Advertisement

Animal tuberculosis in a free-ranging fallow deer in northwest Italy: a case of “lucky strain survival” or multi-host epidemiological system complexity?

  • Alessia Di Blasio
  • Katia Varello
  • Nicoletta Vitale
  • Lara Irico
  • Elena Bozzetta
  • Maria Goria
  • Laura Chiavacci
  • Simona ZoppiEmail author
  • Alessandro Dondo
Original Article
  • 2 Downloads

Abstract

We report the first case of Mycobacterium bovis infection in a free-living fallow deer (Dama dama) in northwest Italy, the epidemiological analysis (i.e., tracing source and dissemination during outbreaks), and the potential source of infection in a historically animal tuberculosis (aTB)-free area. Gross lung and lymph node lesions were histologically consistent with a severe parasitic bronchopneumonia due to lungworms associated with severe mycobacterial infection. The lesions contained numerous densely packaged, acid-fast bacilli, raising suspicion of an active, open form of aTB. Acid-fast organisms were characterized as M. bovis SB0120-ETR 45533, one of the most common profiles in Italy. Epidemiological investigation into the most recent outbreaks caused by M. bovis SB0120-ETR 45533 within a 50-km radius of where the fallow deer was retrieved disclosed two different situations: one case involving a water buffalo (Bubalus bubalis) in 2008 and one involving a donkey in 2016. Analysis of spoligotype and VNTR-type pattern circulating and recorded in northwest Italy from 1999 to 2014 suggested that in the cases of the donkey and the fallow deer, the source of infection was most likely attributable to spillover from outbreaks in domestic species: cattle and water buffalo, respectively. According to the European Commission, aTB status of livestock does not depend on aTB cases in wildlife (Council Directive 64/432/33C of 26 June 1964); nevertheless, the primary aim of aTB eradication should include global monitoring of all susceptible species if the re-emergence of M. bovis from established wildlife reservoir is to be prevented.

Keywords

Mycobacterium bovis Fallow deer Donkey Water buffalo 

Notes

Acknowledgments

We thank the staff of the General Diagnostic and Biotechnology laboratories of our Institute for their technical assistance.

Funding information

This study was in part funded by the Italian Ministry of Health (Project n. IZS PLV 06/16 RC).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10344_2019_1316_MOESM1_ESM.doc (60 kb)
ESM 1 (DOC 60 kb)
10344_2019_1316_MOESM2_ESM.doc (78 kb)
ESM 2 (DOC 78 kb)

