Skip to main content

Advertisement

SpringerLink
Log in

Coupling models of cattle and farms with models of badgers for predicting the dynamics of bovine tuberculosis (TB)

  • Original Paper
  • Published:
Stochastic Environmental Research and Risk Assessment Aims and scope Submit manuscript

Abstract

Bovine Tuberculosis (TB) is a major problem for the agricultural industry in several countries. TB can be contracted and spread by species other than cattle and this can cause a problem for disease control. In the UK and Ireland, badgers are a recognised reservoir of infection and there has been substantial discussion about potential control strategies. We present a coupling of individual based models of bovine TB in badgers and cattle, which aims to capture the key details of the natural history of the disease and of both species at approximately county scale. The model is spatially explicit it follows a very large number of cattle and badgers on a different grid size for each species and includes also winter housing. We show that the model can replicate the reported dynamics of both cattle and badger populations as well as the increasing prevalence of the disease in cattle. Parameter space used as input in simulations was swept out using Latin hypercube sampling and sensitivity analysis to model outputs was conducted using mixed effect models. By exploring a large and computationally intensive parameter space we show that of the available control strategies it is the frequency of TB testing and whether or not winter housing is practised that have the most significant effects on the number of infected cattle, with the effect of winter housing becoming stronger as farm size increases. Whether badgers were culled or not explained about 5 %, while the accuracy of the test employed to detect infected cattle explained less than 3 % of the variance in the number of infected cattle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • AHVLA (2013) Pre-movement and post-movement testing of cattle in Great Britain. Animal Health and Veterinary Laboratory Agencies, Weybridge

    Google Scholar 

  • Benham PFJ, Broom DM (1991) Responses of dairy cows to badger urine and faeces on pasture with reference to bovine tuberculosis transmission. Br Vet J 147:517–532

    Article  CAS  Google Scholar 

  • Biek R, O’Hare A, Wright D, Mallon T, McCormick C, Orton RJ, McDowell S, Trewby H, Skuce RA, Kao RR (2012) Whole genome sequencing reveals local transmission patterns of Mycobacterium bovis in sympatric cattle and badgers. PLoS Pathog 8:e1003008

    Article  CAS  Google Scholar 

  • Bielby J, Donnelly CA, Pope LC, Burke T, Woodroffe R (2014) Badger responses to small-scale culling may compromise targeted control of bovine tuberculosis. Proc Natl Acad Sci USA 111:9193–9198

    Article  CAS  Google Scholar 

  • Bithell M, Brasington J (2009) Coupling agent-based models of subsistence farming with individual-based forest models and dynamic models of water distribution. Environ Model Softw 24:173–190

    Article  Google Scholar 

  • Bithell M, Macmillan WD (2007) Escape from the cell: spatially explicit modelling with and without grids. Ecol Model 200:59–78

    Article  Google Scholar 

  • Bourne J, Donnelly CA, Cox DR, Gettinby G, McInerney JP, Morrison WI, Woodroffe R (2007) Bovine TB: the scientific evidence. DEFRA, London, p 289

    Google Scholar 

  • Brennan ML, Christley RM (2012) Biosecurity on cattle farms: a study in north-west England. PLoS One 7:e28139

    Article  CAS  Google Scholar 

  • Byrne AW, O’Keeffe J, Green S, Sleeman DP, Corner LAL, Gormley E, Murphy D, Martin SW, Davenport J (2012) Population estimation and trappability of the European badger (Meles meles): implications for tuberculosis management. PLoS One 7:e50807

    Article  CAS  Google Scholar 

  • Cheeseman CL, Jones GW, Gallagher J, Mallinson PJ (1981) The Population structure, density and prevalence of tuberculosis (Mycobacterium bovis) in Badgers (Meles meles) from Four Areas in South-West England. J Appl Ecol 18:795–804

    Article  Google Scholar 

  • Cheeseman CL, Cresswell WJ, Harris S, Mallinson PJ (1988) Comparison of dispersal and other movements in two Badger (Meles meles) populations. Mamm Rev 18:51–59

    Article  Google Scholar 

  • Christakos G, Hristopulos DT (1998) Spatiotemporal environmental health modelling: a tractatus stochasticus. Springer, New York

    Book  Google Scholar 

  • Claridge J, Diggle P, McCann CM, Mulcahy G, Flynn R, McNair J, Strain S, Welsh M, Baylis M, Williams DJL (2012) Fasciola hepatica is associated with the failure to detect bovine tuberculosis in dairy cattle. Nat Commun 3:853

    Article  Google Scholar 

  • Conlan AJK, McKinley TJ, Karolemeas K, Pollock EB, Goodchild AV, Mitchell AP, Birch CPD, Clifton-Hadley RS, Wood JLN (2012) Estimating the hidden burden of bovine tuberculosis in Great Britain. PLoS Comput Biol 8:e1002730

    Article  CAS  Google Scholar 

  • Costello E, Doherty ML, Monaghan ML, Quigley FC, O’Reilly PF (1998) A study of cattle-to-cattle transmission of Mycobacterium bovis infection. Vet J 155:245–250

