Advertisement

European Journal of Wildlife Research

, Volume 57, Issue 4, pp 697–706 | Cite as

Six recommendations for improving monitoring of diseases shared with wildlife: examples regarding mycobacterial infections in Spain

  • Mariana BoadellaEmail author
  • Christian Gortazar
  • Pelayo Acevedo
  • Tania Carta
  • María Paz Martín-Hernando
  • José de la Fuente
  • Joaquín Vicente
Review

Abstract

Monitoring is needed to identify changes in disease occurrence and to measure the impact of intervention. Using mycobacterial diseases as an example, we discuss herein the pros and cons of the current Spanish Wildlife Disease Surveillance Scheme providing suggestions for monitoring relevant diseases shared with wildlife in other regions facing similar challenges. Six points should be considered. This includes: (1) making sure the disease is properly monitored in the relevant domestic animals or even in humans; (2) also making sure that background information on wildlife population ecology is available to maximize the benefits of the monitoring effort; (3) selecting the appropriate wildlife hosts for monitoring, while being flexible enough to incorporate new ones if research suggests their participation; (4) selecting the appropriate methods for diagnosis and for time and space trend analysis; (5) deciding which parameters to target for monitoring; and finally (6) establishing a reasonable sampling effort and a suitable sampling stratification to ensure detecting changes over time and changes in response to management actions. Wildlife disease monitoring produces knowledge that benefits at least three different agencies, namely, animal health, public health and conservation, and these should combine efforts and resources. Setting up stable, comprehensive and accurate schemes at different spatial scales should become a priority. Resources are always a limiting factor, but experience shows that combined, cross-collaborative efforts allow establishing acceptable schemes with a low enough cost to be sustainable over time. These six steps for monitoring relevant shared diseases can be adapted to many other geographical settings and different disease situations.

Keywords

Disease monitoring Paratuberculosis Time trends Tuberculosis Wildlife diseases Zoonoses 

Notes

Acknowledgments

This is a contribution to MCINN Plan Nacional I + D+i research grant AGL2008-03875 and FEDER and to TB-STEP EU grant 212414. Studies on diseases shared between domestic animals and wildlife are also supported by Grupo Santander — Fundación Marcelino Botín. Tania Carta acknowledges a grant from Regione Sardegna, and Pelayo Acevedo and Maria Paz Martín-Hernando acknowledge a Juan de la Cierva (Fondo Social Europeo) and an ISCIII postdoctoral contract from MCINN, respectively. Jose Luis Sáez made valuable comments to the first draft.

