Skip to content
Accessible Unlicensed Requires Authentication Published by De Gruyter June 5, 2013

Joint Spatio-Temporal Modeling of Mycobacterium bovis Infections in Badgers and Cattle – Results from the Irish Four Area Project

Gabrielle E. Kelly


In Ireland and in the UK, bovine tuberculosis (bTB) infects cattle and wildlife badgers (Meles meles linnaeus) and badgers contribute to the spread of the disease in cattle. Isotropic and anisotropic spatio-temporal models are fitted to cattle herd and badger sett bTB incidence data from the Four Area Project using sequences of linear geostatistical models. An association was found between the spatial distribution of the disease in cattle and badgers in two of three areas. The limited association may be due to irregularity of sett territories, fragmentation of farms, TB-test insensitivity, temporal lags associated with transmission or non-spatial transmission. A statistical methodology is outlined whereby hypotheses related to spatial correlation structure may be tested.


I thank the referees for helpful comments that greatly improved this manuscript. I would like to thank Professor Sir David Cox for helpful conversations. I thank the Center for Veterinary Epidemiology and Risk Analysis (CVERA), University College Dublin, who provided the data and maps of the FAP for this study. Finally, I would like to thank the Department of Agriculture, Food and the Marine for financial support in relation to some previous work quoted here.

Conflict of interest statement

There is no conflict of interest in relation to this work.


Ashe, S., S. More, J. O’Keeffe, P. White, G. McGrath, and I. Aznar. 2009. “Survival and Dispersal of a Defined Cohort of Irish Cattle.” Irish Veterinary Journal 62:44–9.Search in Google Scholar

Bourne, F.J., C.A. Donnelly, D.R. Cox, G. Gettinby, J.P. McInerney, W.I. Morrison, and R. Woodroffe. 2007. “A Science Base for a Sustainable Policy to Control TB in Cattle: An Epidemiological Investigation into Bovine Tuberculosis. Final report of the independent scientific group on cattle TB. London: Defra. Accessed May 29, 2013.Search in Google Scholar

Clegg, T.A., S.J. More, I.M. Higgins, M. Good, M. Blake, and D.H. Williams. 2008. “Potential Infection-Control Benefit for Ireland from Pre-movement Testing of Cattle for Tuberculosis.” Preventive Veterinary Medicine 84:94–111.Search in Google Scholar

Clegg, T.A., A. Duignan, C. Whelan, E. Gormley, M. Good, J. Clarke, N. Toft, and S.J. More. 2011. “Using Latent Class Analysis to Estimate the Test Characteristics of the γ-Interferon Test, the Single Intradermal Comparative Tuberculin Test and a Multiplex Immunoassay under Irish Conditions.” Veterinary Microbiology 151:68–76.Search in Google Scholar

Costello, E., D. O’Grady, O. Flynn, R. O’Brien, M. Rogers, F. Quigley, J. Egan, and J. Griffin. 1999. “Study of Restriction Fragment Length Polymorphism Analysis and Spoligotyping for Epidemiological Investigation of Mycobacterium bovis Infection.” Journal of Clinical Microbiology 37:3217–22.Search in Google Scholar

Cressie, N.A.C. 1993. Statistics for Spatial Data. Hoboken, NJ: Wiley, chapter 4.6.Search in Google Scholar

Diggle, P.J., and P.J. Ribeiro. 2007. Model-based Geostatistics. New York: Springer, chapter 2.Search in Google Scholar

Donnelly, C.A., G. Wei, W.T. Johnston, D.R. Cox, R. Woodroffe, F.J. Bourne, C.L. Cheeseman, R.S. Clifton-Hadley, G. Gettinby, P. Gilks, H.E. Jenkins, A.M. Le Fevre, J.P. McInerney, and W.I. Morrison. 2007. “Impacts of Widespread Badger Culling on Cattle Tuberculosis: Concluding Analyses from a Large-Scale Field Trial.” International Journal of Infectious Diseases 11:300–8.Search in Google Scholar

Etter, E., P. Donado, F. Jori, A. Caron, F. Goutard, and F. Roger. 2006. “Risk Analysis and Bovine Tuberculosis, a Re-emerging Zoonosis.” Annals of the New York Academy of Sciences 108:61–73.Search in Google Scholar

