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European Journal of Wildlife Research

, Volume 60, Issue 1, pp 113–123 | Cite as

Risk factors for the detected presence of Mycobacterium bovis in cattle in south central Spain

  • Catherine E. Cowie
  • Beatriz Beltran Beck
  • Christian Gortazar
  • Joaquin Vicente
  • Michael R. Hutchings
  • Dominic Moran
  • Piran C. L. WhiteEmail author
Original Paper

Abstract

Tuberculosis (TB) is a chronic bacterial disease of livestock and wildlife, which has major social and economic costs. In Spain, cattle test-and-slaughter schemes have dramatically reduced TB levels, but a wildlife reservoir of the disease is thought to be preventing total eradication. We aim to identify the risk factors for the presence of TB in cattle in Spain. In this case–control study, we combined a farmer-based questionnaire and participatory mapping with government records in Almodovar, Spain. Data were collected from a mixture of TB-free and TB-infected farms, yielding a total sample of 73 farms. Generalised linear modelling and information theory were used to identify the risk factors strongly associated with TB, and farmers were also asked their opinions on TB and wildlife management. The risk factors most strongly associated with TB on a farm were the presence of wildlife, the number of streams per hectare and feeding volume foods (e.g. hay) on the ground. Farmers’ opinions about TB were influenced by their experience of the disease and their interactions with wildlife. The results highlight the complexities of managing TB, and demonstrate the need for a system-level understanding of the inter-relationships among epidemiological, ecological, environmental, social and political risk factors.

Keywords

Questionnaire Risk factors Wildlife reservoir Disease management Participatory GIS Tuberculosis 

Notes

Acknowledgments

Our deep gratitude goes to all the farmers who gave up their time to take part in this study. We thank the many colleagues at IREC who helped to make this work possible. This study was funded by Plan Nacional/FEDER research project AGL2010- 55120730-C02-01 (Ministerio de Economía y Competitividad). We also thank the Agriculture department of the Regional Government of Castilla–La Mancha (JCCM) for providing data from animal health campaigns. Pilar García-Jané (JCCM) and Jose Luis Sáez (MARM) made valuable comments on an earlier draft of the paper.

Ethical standards

This study conforms with the current laws of the country (Spain) where it was conducted.

Conflict of interest

The authors declare they have no conflict of interest.

Supplementary material

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10344_2013_757_MOESM2_ESM.pdf (468 kb)
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10344_2013_757_MOESM3_ESM.pdf (286 kb)
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References