References

  1. Abernethy DA, Denny GO, Menzies FD, McGuckian P, Honhold N, Roberts AR (2006) The Northern Ireland programme for the control and eradication of Mycobacterium bovis. Vet Microbiol 112(2–4):231–237CrossRefGoogle Scholar
  2. Amato B, Mignacca SA, Pacciarini ML, Vitale M, Antoci S, Cucinotta S, Puleio R, Biasibetti E, Fiasconaro M, Capucchio MT, Di Marco Lo Presti V (2016) An outbreak of bovine tuberculosis in a fallow deer herd (Dama dama) in Sicily. Res Vet Sci 106:116–120CrossRefGoogle Scholar
  3. Amato B, Di Marco Lo Presti V, Gerace E, Capucchio MT, Vitale M, Zanghì P, Pacciarini ML, Marianelli C, Boniotti MB (2017) Molecular epidemiology of Mycobacterium tuberculosis complex strains isolated from livestock and wild animals in Italy suggests the need for a different eradication strategy for bovine tuberculosis. Transbound Emerg Dis 1–9Google Scholar
  4. Aranaz A, De Juan L, Montero N, Sánchez C, Galka M, Delso C, Alvarez J, Romero B, Bezos J, Vela AI, Briones V, Mateos A, Domínguez L (2004) Bovine tuberculosis (Mycobacterium bovis) in wildlife in Spain. J Clin Microbiol 42(6):2602–2608CrossRefGoogle Scholar
  5. Balseiro A, Oleaga A, Orusa R, Robetto S, Zoppi S, Dondo A, Goria M, Gortázar C, Marin JFG, Domenis L (2009) Tuberculosis in roe deer from Spain and Italy. Vet Rec 164:468–470CrossRefGoogle Scholar
  6. Bellio A, Traversa A, Adriano D, Bianchi MD, Colzani A, Gili S, Dondo A, Gallina S, Grattarola C, Maurella C, Zoppi S, Zuccon F, Decastelli L (2014) Occurrence of thermotolerant Campylobacter in raw poultry meat, environment and pigeon stools collected in open-air markets. Ital J Food Saf 3:1706PubMedPubMedCentralGoogle Scholar
  7. Biagini D, Lazzaroni C, Zoppi S (2013) Microbial inoculum for litter conditioning in calves rearing: preliminary results on litter quality and health. Italian J Anim Sci 12:93–94Google Scholar
  8. Busch F, Bannerman F, Liggett S, Griffin F, Clarke J, Lyashchenko KP, Rhodes S (2017) Control of bovine tuberculosis in a farmed red deer herd in England. Vet Rec 180(3):8CrossRefGoogle Scholar
  9. Carnevali L, Pedrotti L, Riga F, Toso S (2009) Banca Dati Ungulati. Status, distribuzione, consistenza, gestione e prelievo venatorio delle popolazioni di Ungulati. in Italia. Rapporto 2001–2005. [117], 1–168. 2009. ISPRA (Istituto Superiore per la Protezione e la Ricerca Ambientale). Biologia e Conservazione della Fauna. http://www.isprambiente.gov.it/it/pubblicazioni/documenti-tecnici/banca-dati-ungulati-status-distribuzione. Accessed 17 October 2018
  10. Chiavacci L, Dondo A, Goria M, Moda G, Ruocco L, Vignetta P, Zoppi S (2014) Tuberculosis eradication in Italy. In: Thoen CO, Steele JH, Kaneene JB (eds) zoonotic tuberculosis: Mycobacterium bovis and other pathogenic mycobacteria, 3rd edn. Wiley & Sons, Inc., Hoboken, New Jersey, pp 357–369CrossRefGoogle Scholar
  11. Clifton-Hadley RS, Wilesmith JW (1991) Tuberculosis in deer: a review. Vet Rec 129(1):5–12CrossRefGoogle Scholar
  12. Corner LA (2006) The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Vet Microbiol 112:303–312CrossRefGoogle Scholar
  13. Cousins DV (2001) Mycobacterium bovis infection and control in domestic livestock. Rev Sci Tech 20:71–85CrossRefGoogle Scholar
  14. Delahay RJ, Smith GC, Barlow AM, Walker N, Harris A, Clifton-Hadley RS, Cheeseman CL (2007) Bovine tuberculosis infection in wild mammals in the south-west region of England: a survey of prevalence and a semi-quantitative assessment of the relative risks to cattle. Vet J 173(2):287–301CrossRefGoogle Scholar
  15. Dondo A, Zoppi S, Angelillo M, Buonincontro G, Garrone A, Squadrone S, Benedetto A, Goria M (2005) Diagnosi post mortem di tubercolosi nei bovini: esiti e considerazioni sul protocollo diagnostico applicato nel periodo 2001-2004 in Piemonte. Il Progresso Veterinario 8(LX):351–358Google Scholar
