattle infected with bovine viral diarrhoea virus in Switzerland. Vet Rec 2000, 147:413-417.
• [10]Presi P, Struchen R, Knight-Jones T, Scholl S, Heim D: Bovine viral diarrhea (BVD) eradication in Switzerland – experiences of the first two years. Prev Vet Med 2011, 99:112-121.
• [11]Köppel C, Knopf L, Thür B, Vogt H, Meli M, Lutz H, Stärk K: Bovine virus diarrhea and the vector-borne diseases Anaplasmosis and Bluetongue: a sero-surveillance in free-ranging red deer (Cervus elaphus) in selected areas of Switzerland. Eur J Wildlife Res 2007, 53:226-230.
• [12]Marreros N, Hüssy D, Albini S, Frey CF, Abril C, Vogt H-R, Holzwarth N, Wirz-Dittus S, Friess M, Engels M, Borel N, Willisch CS, Signer C, Hoelzle LE, Ryser-Degiorgis M-P: Epizootiologic investigations of selected abortive agents in free-ranging Alpine ibex (Capra ibex ibex) in Switzerland. J Wildl Dis 2011, 47:530-543.
• [13]Holzwarth N, Pospischil A, Mavrot F, Vilei EM, Hilbe M, Zlinszky K, Regenscheit N, Pewsner M, Thoma R, Borel N: Occurrence of Chlamydiaceae, Mycoplasma conjunctivae, and pestiviruses in Alpine chamois (Rupicapra r. rupicapra) of Grisons, Switzerland. J Vet Diagn Invest 2011, 23:333-337.
• [14]Ryser-Degiorgis M-P, Ingold P, Tenhu H, Tebar-Less A-M, Ryser A, Giacometti M: Encounters between Alpine ibex, Alpine chamois and domestic sheep in the Swiss Alps. Hystrix 2002, 13:1-11.
• [15]Ruettimann S, Giacometti M, McElligott AG: Effect of domestic sheep on chamois activity, distribution and abundance on sub-alpine pastures. Eur J Wildlife Res 2008, 54:110-116.
• [16]Breitenmoser U, Breitenmoser-Würsten C: Der Mensch und seine Nutztiere. In Der Luchs. Ein Grossraubtier in der Kulturlandschaft. 1st edition. Salm Verlag, Wohlen, Switzerland; 2008:150-157.
• [17]Mattiello S, Redaelli W, Carenzi C, Crimella C: Effect of dairy cattle husbandry on behavioural patterns of red deer (Cervus elaphus) in the Italian Alps. Appl Anim Behav Sci 2002, 79:299.
• [18]Richomme C, Gauthier D, Fromont E: Contact rates and exposure to inter-species disease transmission in mountain ungulates. Epidemiol Infect 2006, 134:21-30.
• [19]Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J, Hoefle U, Froelich K: Diseases shared between wildlife and livestock: a European perspective. Eur J Wildlife Res 2007, 53:241-256.
• [20]Plant JW, Littlejohns IE, Gardiner AC, Vantsis JT, Huck RA: Immunological relationship between border disease, mucosal disease and swine fever. Vet Rec 1973, 92:455.
• [21]Fernández-Sirera L, Cabezón O, Rossi L, Meneguz PG, Rosell R, Casas-Díaz E, Lavín S, Marco I: Investigations of pestivirus infection in wild Caprinae in Europe. Vet Rec 2011, 169:15.
• [22]Olde Riekerink RGM, Dominici A, Barkema HW, de Smit AJ: Seroprevalence of pestivirus in four species of Alpine wild ungulates in the High Valley of Susa, Italy. Vet Microbiol 2005, 108:297-303.
• [23]Pioz M, Loison A, Gibert P, Dubray D, Menaut P, Le Tallec B, Artois M, Gilot-Fromont E: Transmission of a pestivirus infection in a population of Pyrenean chamois. Vet Microbiol 2007, 119:19-30.