    Article  CAS  Google Scholar 

  • DEFRA (2009) Bovine tuberculosis in England: Towards eradication. Final Report of the Bovine TB Advisory Group, London

    Google Scholar 

  • DEFRA (2011) The Government’s policy on Bovine TB and badger control in England. DEFRA, London

    Google Scholar 

  • DEFRA (2014a) Annex: background and methodologies to the National Statistics on the Incidence of Tuberculosis (TB) in cattle in Great Britain, Latest statistics on the incidence of tuberculosis (TB) in cattle in Great Britain

  • DEFRA (2014b) Incidence of TB in cattle in Great Britain—GB dataset. https://www.gov.uk/government/publications/incidence-of-tuberculosis-tb-in-cattle-in-great-britain. Accessed 10 Apr 2014

  • DEFRA (2014c) Monthly publication of National Statistics on the Incidence of Tuberculosis (TB) in cattle to end June 2014 for Great Britain

  • Delahay RJ, Langton S, Smith GC, Clifton-Hadley RS, Cheeseman CL (2000) The spatio-temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high-density badger population. J Anim Ecol 69:428–441

    Article  Google Scholar 

  • Eurostat (2009) Farm structure survey in the United Kingdom—2007 statistics in focus. http://epp.eurostat.ec.europa.eu/cache/ITY_OFFPUB/KS-SF-09-081/EN/KS-SF-09-081-EN.PDF

  • Evans MR, Bithell M, Cornell SJ, Dall SRX, Díaz S, Emmott S, Ernande B, Grimm V, Hodgson DJ, Lewis SL, Mace GM, Morecroft M, Moustakas A, Murphy E, Newbold T, Norris KJ, Petchey O, Smith M, Travis JMJ, Benton TG (2013a) Predictive systems ecology. Proc R Soc B, Biological Sciences. doi:10.1098/rspb.2013.1452

    Google Scholar 

  • Evans MR, Grimm V, Johst K, Knuuttila T, de Langhe R, Lessells CM, Merz M, O Malley MA, Orzack SH, Weisberg M, Wilkinson DJ, Wolkenhauer O, Benton TG (2013b) Do simple models lead to generality in ecology? Trends Ecol Evol 28:578–583

    Article  Google Scholar 

  • Evans MR, Benton TG, Grimm V, Lessells CM, O’Malley MA, Moustakas A, Weisberg M (2014) Data availability and model complexity, generality, and utility: a reply to Lonergan. Trends Ecol Evol 29:302–303

    Article  Google Scholar 

  • Gibbens N (2009) Progress through partnership: The UK Chief Veterinary Officer’s 2009 report on animal health and welfare. Department for Environment Food and Rural Affairs, London

    Google Scholar 

  • Gilbert M, Mitchell A, Bourn D, Mawdsley J, Clifton-Hadley RS, Wint W (2005) Cattle movements and bovine tuberculosis in Great Britain. Nature 435:491–496

    Article  CAS  Google Scholar 

  • Godfray HCJ, Curnow RN, Dye C, Pfeiffer D, Sutherland WJ, Woolhouse MEJ (2004) Independent scientific review of the randomised badger culling trial and associated epidemiological research. Department for Environment, Food and Rural Affairs, London

    Google Scholar 

  • Godfray HCJ, Donnelly CA, Kao RR, Macdonald DW, McDonald RA, Petrokofsky G, Wood JLN, Woodroffe R, Young DB, McLean AR (2013) A restatement of the natural science evidence base relevant to the control of bovine tuberculosis in Great Britain†. Proc R Soc B 280:20131634

    Article  Google Scholar 

  • Goodchild AV, Clifton-Hadley RS (2001) Cattle-to-cattle transmission of Mycobacterium bovis. Tuberculosis 81:23–41

    Article  CAS  Google Scholar 

  • Goodchild AV, Watkins GH, Sayers AR, Jones JR, Clifton-Hadley RS (2012) Geographical association between the genotype of bovine tuberculosis in found dead badgers and in cattle herds. Vet Rec 170:259

    Article  CAS  Google Scholar 

  • Green DM, Kiss IZ, Mitchell AP, Kao RR (2008) Estimates for local and movement-based transmission of bovine tuberculosis in British cattle. Proc R Soc B 275:1001–1005

    Article  Google Scholar 

  • Harris S, Yalden D (2008) Mammals of the British Isles, 4th edn. Mammal Society, London

    Google Scholar 

  • Jenkins HE, Woodroffe R, Donnelly CA (2010) The duration of the effects of repeated widespread badger culling on cattle tuberculosis following cessation of culling. PLoS One 5:e9090

    Article  Google Scholar 

  • Jenkins HE, Cox DR, Delahay RJ (2012) Direction of association between bite wounds and Mycobacterium bovis Infection in badgers: implications for transmission. PLoS ONE 7:e45584

    Article  CAS  Google Scholar 

  • Kao RR, Gravenor MB, Charleston B, Hope JC, Martin M, Howard CJ (2007) Mycobacterium bovis shedding patterns from experimentally infected calves and the effect of concurrent infection with bovine viral diarrhoea virus. J R Soc Interface 4:545–551