References

  1. Acevedo P, Vicente J, Hofle 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 135:519–527PubMedCrossRefGoogle Scholar
  2. Acevedo P, Ruiz-Fons F, Vicente J, Reyes-Garcia AR, Alzaga V, Gortazar C (2008) Estimating red deer abundance in a wide range of management situations in Mediterranean habitats. J Zool 276:37–47CrossRefGoogle Scholar
  3. Acevedo P, Ferreres J, Jaroso R, Durán M, Escudero MA, Marco J et al (2010) Estimating roe deer abundance from pellet group counts in Spain: An assessment of methods suitable for Mediterranean woodlands. Ecol Indic 10:1226–1230CrossRefGoogle Scholar
  4. Aller B, Fernández-Díez M, Escudero-Díez A (1973) Paratuberculosis ovina. Supl Científico Bol Inf CGCVE 196:11–18Google Scholar
  5. Álvarez J, De Juan L, Briones V, Romero B, Aranaz A, Fernández-Garayzábal JF et al (2005) Mycobacterium avium subspecies paratuberculosis in fallow deer and wild boar in Spain. Vet Rec 156:212–213PubMedGoogle Scholar
  6. Artois M, Bengis R, Delahay R, Duchêne M, Duff P, Ferroglio E et al (2009) Wildlife disease surveillance and monitoring. In: Delahay R, Smith G, Hutchings M (eds) Management of disease in wild mammals. Springer, New YorkGoogle Scholar
  7. Aurtenetxe O, Barral M, Vicente J, de la Fuente J, Gortazar C, Juste RA (2008) Development and validation of an enzyme-linked immunosorbent assay for antibodies against Mycobacterium bovis in European wild boar. BMC Vet Res 4:43PubMedCrossRefGoogle Scholar
  8. Ballesteros C, Garrido JM, Vicente J, Romero B, Galindo RC, Minguijón E et al (2009) First data on Eurasian wild boar response to oral immunization with BCG and challenge with a Mycobacterium bovis field strain. Vaccine 27:6662–6668PubMedCrossRefGoogle Scholar
  9. Balseiro A, García Marín JF, Solano P, Garrido JM, Prieto JM (2008) Histopathological classification of lesions observed in natural cases of paratuberculosis in free-ranging fallow deer (Dama dama). J Comp Pathol 138:180–188PubMedCrossRefGoogle Scholar
  10. Beard PM, Rhind SM, Buxton D, Daniels MJ, Henderson D, Pirie A et al (2001) Natural paratuberculosis infection in rabbits in Scotland. J Comp Pathol 124:290–299PubMedCrossRefGoogle Scholar
  11. Belant JL, Deese AR (2010) Importance of wildlife disease surveillance. Human–Wildlife. Interactions 4:165–169Google Scholar
  12. Blancou J (2001) History of trichinellosis surveillance. Parasite 8:16–19Google Scholar
  13. Boadella M, Lyashchenko K, Greenwald R, Esfandiari J, Jaroso R et al (2011) Serological tests for detecting antibodies against Mycobacterium bovis and Mycobacterium avium subspecies paratuberculosis in Eurasian wild boar. J Vet Diagn Invest 23:77–83PubMedCrossRefGoogle Scholar
  14. Bouvier G (1963) Transmission possible de la Tuberculose et de la Brucellose du gibier a l’home et aux animaux domestiques et sauvages. Bull LOffice Int Epizooties 59:433–436Google Scholar
  15. Carta T, Aurtenetxe O, Sobrino R, Mamian L, Gerrikagoitia X, Balseiro A et al (2011) Erratum to: lack of evidence of paratuberculosis in wild canids from south-western Europe. Eur J Wildl Res 57(3):695Google Scholar
  16. Carta T, Martin-Hernando MP, Boadella M, Fernández-de-Mera IG, Balseiro A, Sevilla IA et al (in press) Wild red deer are not a Mycobacterium avium paratuberculosis reservoir in the Iberian Peninsula. Vet J Google Scholar
  17. Chambers MA, Rogers F, Delahay RJ, Lesellier S, Ashford R et al (2011) Bacillus Calmette-Guérin vaccination reduces the severity and progression of tuberculosis in badgers. Proc R Soc Biol Sci B. doi: 10.1098/rspb.2010.1953 Google Scholar
  18. Chen H, Smith GJD, Zhang SY, Qin K, Wang J, Li KS et al (2005) Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191–192PubMedCrossRefGoogle Scholar
  19. Chiodini RJ, Vankruiningen HJ, Merkal RS (1984) Paratuberculosis (Johne’s disease): The current status and future prospects. Cornell Vet 74:218–262PubMedGoogle Scholar