• [24]Marco I, Rosell R, Cabezón O, Mentaberre G, Casas E, Velarde R, López-Olvera JR, Hurtado A, Lavín S: Epidemiological study of border disease virus infection in Southern chamois (Rupicapra pyrenaica) after an outbreak of disease in the Pyrenees (NE Spain). Vet Microbiol 2008, 127:29-38.
• [25]Martin C, Letellier C, Caij B, Gauthier D, Jean N, Shaffii A, Saegerman C: Epidemiology of Pestivirus infection in wild ungulates of the French South Alps. Vet Microbiol 2011, 147:320-328.
• [26]Krametter R, Nielsen SS, Loitsch A, Froetscher W, Benetka V, Moestl K, Baumgartner W: Pestivirus exposure in free-living and captive deer in Austria. J Wildl Dis 2004, 40:791-795.
• [27]Rossmanith W, Deinhofer M, Janacek R, Trampler R, Wilhelm E: Voluntary and compulsory eradication of bovine viral diarrhoea virus in Lower Austria. Vet Microbiol 2010, 142:143-149.
• [28]Kleinschmidt M: Prävalenz von Infektionen mit dem Virus der Bovinen Virusdiarrhoe in der Wildwiederkäuerpopulation in Zusammenhang mit der Weidehaltung von Rindern. Doctoral thesis. Ludwig-Maximilian-Universität München, Institut für Medizinische Mikrobiologie, Infektions- und Seuchenlehre der Tierärztlichen Fakultät, Germany; 2004. http://edoc.ub.uni-muenchen.de/2435/1/Kleinschmidt_Markus_J.pdf webcite
• [29]Lillehaug A, Vikøren T, Larsen I-L, Akerstedt J, Tharaldsen J, Handeland K: Antibodies to ruminant alpha-herpesviruses and pestiviruses in Norwegian cervids. J Wildl Dis 2003, 39:779-786.
• [30]Nielsen SS, Roensholt L, Bitsch V: Bovine virus diarrhea virus in free-living deer from Denmark. J Wildl Dis 2000, 36:584-587.
• [31]Schmitt D, Wittkowski G: Untersuchungen zur Verbreitung von BVD-Virusinfektionen bei Schalenwild in Bayern. Tierärztl Umschau 1999, 54:284-288.
• [32]Müller T, Kramer M, Beier D: Untersuchungen zum Vorkommen von Antikörpern gegen ausgewählte bovine und ovide Viruserkrankungen bei Reh-(Capreolus capreolus), Rot-(Cervus elaphus), Dam-(Dama dama) und Muffelwild (Ovis musimon) im Bundesland Brandenburg. Z Jagdwiss 1997, 43:166-175.
• [33]Frölich K: Bovine virus diarrhea and mucosal disease in free-ranging and captive deer (Cervidae) in Germany. J Wildl Dis 1995, 31:247-250.
• [34]Baradel JM, Barrat J, Blancou J, Boutin JM, Chastel C, Dannacher G, Delorme D, Gerard Y, Gourreau JM, Kihm U, Larenaudie B, Le Goff C, Pastoret PP, Perreau P, Schwers A, Thiry E, Trap D, Uilenberg G, Vannier P: Results of a serological survey of wild mammals in France. Rev Sci Tech OIE 1988, 7:873-883.
• [35]Frölich K, Hamblin C, Parida S, Tuppurainen E, Schettler E: Serological survey for potential disease agents of free-ranging cervids in six selected national parks from Germany. J Wildl Dis 2006, 42:836-843.
• [36]Dedek J, Loepelmann R, Kokles R, Kretzschmar M, Müller M, Bergmann H: Ergebnisse serologischer Untersuchungen auf Antikörper gegen das Virus der bovinen Virusdiarrhoe/Mucosal disease beim Rot-, Reh-, Dam- und Muffelwild. Monatsh Veterinarmed 1988, 43:63-65.
• [37]Frölich K, Hofmann M: Isolation of bovine viral diarrhea virus-like pestiviruses from roe deer (Capreolus capreolus). J Wildl Dis 1995, 31:243-246.