  16. Fitzgerald SD, Kaneene JB (2012) Wildlife reservoirs of bovine tuberculosis worldwide: hosts, pathology, surveillance, and control. Vet Pathol 50(3):488–499CrossRefGoogle Scholar
  17. Ghavidel M, Mansury D, Nourian K, Ghazvini K (2012) The most common spoligotype of Mycobacterium bovis isolated in the world and the recommended loci for VNTR typing; a systematic review. Microb Pathog 118:310–315CrossRefGoogle Scholar
  18. Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J (2007) Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53:241–256CrossRefGoogle Scholar
  19. Gortázar C, Torres MJ, Acevedo P, Aznar J, Negro JJ, de la Fuente J, Vicente J (2011a) Fine-tuning the space, time, and host distribution of mycobacteria in wildlife. BMC Microbiol 11(1):27CrossRefGoogle Scholar
  20. Gortázar C, Vicente J, Boadella M, Ballesteros C, Galindo RC, Garrido J, Aranaz A, de la Fuente J (2011b) Progress in the control of bovine tuberculosis in Spanish wildlife. Vet Microbiol 151:170–178CrossRefGoogle Scholar
  21. Gortázar C, Delahay EJ, Mcdonald RA, Boadella M, Wilson GJ, Gavier-Widen D, Acevedo P (2012) The status of tuberculosis in European wild mammals. Mammal Rev 42:193–206CrossRefGoogle Scholar
  22. Griffin JF, Buchan GS (1994) Aetiology, pathogenesis and diagnosis of Mycobacterium bovis in deer. Vet Microbiol 40(1–2):193–205CrossRefGoogle Scholar
  23. Hardstaff JL, Marion G, Hutchings MR, White PC (2014) Evaluating the tuberculosis hazard posed to cattle from wildlife across Europe. Res Vet Sci 97:S86–S93CrossRefGoogle Scholar
  24. Hauer A, De Cruz K, Cochard T, Godreuil S, Karoui C, Henault S, Bulach T, Bañuls AL, Biet F, Boschiroli ML (2015) Genetic evolution of Mycobacterium bovis causing tuberculosis in livestock and wildlife in France since 1978. PLoS One 10(2):1–17CrossRefGoogle Scholar
  25. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK (2002) Identifying reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis 8(12):1468–1473CrossRefGoogle Scholar
  26. Iannaccone M, Cosenza G, Pauciullo A, Martino G, Capparelli R (2018) The SNP g.4667G>A at 3′UTR of IFNG gene is associated with susceptibility to bovine tuberculosis in Mediterranean water buffalo (Bubalus bubalis). Anim Genet 49(5):496–497CrossRefGoogle Scholar
  27. Johnson LK, Liebana E, Nunez A, Spencer Y, Clifton-Hadley R, Jahans K, Ward A, Barlow A, Delahay R (2008) Histological observations of bovine tuberculosis in lung and lymph node tissues from British deer. Vet J 175(3):409–412CrossRefGoogle Scholar
  28. Kohl TA, Utpatel C, Niemann S, Moser I (2018) Mycobacterium bovis persistence in two different captive wild animal populations in Germany: a longitudinal molecular epidemiological study revealing pathogen transmission by whole-genome sequencing. J Clin Microbiol 56(9):1–9CrossRefGoogle Scholar
  29. Martín-Hernando MP, Torres MJ, Aznar J, Negro JJ, Gandía A, Gortázar C (2010) Distribution of lesions in red and fallow deer naturally infected with Mycobacterium bovis. J Comp Pathol 142(1):43–50CrossRefGoogle Scholar
  30. Miller RS, Sweeney SJ (2013) Mycobacterium bovis (bovine tuberculosis) infection in north American wildlife: current status and opportunities for mitigation of risks of further infection in wildlife populations. Epidemiol Infect 141(7):1357–1370CrossRefGoogle Scholar
  31. Naranjo V, Gortázar C, Vicente J, de la Fuente J (2008) Evidence of the role of European wild boar as a reservoir of Mycobacterium tuberculosis complex. Vet Microbiol 127(1–2):1–9CrossRefGoogle Scholar
  32. Nugent G (2011) Maintenance, spillover and spillback transmission of bovine tuberculosis in multi-host wildlife complexes: a New Zealand case study. Vet Microbiol 151:34–42CrossRefGoogle Scholar