  20. Corner LAL, Murphy D, Costello E, Gormley E (2009) Tuberculosis in European badgers (Meles meles) and the control of infection with Bacille Calmette–Guérin vaccination. J Wildl Dis 45:1042–1047PubMedGoogle Scholar
  21. Delahay RJ, Cheeseman CL, Clifton-Hadley RS (2001) Wildlife disease reservoirs: the epidemiology of Mycobacterium bovis infection in the European badger (Meles meles) and other British mammals. Tuberculosis 81:43–49PubMedCrossRefGoogle Scholar
  22. Delahay RJ, Smith GC, Hutchings MR (2009) The science of wildlife disease management. In: Delahay R, Smith G, Hutchings M (eds) Management of disease in wild mammals. Springer, New York, pp 1–8CrossRefGoogle Scholar
  23. Dolan LA (1993) Badgers and bovine tuberculosis in Ireland: A review. In: Hayden TH (ed) The badger. Royal Irish Academy, Dublin, pp 108–116Google Scholar
  24. Donnelly CA, Hone J (2010) Is there an association between levels of bovine tuberculosis in cattle herds and badgers? Stat Comm Infect Dis 2:3Google Scholar
  25. European Food Safety Authority (EFSA) (2010) Technical specifications for monitoring community trends in zoonotic agents in foodstuffs and animal populations on request from EFSA. EFSA J 8:1530–1545, Available online: www.efsa.europa.eu. Accessed June 2010Google Scholar
  26. Fernández-de-Mera IG, Vicente J, Höfle U, Fons FR, Ortiz JA, Gortazar C (2009) Factors affecting red deer skin test responsiveness to bovine and avian tuberculin and to phytohaemagglutinin. Prev Vet Med 90:119–126PubMedCrossRefGoogle Scholar
  27. Garrido F, León-Vizcaíno L (1979) Diagnóstico de paratuberculosis caprina en Andalucía. In: Proceedings of the VII Congreso Nacional de Microbiología. SEM, Cádiz, p 321Google Scholar
  28. Gortazar C, Vicente J, Samper S, Garrido JM, Fernandez-de-Mera IG, Gavin P et al (2005) Molecular characterization of Mycobacterium tuberculosis complex isolates from wild ungulates in south-central Spain. Vet Res 36:43–52. doi: 10.1051/vetres:2004051 PubMedCrossRefGoogle Scholar
  29. Gortazar C, Acevedo P, Ruiz-Fons F, Vicente J (2006) Disease risks and overabundance of game species. Eur J Wildl Res 52:81–87CrossRefGoogle Scholar
  30. Gortazar C, Ferroglio E, Hofle U, Frolich K, Vicente J (2007) Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53:241–256CrossRefGoogle Scholar
  31. Gortazar C, Torres J, Vicente J, Acevedo P, Reglero M, de la Fuente J 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:e2776PubMedCrossRefGoogle Scholar
  32. Gortazar C, Vicente J, Boadella M, Ballesteros C, Galindo RC, Garrido J et al (in press) Progress in the control of bovine tuberculosis in Spanish wildlife. Vet Microbiol. doi: 10.1016/j.vetmic.2011.02.041
  33. Gortazar C, Delahay R, McDonald R, Boadella M, Wilson G, Gavier-Widen D et al (accepted for publication) The status of tuberculosis in European wildlife. Mammal RevGoogle Scholar
  34. Jewell NP (2009) Statistics for epidemiology. Chapman & Hall/CRC, WashingtonGoogle Scholar
  35. Joly DO, Samuel MD, Langenberg JA, Rolley RE, Keane DP (2009) Surveillance to detect chronic wasting disease in white-tailed deer in Wisconsin. J Wildl Dis 45:989–997PubMedGoogle Scholar
  36. King AA, Fooks AR, Aubert M, Wandeler AI (2004) Historical perspective of rabies in Europe and the Mediterranean Basin. World Organization for Animal Health (OIE), ParisGoogle Scholar
  37. Kock R, Kebkiba B, Heinonen R, Bedane B (2002) Wildlife and pastoral society — Shifting paradigms in disease control. Domestic Animal/Wildlife Interface: Issue for Disease Control, Conservation, Sustainable Food Production, and Emerging Diseases 969:24–33Google Scholar
  38. Krebs JR (1997) Bovine tuberculosis in cattle and badgers. Ministry of Agriculture, Fisheries and Food, London, p 191Google Scholar
  39. Leighton A (1995) Surveillance of wild animal diseases in Europe. Rev Sci Tech 14:819–830PubMedGoogle Scholar
  40. López G, López-Parra M, Fernández L, Martínez-Granados C, Martínez F et al (2009) Management measures to control a feline leukemia virus outbreak in the endangered Iberian lynx. Anim Conserv 12:173–182CrossRefGoogle Scholar