• [38]Fulton RW, Briggs RE, Payton ME, Confer AW, Saliki JT, Ridpath JF, Burge LJ, Duff GC: Maternally derived humoral immunity to bovine viral diarrhea virus (BVDV) 1a, BVDV1b, BVDV2, bovine herpesvirus-1, parainfluenza-3 virus bovine respiratory syncytial virus, Mannheimia haemolytica and Pasteurella multocida in beef calves, antibody decline by half-life studies and effect on response to vaccination. Vaccine 2004, 22:643-649.
• [39]Muñoz-Zanzi CA, Thurmond MC, Johnson WO, Hietala SK: Predicted ages of dairy calves when colostrum-derived bovine viral diarrhea virus antibodies would no longer offer protection against disease or interfere with vaccination. J Am Vet Med Assoc 2002, 221:678-685.
• [40]Meier P: Studies on the molecular evolution of bovine viral diarrhea virus (BVDV). Doctoral thesis. Universität Bern, Philosophisch-naturwissenschaftliche Fakultät, Switzerland; 1998.
• [41]Braun U, Schönmann M, Ehrensperger F, Hilbe M, Strasser M: Intrauterine infection with bovine virus diarrhoea virus on alpine communal pastures in Switzerland. Zentralbl Veterinarmed A 1999, 46:13-17.
• [42]Siembieda JL, Kock RA, McCracken TA, Newman SH: The role of wildlife in transboundary animal diseases. Anim Health Res Rev 2011, 12:95-111.
• [43]Benetka V, Krametter-Froetscher R, Baumgartner W, Moestl K: Investigation of the role of Austrian ruminant wildlife in the epidemiology of malignant catarrhal fever viruses. J Wildl Dis 2009, 45:508-511.
• [44]Latham J: Interspecific interactions of ungulates in European forests: an overview. For Ecol Manage 1999, 120:13-21.
• [45]Boldt A: Rhythms and patterns of activity of chamois in the Swiss Alps. Advances in Ethology 35, Supplements to Ethology 2000., 7
• [46]Georgii B, Schröder W: Home range and activity patterns of male red deer (Cervus elaphus L.) in the Alps. Oecologia 1983, 58:238-248.
• [47]Cederlund G: Activity patterns in moose and roe deer in a north boreal forest. Holarctic Ecology 1989, 12:39-45.
• [48]Meile P, Giacometti M, Ratti P: Der Steinbock - Biologie und Jagd. Salm Verlag, Wohlen, Switzerland; 2003.
• [49]Ryser-Degiorgis M-P, Bischof DF, Marreros N, Willisch C, Signer C, Filli F, Brosi G, Frey J, Vilei EM: Detection of Mycoplasma conjunctivae in the eyes of healthy, free-ranging Alpine ibex: possible involvement of Alpine ibex as carriers for the main causing agent of infectious keratoconjunctivitis in wild Caprinae. Vet Microbiol 2009, 134:368-374.
• [50]Giacometti M, Roganti R, De Tann D, Stahlberger-Saitbekova N, Obexer-Ruff G: Alpine ibex Capra ibex ibex x domestic goat C. aegagrus domestica hybrids in a restricted area of southern Switzerland. Wildlife Biol 2004, 10:137-143.
• [51]Ferretti F, Sforzi A, Lovari S: Behavioural interference between ungulate species: roe are not on velvet with fallow deer. Behav Ecol Sociobiol 2011, 65:875-887.
• [52]Hofmann A, Nievergelt B: Das jahreszeitliche Verteilungsmuster und der Aesungsdruck von Alpensteinbock, Gemse, Rothirsch und Reh in einem begrenzten Gebiet im Obergengadin. [The seasonal pattern of distribution and the grazing activity of Alpine ibex, chamois, red deer, and roe deer in a limited area in Oberengadin.]. Z Jagdwiss 1974, 18:185-212.