  1. Acevedo P, Vicente J, Höfle U, Cassinello J, Ruiz-Fons F, Gortazar C (2007) Estimation of European wild boar relative abundance and aggregation: a novel method in epidemiological risk assessment. Epidemiol Infect 135:519–527. doi: 10.1017/S0950268806007059 PubMedCrossRefGoogle Scholar
  2. Acevedo P, Ruiz-Fons F, Vicente J, Reyes-García AR, Alzaga V, Gortázar C (2008) Estimating red deer abundance in a wide range of management situations in Mediterranean habitats. J Zool 276:37–47. doi: 10.1111/j.1469-7998.2008.00464.x CrossRefGoogle Scholar
  3. Allepuz A, Casal J, Napp S, Saez M, Alba A, Vilar M, Domingo M et al (2011) Analysis of the spatial variation of bovine tuberculosis disease risk in Spain (2006–2009). Prev Vet Med 100:44–52. doi: 10.1016/j.prevetmed.2011.02.012 PubMedCrossRefGoogle Scholar
  4. Austin Z, Cinderby S, Smart JCR, Raffaelli D, White PCL (2009) Mapping wildlife: integrating stakeholder knowledge with modelled patterns of deer abundance by using participatory GIS. Wildl Res 36:553–564. doi: 10.1071/WR08153 CrossRefGoogle Scholar
  5. Austin Z, Smart JCR, Yearley S, Irvine RJ, White PCL (2010) Identifying conflicts and opportunities for collaboration in the management of a wildlife resource: a mixed-methods approach. Wildl Res 37:647–657CrossRefGoogle Scholar
  6. Balseiro A, Merediz I, Sevilla IA, García-Castro C, Gortázar C, Prieto JM, Delahay RJ (2011) Infection of Eurasian badgers (Meles meles) with Mycobacterium avium complex (MAC) bacteria. Vet J 188(2):231–233. doi: 10.1016/j.tvjl.2010.05.003 PubMedCrossRefGoogle Scholar
  7. Barasona JA, VerCauteren KA, Saklou N, Gortazar C, Vicente J (2013) Effectiveness of cattle operated bump gates and exclusion fences in preventing ungulate multi-host sanitary interaction. Prev Vet Med 111:42–50. doi: 10.1016/j.prevetmed.2013.03.009
  8. Beltrán-Beck B, Ballesteros C, Vicente J, de la Fuente J, Gortázar C (2012) Progress in oral vaccination against tuberculosis in its main wildlife reservoir in Iberia, the Eurasian wild boar. Vet Med Int article ID: 978501. doi: 10.1155/2012/978501
  9. Brook RK (2010) Incorporating farmer observations in efforts to manage bovine tuberculosis using barrier fencing at the wildlife-livestock interface. Prev Vet Med 94:301–305. doi: 10.1016/j.prevetmed.2010.01.010 PubMedCrossRefGoogle Scholar
  10. Brook RK, McLachlan SM (2006) Factors influencing farmers’ concerns regarding bovine tuberculosis in wildlife and livestock around Riding Mountain National Park. J Environ Manage 80:156–166. doi: 10.1016/j.jenvman.2005.08.022 PubMedCrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  12. Carstensen M, O'Brien DJ, Schmitt SM (2011) Public acceptance as a determinant of management strategies for bovine tuberculosis in free-ranging U.S. wildlife. Vet Microbiol 151:200–204PubMedCrossRefGoogle Scholar
  13. Carter SP, Delahay RJ, Smith GC, Macdonald DW, Riordan P, Etherington TR, Pimley ER et al (2007) Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology. Proc Biol Sci 274:2769–2777. doi: 10.1098/rspb.2007.0998 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Corner LAL (2006) The role of wild animal populations in the epidemiology of tuberculosis in domestic animals: how to assess the risk. Vet Microbiol 112:303–312. doi: 10.1016/j.vetmic.2005.11.015 PubMedCrossRefGoogle Scholar
  15. Diez M, Huerta C, Moreno T, Caloto T, Guerra D, Pozo F, Alcaide J, et al (2002) Tuberculosis in Spain: epidemiological pattern and clinical practice. Int J Tuberc Lung Dis 6:295–300. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11936737 Google Scholar
  16. Donnelly CA, Wei G, Johnston WT, Cox DR, Woodroffe R, Bourne FJ, Cheeseman CL et al (2007) Impacts of widespread badger culling on cattle tuberculosis: concluding analyses from a large-scale field trial. Int J Infect Dis 11:300–308. doi: 10.1016/j.ijid.2007.04.001 PubMedCrossRefGoogle Scholar
  17. Dougill AJ, Fraser EDG, Holden J, Hubacek K, Prell C, Reed MS, Stagl S et al (2006) Learning from doing participatory rural research: lessons from the Peak District National Park. J Agric Econ 57:259–275. doi: 10.1111/j.1477-9552.2006.00051.x CrossRefGoogle Scholar
  18. Gaspar P, Escribano M, Mesías FJ, Ledesma ARD, Pulido F (2008) Sheep farms in the Spanish rangelands (dehesas): typologies according to livestock management and economic indicators. Small Rumin Res 74:52–63. doi: 10.1016/j.smallrumres.2007.03.013 CrossRefGoogle Scholar
  19. Gaspar P, Mesı FJ, Escribano M, Pulido F (2009) Sustainability in Spanish extensive farms (dehesas): an economic and management indicator-based evaluation. Rangeland Ecol Manage 62:153–162CrossRefGoogle Scholar