  33. O’Reilly LM, Daborn CJ (1995) The epidemiology of Mycobacterium bovis infections in animals and man: a review. Tuber Lung Dis 76(1):1–46CrossRefGoogle Scholar
  34. OIE (2008) Office International des Epizooties, Chapter 2.9.10. Verocytotoxygenic Escherichia coli in: manual of diagnostic tests and vaccines for terrestrial animals 2018, web format http://www.oie.int/international-standard-setting/terrestrial-manual/access-online/ accessed: 04/08/2018
  35. OIE (2014) Office International des Epizooties, Chapter 2.1.15. Paratuberculosis (Johne’s disease) in manual of diagnostic tests and vaccines for terrestrial animals 2018, web format http://www.oie.int/international-standard-setting/terrestrial-manual/access-online/ accessed: 04/08/2018
  36. OIE (2016a) Office International des Epizooties, Chapter 2.9.8. Salmonellosis in manual of diagnostic tests and vaccines for terrestrial animals 2018, web format http://www.oie.int/international-standard-setting/terrestrial-manual/access-online/ accessed: 04/08/2018
  37. OIE (2016b) Office International des Epizooties, Chapter 2.1.4. Brucellosis (infection with B. abortus, B. melitensis and B. suis) in manual of diagnostic tests and vaccines for terrestrial animals 2018, web format http://www.oie.int/international-standard-setting/terrestrial-manual/access-online/ accessed: 04/08/2018
  38. Parra A, Garcia A, Inglis NF, Tato A, Alonso JM, Hermoso de Mendoza M, Hermoso de Mendoza J, Larrasa J (2006) An epidemiological evaluation of Mycobacterium bovis infections in wild game animals of the Spanish Mediterranean ecosystem. Res Vet Sci 80:140–146CrossRefGoogle Scholar
  39. Pavlik I, Jahn P, Dvorska L, Bartos M, Novotny L, Halouzka R (2004) Mycobacterial infections in horses: a review of the literature. Veterinarni Medicina – UZPI 49:427–440CrossRefGoogle Scholar
  40. Peletto S, Caruso C, Cerutti F, Modesto P, Zoppi S, Dondo A, Acutis PL, Masoero L (2016) A new genotype of border disease virus with implications for molecular diagnostics. Arch Virol 161(2):471–477CrossRefGoogle Scholar
  41. Richomme C, Boadella M, Courcoul A, Durand B, Drapeau A, Corde Y, Hars J, Payne A, Fediaevsky A, Boschiroli ML (2013) Exposure of wild boar to Mycobacterium tuberculosis complex in France since 2000 is consistent with the distribution of bovine tuberculosis outbreaks in cattle. PLoS One 8(10):e77842CrossRefGoogle Scholar
  42. Rossi F, Zoppi S, Bergagna S, Tinelli F, Borella A, Bollo E, Suma G, Goria M, Dondo A (2008) Focolaio di tubercolosi da Mycobacterium bovis in un parco safari in Piemonte. Atti del X Convegno Nazionale SIDILV, pp 282–283Google Scholar
  43. Serraino A, Marchetti G, Sanguinetti V, Rossi MC, Zanoni RG, Catozzi L, Bandera A, Dini W, Mignone W, Franzetti F, Gori A (1999) Monitoring of transmission of tuberculosis between wild boars and cattle: genotypical analysis of strains by molecular epidemiology techniques. J Clin Microbiol 37(9):2766–2771PubMedPubMedCentralGoogle Scholar
  44. Smith NH (2012) The global distribution and phylogeography of Mycobacterium bovis. Infect Genet Evol 12:857–865CrossRefGoogle Scholar
  45. Woebeser G (2009) Bovine tuberculosis in Canadian wildlife: an updated history. Can Vet J 50(11):1169–1176Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Alessia Di Blasio
    • 1
  • Katia Varello
    • 1
  • Nicoletta Vitale
    • 1
  • Lara Irico
    • 1
  • Elena Bozzetta
    • 1
  • Maria Goria
    • 1
  • Laura Chiavacci
    • 1
  • Simona Zoppi
    • 1
    Email author
  • Alessandro Dondo
    • 1
  1. 1.Istituto Zooprofilattico Sperimentale del Piemonte Liguria e Valle d’AostaTurinItaly

Personalised recommendations