Gordejo, R.F.J., and J.P. Vermeersch. 2006. “Towards Eradication of Bovine Tuberculosis in the European Union.” European Union Veterinary Microbiology 112:101–9.Search in Google Scholar

Griffin, J.M., S.W. Martin, M.A. Thorburn, J.A. Eves, and R.F. Hammond. 1996. “A Case-control Study on the Association of Selected Risk Factors with the Occurrence of Bovine Tuberculosis in the Republic of Ireland.” Preventive Veterinary Medicine 27:75–87.Search in Google Scholar

Griffin, J.M., D.H. Williams, G.E. Kelly, T.A. Clegg, I. O’Boyle, J.D. Collins, and S.J. More. 2005. “The Impact of Badger Removal on the Control of Tuberculosis in Cattle Herds in Ireland.” Preventive Veterinary Medicine 67:237–66.Search in Google Scholar

Henley, S. 1981. Nonparametric Geostatistics. London: Applied Science Publishers.Search in Google Scholar

Huang, C., T. Hsing, and N. Cressie. 2011 Nonparametric Estimation of the Variogram and Its Spectrum.” Biometrika 98:775–89.Search in Google Scholar

Jenkins, H.E., R. Woodroffe, C.A. Donnelly, D.R. Cox, W.T. Johnston, F.J. Bourne, C.L. Cheeseman, R. Clifton-Hadley, and G. Gettinby. 2007. “Effects of Culling on Spatial Associations of Mycobacterium bovis Infections in Badgers and Cattle.” Journal of Applied Ecology 44:897–908.Search in Google Scholar

Kaneene, J.B., C.S. Bruning-Fann, L.M. Granger, R. Miller, and B.S. Porter-Spalding. 2002. “Environmental and Farm Management Factors Associated with Tuberculosis on Cattle Farms in Northeastern Michigan.” Journal of the American Veterinary Medical Association 221:837–42.Search in Google Scholar

Kelly, G.E. 2011. “Anisotropic Spatial Clustering of TB in Cattle – The Implications for Control Policy.” Procedia Environmental Sciences 3:111–6.Search in Google Scholar

Kelly, G.E. 2012. “Spatio-Temporal Modeling of TB in Cattle Herds.” Journal of Environmental Statistics 3(4):1–9.Search in Google Scholar

Kelly, G.E., and S.J. More. 2011. “Spatial Clustering of TB-Infected Cattle Herds Prior to and Following Proactive Badger Removal.” Epidemiology and Infection 139:1220–9.Search in Google Scholar

Kelly, G.E., G.E. McGrath, and S.J. More. 2010. “Estimating the Extent of Spatial Association of Mycobacterium bovis Infection in Badgers in Ireland.” Epidemiology and Infection 38:270–9.Search in Google Scholar

Kelly, G.E., J. Condon, S.J. More, L. Dolan, I. Higgins, and J. Eves. 2008. “A Long-Term Observational Study of the Impact of Badger Removal on Herd Restrictions due to Bovine TB in the Irish Midlands during 1989–2004.” Epidemiology and Infection 136:1362–73.Search in Google Scholar

Keohane, T., and J. McCarthy. 2009. “Tracking Badger Visits to Farmyards.” Veterinary Record 164:668.Search in Google Scholar

Kulldorff, M., and N. Nagarwalla. 1995. “Spatial Disease Cluster: Detection and Inference.” Statistics in Medicine 14:799–810.Search in Google Scholar

Laffan S.W., Z. Wang, and M.P. Ward. 2011. “The effect of neighbourhood definitions on spatio-temporal models of disease outbreaks: Separation distance versus range overlap.” Preventive Veterinary Medicine 102:218–229.Search in Google Scholar

Macdonald, D.W., P. Riordan, and F. Mathews. 2006. “Biological Hurdles to the Control of TB in Cattle: A Test of Two Hypotheses Concerning Wildlife to Explain the Failure of Control.” Biological Conservation 131:268–86.Search in Google Scholar

McGrath, G., D. Abernethy, L. Stringer, and S.J. More. 2009. “An All-Island Approach to Mapping Bovine Tuberculosis in Ireland.” Irish Veterinary Journal 62:192–7.Search in Google Scholar