  20. Gomez-Laguna J, Carrasco L, Ramis G, Quereda J, Gomez S, Pallares F (2010) Use of real-time and polymerase chain reaction assays for the diagnosis of porcine tuberculosis in formalin-fixed, paraffin-embedded tissues. J Vet Diagn Investig 22:123–128CrossRefGoogle Scholar
  21. Gormley E, Corner L (2009) Control of TB in wildlife by oral BCG vaccination. Expert Rev Vaccines 8:1339–1342PubMedCrossRefGoogle Scholar
  22. Gortázar C, Vicente J, Samper S, Garrido JM, Fernandez-de-Mera IG, Gavín P, Juste RA et al (2005) Original article molecular characterization of Mycobacterium tuberculosis complex isolates from wild ungulates in south-central Spain. Vet Res 36:43–52. doi: 10.1051/vetres PubMedCrossRefGoogle Scholar
  23. Gortázar C, Torres MJ, Vicente J, Acevedo P, Reglero M, de la Fuente J, Negro JJ et al (2008) Bovine tuberculosis in Doñana Biosphere Reserve: the role of wild ungulates as disease reservoirs in the last Iberian lynx strongholds. PLoS One 3(7):e2776. doi: 10.1371/journal.pone.0002776 PubMedCentralPubMedCrossRefGoogle Scholar
  24. Gortázar C, Ferroglio E, Lutton CE, Acevedo P (2010) Disease-related conflicts in mammal conservation. Wildl Res 37:668–675CrossRefGoogle Scholar
  25. Gortázar C, Vicente J, Boadella M, Ballesteros C, Galindo RC, Garrido J, Aranaz A et al (2011) Progress in the control of bovine tuberculosis in Spanish wildlife. Vet Microbiol 151:170–178. doi: 10.1016/j.vetmic.2011.02.041 PubMedCrossRefGoogle Scholar
  26. Griffin J (1993) The association of cattle husbandry practices, environmental factors and farmer characteristics with the occurrence of chronic bovine tuberculosis in dairy herds in the Republic of Ireland. Prev Vet Med 17:145–160. doi: 10.1016/0167-5877(93)90025-O CrossRefGoogle Scholar
  27. Griffin J (1996) A case–control study on the association of selected risk factors with the occurrence of bovine tuberculosis in the Republic of Ireland. Prev Vet Med 27:217–229. doi: 10.1016/0167-5877(95)00571-4 CrossRefGoogle Scholar
  28. Gutierrez M, Marin JFG (1999) Cryptococcus neoformans and Mycobacterium bovis causing granulomatous pneumonia in a goat. Vet Pathol 36:445–448. doi: 10.1354/vp.36-5-445 PubMedCrossRefGoogle Scholar
  29. Hegyi G, Garamszegi LZ (2011) Using information theory as a substitute for stepwise regression in ecology and behaviour. Behav Ecol Sociobiol 65:69–76CrossRefGoogle Scholar
  30. Irvine RJ, Fiorini S, Yearley S, McLeod JE, Turner A, Armstrong H, White PCL et al (2009) Can managers inform models? Integrating local knowledge into models of red deer habitat use. J Appl Ecol 46:344–352. doi: 10.1111/j.1365-2664.2009.01626.x CrossRefGoogle Scholar
  31. Jenkins HE, Woodroffe R, Donnelly CA (2010) The duration of the effects of repeated widespread badger culling on cattle tuberculosis following the cessation of culling. PLoS One 5:e9090. doi: 10.1371/journal.pone.0009090 PubMedCentralPubMedCrossRefGoogle Scholar
  32. Kaneene JB, Bruning-Fann CS, Granger LM, Miller RA, Porter-Spalding BA (2002) Environmental and farm management factors associated with tuberculosis on cattle farms in northeastern Michigan. J Am Vet Med Assoc 221:837–842PubMedCrossRefGoogle Scholar
  33. Lopez-Valencia G, Renteria-Evangelista T, Williams JDJ, Licea-Navarro A, Mora-Valle ADL, Medina-Basulto G (2010) Field evaluation of the protective efficacy of Mycobacterium bovis BCG vaccine against bovine tuberculosis. Res Vet Sci 88:44–49. doi: 10.1016/j.rvsc.2009.05.022 PubMedCrossRefGoogle Scholar
  34. Marangon S, Martini M, Dalla Pozza M, Neto F (1998) A case–control study on bovine tuberculosis in the Veneto Region (Italy). Prev Vet Med 34:87–95. http://www.ncbi.nlm.nih.gov/pubmed/9604258 Google Scholar
  35. Massei G, Cowan DP, Coats J, Gladwell F, Lane JE, Miller LA (2008) Effect of the GnRH vaccine GonaCon on the fertility, physiology and behaviour of wild boar. Wildl Res 35:540–547. doi: 10.1071/WR07132 CrossRefGoogle Scholar
  36. Milan M, Bartolome J, Quintanilla R, Garcia-Cachan M, Espejo M, Herraiz P, Sanchez-Recio J et al (2006) Structural characterisation and typology of beef cattle farms of Spanish wooded rangelands (dehesas). Livest Sci 99:197–209CrossRefGoogle Scholar
  37. Moda G, Daborn CJ, Grange JM, Cosivi O (1996) The zoonotic importance of Mycobacterium bovis. Tuberc Lung Dis 77:103–108CrossRefGoogle Scholar
  38. Naranjo V, Gortazar 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 127:1–9. doi: 10.1016/j.vetmic.2007.10.002 PubMedCrossRefGoogle Scholar