• [53]Gortazar C, Vicente J, Boadella M, Ballesteros C, Galindo RC, Garrido J, Aranaz A, de la Fuente J: Progress in the control of bovine tuberculosis in Spanish wildlife. Vet Microbiol 2011, 151:170-178.
• [54]Boadella M, Ruiz-Fons JF, Vicente J, Martín M, Segalés J, Gortazar C: Seroprevalence evolution of selected pathogens in Iberian wild boar. Transbound Emerg Dis 2011,  .
• [55]Thrusfield M: Veterinary Epidemiology. 3rd edition. Blackwell Science, Oxford, UK; 2005.
• [56]Giacometti M, Janovsky M, Belloy L, Frey J: Infectious keratoconjunctivitis of ibex, chamois and other Caprinae. Rev Sci Tech OIE 2002, 21:335-345.
• [57]Danuser R, Vogt H-R, Kaufmann T, Peterhans E, Zanoni R: Seroprevalence and characterization of pestivirus infections in small ruminants and new world camelids in Switzerland. Schweiz Arch Tierheilkd 2009, 151:109-117.
• [58]Gonseth Y, Wohlgemuth T, Sansonnens B, Buttler A: Les régions biogéographiques de la Suisse – Explications et division standard. Cahier de l’Environnement 2001, 137:1-48. [ http://www.bafu.admin.ch/publikationen/publikation/00207/index.html?download=NHzLpZig7t,xlnp6I0NTU042l2Z6ln1acy4Zn4Z2qZpnO2Yuq2Z6gpJCGdoF_e2ym162dpYbUzd,Gpd6emK2Oz9aGodetmqaN19XI2IdvoaCVZ,s-.pdf&lang=de webcite]
• [59]Flächenanteil der verschiedenen Bodennutzungen. http://www.bfs.admin.ch/bfs/portal/de/index/themen/02/06/ind13.indicator.130704.html?open=1305#1305 webcite
• [60]Anonymous: Agrarbericht 2011. Bundesamt für Landwirtschaft (BLW), Bern, Switzerland; 2011:284.
• [61]Thrusfield M, Ortega C, de Blas I, Noordhuizen JP, Frankena K: WIN EPISCOPE 2.0: improved epidemiological software for veterinary medicine. Vet Rec 2001, 148:567-572.
• [62]Habermehl KH: Altersbestimmung bei Wild- und Pelztieren: Möglichkeiten u. Methoden, 2nd edition. Paul Parey Verlag, Hamburg, Germany; 1985.
• [63]Canal CW, Strasser M, Hertig C, Masuda A, Peterhans E: Detection of antibodies to bovine viral diarrhoea virus (BVDV) and characterization of genomes of BVDV from Brazil. Vet Microbiol 1998, 63:85-97.
• [64]Steck F, Lazary S, Fey H, Wandeler A, Huggler C, Oppliger G, Baumberger H, Kaderli R, Martig J: Immune responsiveness in cattle fatally affected by bovine virus diarrhea-mucosal disease. Zentralbl Veterinarmed B 1980, 27:429-445.
• [65]Spearman C: The method of “right or wrong cases” (constant stimuli) without Gauss’s formulae. Br J Psychol 1908, 2:227-242.
• [66]Kärber G: Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn Schmiedebergs Arch Pharmacol 1931, 162:480-483.
• [67]Vilcek S: Development of PCR tests for the detection of bovine herpesvirus-1, bovine respiratory syncytial viruses and pestiviruses. Vet Med (Praha) 1994, 39:687-700.
• [68]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
• [69]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
• [70]Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987, 4:406-425.
• [71]Tamura K, Nei M, Kumar S: Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 2004, 101:11030-11035.
• [72]Glawischnig W, Allerberger F, Messner C, Schönbauer M, Prodinger WM: Tuberkulose-Endemie bei freilebendem Rotwild (Cervus elaphus hippelaphus) in den nördlichen Kalkalpen. Wien Tierarztl Monatsschr 2003, 90:38-44.