O’Corry-Crowe, G., R. Hammond, J. Eves, and T.J. Hayden. 1996. “The Effect of Reduction in Badger Density on the Spatial Organization and Activity of Badgers Meles meles L. in Relation to Farms in Central Ireland.” Biology and Environment: Proceedings of the Royal Irish Academy 96B:147–58.Search in Google Scholar

O’Meara, D.B., C.J. Edwards, D.P. Sleeman, T.F. Cross, M.J. Statham, J.R. McDowell, E. Dillane, Coughlan, J.P., D. O’Leary, C. O’Reilly, D.G. Bradley, and J. Carlsson. 2012. “Genetic Structure of Eurasian Badgers Meles meles (Carnivora: Mustelidae) and the Colonization History of Ireland.” Biological Journal of the Linnean Society. doi:10.1111/j.1095–8312.2012.01927.Search in Google Scholar

Schabenberger, O., and C.A. Gotway. 2005. Statistical Methods for Spatial Data Analysis. Boca Raton, FL: Chapman and Hall/CRC, chapters 4,6,11.Search in Google Scholar

Self, S.G., and K.Y. Liang. 1987. “Asymptotic Properties of Maximum Likelihood Estimators and Likelihood Ratio Tests under Nonstandard Conditions.” Journal of the American Statistical Association 82:605–10.Search in Google Scholar

Sheridan, M. 2011. “Progress in Tuberculosis Eradication in Ireland.” Veterinary Microbiology 151:160–9.Search in Google Scholar

Sleeman, D., and M. Mulcahy. 1993. “Behaviour of Irish Badgers in Relation to Bovine Tuberculosis. In The Badger, edited by T.J. Hayden, 154–65. Dublin: Royal Irish Academy.Search in Google Scholar

Sleeman, D.P., and M.F. Mulcahy. 2005. “Loss of Territoriality in a Local Badger Meles meles Population at Kilmurry, Co Cork, Ireland.” Irish Naturalists’ Journal 28:11–9.Search in Google Scholar

Sleeman, D.P., J. Davenport, and A. Fitzgerald. 2008. “Incidence of Visits by Badgers to Farmyards in Ireland in Winter.” Veterinary Record 163:724.Search in Google Scholar

Sleeman, D.P., J. Davenport, S.J. More, T.A. Clegg, J.M. Griffin, and I. O’Boyle. 2009. The Effectiveness of Barriers to Badger Meles meles Immigration in the Irish Four Area Project.” European Journal of Wildlife Research 55:267–78.Search in Google Scholar

Stram, D.O., and J.W. Lee. 1994. “Variance Components Testing in the Longitudinal Mixed Effects Model.” Biometrics 50:1171–7Search in Google Scholar

Tolhurst, B.A., R.J. Delahay, N.J. Walker, A.I. Ward, and T.J. Roper. 2009. “Behaviour of Badgers (Meles meles) in Farm Buildings: Opportunities for Transmission of Mycobacterium bovis to Cattle.” Applied Animals Behavioural Science 117:103–13.Search in Google Scholar

Tuyttens, F.A.M., R.J. Delahay, D.W. Macdonald, C.L. Cheeseman, B. Long, and C.A. Donnelly. 2000. “Spatial Perturbation Caused by a Badger Meles meles Culling Operation: Implications for the Function of Territoriality and the Control of Bovine Tuberculosis Mycobacterium bovis.” Journal of Animal Ecology 69:815–28.Search in Google Scholar

Woodroffe, R., C.A. Donnelly, W.T. Johnston, F.J. Bourne, C.L. Cheeseman, R.S. Clifton-Hadley, D.R. Cox, G. Gettinby, R.G. Hewinson, A.M. Fevre, J.P. McInerney, and W.I. Morrison. 2005. “Spatial Association of Mycobacterium bovis Infection in Cattle and Badgers Meles meles.” Journal of Applied Ecology 42:852–62.Search in Google Scholar

Woodroffe, R., C.A. Donnelly, D.R. Cox, F.J. Bourne, C.L. Cheeseman, R.J. Delahay, G. Gettinby, J.P. McInerney, and W.I. Morrison. 2006. “Effects of Culling on Badger Meles meles Spatial Organization: Implications for the Control of Bovine Tuberculosis.” Journal of Applied Ecology 43:1–10.Search in Google Scholar

Published Online: 2013-06-05

©2013 by Walter de Gruyter Berlin / Boston