  39. Parra A, Fernández-Llario P, Tato A, Larrasa J, Garcı́a A, Alonso J, Hermoso de Mendoza M et al (2003) Epidemiology of Mycobacterium bovis infections of pigs and wild boars using a molecular approach. Vet Microbiol 97:123–133. doi: 10.1016/j.vetmic.2003.08.007 PubMedCrossRefGoogle Scholar
  40. Phillips CJC, Foster CRW, Morris PA, Teverson R (2003) The transmission of Mycobacterium bovis infection to cattle. Res Vet Sci 74:1–15. http://www.ncbi.nlm.nih.gov/pubmed/12507561
  41. Plieninger T, Pulido FJ, Schaich H (2004) Effects of land-use and landscape structure on holm oak recruitment and regeneration at farm level in Quercus ilex L. dehesas. J Arid Environ 57:345–364. doi: 10.1016/S0140-1963(03)00103-4 CrossRefGoogle Scholar
  42. R Core Team (2013) A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.r-project.org/. Accessed 14 Dec 2012
  43. Radostits OM, Gay CC, Hinchcliff KW, Constable PD (2007) Veterinary medicine: a textbook of the diseases of cattle, horses, sheep, pigs and goats. Springer, New YorkGoogle Scholar
  44. Ramirez-Villaescusa A, Medley GF, Mason S, Green LE (2010) Risk factors for herd breakdown with bovine tuberculosis in 148 cattle herds in the south west of England. Prev Vet Med 95:224–230. doi: 10.1016/j.prevetmed.2010.03.009 PubMedCrossRefGoogle Scholar
  45. Ramsey DSL, Efford MG (2010) Management of bovine tuberculosis in brushtail possums in New Zealand: predictions from a spatially explicit, individual-based model. J Appl Ecol 47:911–919CrossRefGoogle Scholar
  46. RASVE (2011) Informe final téchnico-financiero programa nacional de la tuberculosis bovine año 2010. http://rasve.mapa.es/publica/programas/NORMATIVAYPROGRAMAS\PROGRAMAS\2011\TUBERCULOSIS BOVINA\PROGRAMA TB 2011.PDF. Accessed 4 Dec 2011
  47. Reed M (2008) Stakeholder participation for environmental management: a literature review. Biol Conserv 141:2417–2431. doi: 10.1016/j.biocon.2008.07.014 CrossRefGoogle Scholar
  48. Richards SA, Whittingham MJ, Stephens PA (2011) Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. Behav Ecol Sociobiol 65:77–89CrossRefGoogle Scholar
  49. Royal Decree 1082/2009 (2009) General provisions for the ministry for the rural and marine environment. Issued by the Boletín Oficial del Estado 177: p62851. http://www.boe.es/boe/dias/2009/07/23/pdfs/BOE-A-2009-12206.pdf. Accessed 28 Nov 2012
  50. Sandström P, Pahlén TG, Edenius L, Tømmervik H, Hemberg L, Olsson H, Baer K et al (2003) Conflict resolution by participatory GIS management: remote sensing and as tools for communicating needs for in northern reindeer herding Sweden. Ambio 32:557–567PubMedGoogle Scholar
  51. Sleeman DP, Davenport J, More SJ, Clegg TA, Collins JD, Martin SW, Williams DH et al (2009) How many Eurasian badgers Meles meles L. are there in the Republic of Ireland? Eur J Wildl Res 55:333–344. doi: 10.1007/s10344-008-0244-1 CrossRefGoogle Scholar
  52. Sobrino R, Martin-Hernando M, Vicente J, Aurtenetxe O, Garrido JM, Gortázar C (2008) Bovine tuberculosis in a badger (Meles meles) in Spain. Vet Rec 163:159–160PubMedCrossRefGoogle Scholar
  53. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  54. Vicente J, Hoflea U, Garrido JM, Fernandez-de-Mera IG, Juste R, Barral M, Gortazar C (2006) Wild boar and red deer display high prevalences of tuberculosis-like lesions in Spain. Vet Res 37:107–119. doi: 10.1051/vetres PubMedCrossRefGoogle Scholar
  55. Ward AI, Judge J, Delahay RJ (2010) Farm husbandry and badger behaviour: opportunities to manage badger to cattle transmission of Mycobacterium bovis? Prev Vet Med 93:2–10. doi: 10.1016/j.prevetmed.2009.09.014 PubMedCrossRefGoogle Scholar
  56. White PCL, Lewis AJG, Harris S (1997) Fertility control as a means of controlling bovine tuberculosis in badger (Meles meles) populations in south-west England: predictions from a spatial stochastic simulation model. Proc R Soc Lond B 264:1737–1747CrossRefGoogle Scholar
  57. White PCL, Jennings NV, Renwick AR, Barker NHL (2005) Questionnaires in ecology: a review of past use and recommendations for best practice. J Appl Ecol 42:421–430. doi: 10.1111/j.1365-2664.2005.01032.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Catherine E. Cowie
    • 1
    • 2
  • Beatriz Beltran Beck
    • 2
  • Christian Gortazar
    • 2
  • Joaquin Vicente
    • 2
  • Michael R. Hutchings
    • 3
  • Dominic Moran
    • 3
  • Piran C. L. White
    • 1
    Email author
  1. 1.Environment DepartmentUniversity of YorkHeslingtonUK
  2. 2.IREC Wildlife Research Institute (CSIC–UCLM–JCCM)Ciudad RealSpain
  3. 3.Scottish Agricultural CollegeEdinburghUK

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