  41. Maio E, Carta T, Balseiro A, Sevilla IA, Romano A, Ortiz JA et al (in press) Paratuberculosis in European wild rabbits from the Iberian Peninsula. Res Vet Sci. doi: 10.1016/j.rvsc.2010.12.014
  42. Martín-Atance P, Palomares F, González-Candela M, Revilla E, Cubero MJ, Calzada J, León-Vizcaíno L (2005) Bovine tuberculosis in a free ranging red fox (Vulpes vulpes) from Doñana National Park (Spain). J Wildl Dis 41:435–436PubMedGoogle Scholar
  43. Martín-Hernando MP, Hofle U, Vicente J, Ruiz-Fons F, Vidal D, Barral M et al (2007) Lesions associated with Mycobacterium tuberculosis complex infection in the European wild boar. Tuberculosis 87:360–367PubMedCrossRefGoogle Scholar
  44. Martín-Hernando MP, Torres MJ, Aznar J, Negro JJ, Gandía A, Gortazar C (2010) Distribution of lesions in red and fallow deer naturally infected with Mycobacterium bovis. J Comp Pathol 142:43–50PubMedCrossRefGoogle Scholar
  45. McDonald RA, Delahay RJ, Carter SP, Smith GC, Cheeseman CL (2008) Perturbing implications of wildlife ecology for disease control. Trends Ecol Evol 23:53–56PubMedCrossRefGoogle Scholar
  46. Millán J, Candela MG, Palomares F, Cubero MJ, Rodríguez A, Barral M et al (2009) Disease threats to the endangered Iberian lynx (Lynx pardinus). Vet J 182:114–124PubMedCrossRefGoogle Scholar
  47. Mörner T, Obendorf D, Artois M, Woodford M (2002) Surveillance and monitoring of wildlife diseases. Rev Sci Tech 21:67–76PubMedGoogle Scholar
  48. Müller T, Teuffert J, Ziedler K, Possardt C, Kramer M, Staubach C et al (1998) Pseudorabies in the European wild boar from Eastern Germany. J Wildl Dis 34:251–258PubMedGoogle Scholar
  49. Muñoz P, Boadella M, Arnal M, de Miguel M, Revilla M, Martinez D et al (2010) Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates. BMC Infect Dis 10:46PubMedCrossRefGoogle Scholar
  50. 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 Micro 127:1–9CrossRefGoogle Scholar
  51. Naser SA, Ghobrial G, Romero C, Valentine JF (2004) Culture of Mycobacterium avium subspecies paratuberculosis from the blood of patients with Crohn’s disease. Lancet 364:1039–1044PubMedCrossRefGoogle Scholar
  52. Oleaga A, Casais R, Gonzalez-Quiros P, Prieto M, Gortazar C (2008) Sarcoptic mange in red deer from Spain: Improved surveillance or disease emergence? Vet Parasitol 154:103–113PubMedCrossRefGoogle Scholar
  53. Palmer MV (2007) Tuberculosis: A reemerging disease at the interface of domestic animals and wildlife. Curr Top Microbiol Immunol 315:195–215PubMedCrossRefGoogle Scholar
  54. Peña L, Garcia P, Jiménez MA, Benito A, Alenza MDP, Sánchez B (2006) Histopathological and immunohistochemical findings in lymphoid tissues of the endangered Iberian lynx (Lynx pardinus). Comp Immunol Microbiol Infect Dis 29:114–126PubMedCrossRefGoogle Scholar
  55. Pfeiffer DU, Robinson TP, Stevenson M, Stevens KB, Rogers DJ, Clements ACA (2008) Spatial analysis in epidemiology. Oxford University Press, New YorkCrossRefGoogle Scholar
  56. Reyes-García R, Perez-de-la-Lastra JM, Vicente J, Ruiz-Fons F, Garrido JM, Gortazar C (2008) Large-scale ELISA testing of Spanish red deer for paratuberculosis. Vet Immunol Immunopathol 124:75–81PubMedCrossRefGoogle Scholar
  57. Rhyan JC, Spraker TR (2010) Emergence of diseases from wildlife reservoirs. Vet Pathol 47:34–39PubMedCrossRefGoogle Scholar
  58. Rodríguez-Sánchez B, Gortazar C, Ruiz-Fons F, Sánchez-Vizcaíno JM (2010) Bluetongue virus serotypes 1 and 4 in red deer, Spain. Emerg Infect Dis 16:518–520PubMedCrossRefGoogle Scholar
  59. Rossi S, Artois M, Pontier D, Cruciere C, Hars J, Barrat J et al (2005) Long-term monitoring of Classical swine fever in wild boar (Sus scrofa sp.) using serological data. Vet Res 36:27–42PubMedCrossRefGoogle Scholar
  60. Ruiz-Fons F, Reyes-Garcia AR, Alcaide V, Gortazar C (2008) Spatial and temporal evolution of bluetongue virus in wild ruminants, Spain. Emerg Infect Dis 14:951–953PubMedCrossRefGoogle Scholar
  61. Santos N, Correla-Neves M, Ghebremichael S, Källenius G, Svenson SB, Almeida V (2009) Epidemiology of Mycobacterium bovis infection in wild boar (Sus scrofa) from Portugal. J Wildl Dis 45:1048–1061PubMedGoogle Scholar
  62. Santos N, Geraldes M, Afonso A, Almeida V, Correia-Neves M (2010) Diagnosis of Tuberculosis in the Wild Boar (Sus scrofa): A Comparison of Methods Applicable to Hunter-Harvested Animals. PLoS ONE 5. doi: 10.1371/journal.pone.0012663
  63. Sobrino R, Martín-Hernando MP, Vicente J, Gortazar C, Aurtenetxe O, Garrido JM (2008) Bovine tuberculosis in a badger (Meles meles) in Spain. Vet Rec 163:159–160PubMedCrossRefGoogle Scholar
  64. Sobrino R, Acevedo P, Escudero MA, Marco J, Gortazar C (2009) Carnivore population trends in Spanish agrosystems after the reduction in food availability due to rabbit decline by rabbit haemorrhagic disease and improved waste management. Eur J Wildl Res 55:161–165CrossRefGoogle Scholar
  65. Sobrino R, Aurtenetxe O, Carta T, Mamian L, Gerrikagoitia X, Balseiro A et al (2011) Lack of evidence of paratuberculosis in wild canids from south-western Europe. Eur J Wildl Res 57:683–688Google Scholar
  66. Tayce J, Acevedo P, Vicente J, Gortazar C (2008) Minimum sampling effort for reliable non-invasive estimations of excretion abundance of Elaphostrongylus cervi L1 in red deer (Cervus elaphus) populations. J Helminthol 82:255–261PubMedCrossRefGoogle Scholar
  67. Tompkins DM, Ramsey DSL, Cross ML, Aldwell FE, De Lisle GW, Buddle BM (2009) Oral vaccination reduces the incidence of tuberculosis in free-living brushtail possums. Proc R Soc Biol Sci B 276:2987–2995CrossRefGoogle Scholar
  68. Uzoigwe JC, Khaitsa ML, Gibbs PS (2007) Epidemiological evidence for Mycobacterium avium subspecies paratuberculosis as a cause of Crohn’s disease. Epidemiol Infect 135:1057–1068PubMedCrossRefGoogle Scholar
  69. Vicente J, Hofle U, Garrido JM, Fernandez-de-Mera IG, Juste R, Barral M et al (2006) Wild boar and red deer display high prevalences of tuberculosis-like lesions in Spain. Vet Res 37:107–119PubMedCrossRefGoogle Scholar
  70. Vicente J, Hofle U, Garrido JM, Fernandez-de-Mera IG, Acevedo P, Juste R et al (2007) Risk factors associated with the prevalence of tuberculosis-like lesions in fenced wild boar and red deer in south central Spain. Vet Res 38:451–464PubMedCrossRefGoogle Scholar
  71. Villafuerte R, Calvete C, Gortazar C, Moreno S (1994) First epizootic of rabbit hemorrhagic disease in free-living populations of Oryctolagus cuniculus at Doñana National Park, Spain. J Wildl Dis 30:176–179PubMedGoogle Scholar
  72. Wacker K, Rodriguez E, Garate T, Geue L, Tackmann K, Selhorst T, Staubach C, Conraths FJ (1999) Epidemiological analysis of Trichinella spiralis infections of foxes in Brandenburg, Germany. Epidemiol Infect 123:139–147PubMedCrossRefGoogle Scholar
  73. Wobeser G (1994) Investigation and management of disease in wild animals. Springer, New YorkGoogle Scholar
  74. Woodford MH (2009) Veterinary aspects of ecological monitoring: The natural history of emerging infectious diseases of humans, domestic animals and wildlife. Trop Anim Health Prod 41:1023–1033PubMedCrossRefGoogle Scholar
  75. Wyss D, Giacometti M, Nicolet J, Burnens A, Pfyffer GE, Audige L (2000) Farm and slaughter survey of bovine tuberculosis in captive deer in Switzerland. Vet Rec 147:713–717PubMedGoogle Scholar
  76. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Mariana Boadella
    • 1
    Email author
  • Christian Gortazar
    • 1
  • Pelayo Acevedo
    • 2
  • Tania Carta
    • 1
  • María Paz Martín-Hernando
    • 1
  • José de la Fuente
    • 1
    • 3
  • Joaquín Vicente
    • 1
  1. 1.Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC–UCLM–JCCM)Ciudad RealSpain
  2. 2.Biogeography, Diversity, and Conservation Research Team, Animal Biology, Department of SciencesUniversity of MalagaMálagaSpain
  3. 3.Department of Veterinary Pathobiology, Center for Veterinary Health SciencesOklahoma State UniversityStillwaterUSA

Personalised recommendations