    Article  CAS  Google Scholar 

  • Karolemeas K, Donnelly CA, Conlan AJK, Mitchell AP, Clifton-Hadley RS, Upton P, Wood JLN, McKinley TJ (2012) The effect of badger culling on breakdown prolongation and recurrence of bovine tuberculosis in cattle herds in Great Britain. PLoS ONE 7:e51342

    Article  CAS  Google Scholar 

  • King D, Roper TJ, Young D, Woolhouse MEJ, Collins DA, Wood P (2007) Tuberculosis in cattle and badgers: a report by the Chief Scientific Advisor. Sir David King, London

    Google Scholar 

  • Krebs JR, Anderson R, Clutton-Brock T, Morrison I, Young D, Donnelly CA, Frost S, Woodroffe R (1997) Bovine tuberculosis in cattle and badgers. Ministry of Agriculture, Fisheries and Food, London, p 191

    Google Scholar 

  • Kruuk H, Parish T (1982) Factors affecting population density, group size and territory size of the European badger, Meles meles. J Zool 196:31–39

    Article  Google Scholar 

  • Lin C-H, Wen T-H, Teng H-J, Chang N-T (2014) The spatio-temporal characteristics of potential dengue risk assessed by Aedes aegypti and Aedes albopictus in high-epidemic areas. Stoch Environ Res Risk Assess. doi:10.1007/s00477-014-0940-1

    Google Scholar 

  • Little T, Naylor P, Wilesmith J (1982) Laboratory study of Mycobacterium bovis infection in badgers and calves. Vet Rec 111:550–557

    CAS  Google Scholar 

  • Marrel A, Perot N, Mottet C (2014) Development of a surrogate model and sensitivity analysis for spatio-temporal numerical simulators. Stoch Environ Res Risk Assess. doi:10.1007/s00477-014-0927-y

    Google Scholar 

  • Matsinos YG, Wolff WF, Moustakas A (2011) Adapting foraging to habitat heterogeneity and climate change: an individual-based model for wading birds. Ethology Ecology & Evolution 24:209–229

    Article  Google Scholar 

  • McKay MD, Beckman RJ, Conover WJ (1979) Comparison of three methods for selecting values of input variables in the analysis of output from a computer code. Technometrics 21:239–245

    Google Scholar 

  • Meyer KM, Wiegand K, Ward D, Moustakas A (2007) SATCHMO: a spatial simulation model of growth, competition, and mortality in cycling savanna patches. Ecol Model 209:377–391

    Article  Google Scholar 

  • Millington JDA, Demeritt D, Romero-Calcerrada R (2011) Participatory evaluation of agent-based land-use models. J Land Use Sci 6:195–210

    Article  Google Scholar 

  • Moustakas A, Evans MR (2013) Integrating evolution into ecological modelling: accommodating phenotypic changes in agent based models. PLoS ONE 8:e71125

    Article  CAS  Google Scholar 

  • Moustakas A, Silvert W (2011) Spatial and temporal effects on the efficacy of marine protected areas: implications from an individual based model. Stoch Environ Res Risk Assess 25:403–413

    Article  Google Scholar 

  • Neal EG, Harbison R (1958) Reproduction in the European badger (Meles meles L.). Trans Zool Soc Lond 29:67–130

    Article  Google Scholar 

  • NSF (2010) Dairy Cow Welfare Strategy. http://www.eblex.org.uk/wp/wpcontent/uploads/2013/06/Dairy-cow-welfare-report-2010.pdf

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-plus. Springer, New York

    Book  Google Scholar 

  • Riordan P, Delahay RJ, Cheeseman C, Johnson PJ, Macdonald DW (2011) Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis. PLoS One 6:e28904

    Article  CAS  Google Scholar 

  • Rogers L, Delahay R, Cheeseman C, Langton S, Smith G, Clifton-Hadley R (1998) Movement of badgers (Meles meles) in a high–density population: individual, population and disease effects. Proc R Soc Lond B 265:1269–1276

    Article  CAS  Google Scholar 

  • Roper TJ, Lüps P (1993) Disruption of territorial behaviour in badgers Meles meles. Zeitschrift fur Saugetierkunde 58:252–255

    Google Scholar 

  • Roper TJ, Ostler JR, Conradt L (2003) The process of dispersal in badgers Meles meles. Mamm Rev 33:314–318

    Article  Google Scholar 

  • Shirley MDF, Rushton SP, Smith GC, South AB, Lurz PWW (2003) Investigating the spatial dynamics of bovine tuberculosis in badger populations: evaluating an individual-based simulation model. Ecol Model 167:139–157

    Article  Google Scholar 

  • Sleeman D (1992) Long-distance movements in an Irish badger population. In: Priede IG, Swift SM (eds) Wildlife telemetry. Wiley, London, pp 670–676

    Google Scholar 

  • Smith GC, Cheeseman CL (2002) A mathematical model for the control of diseases in wildlife populations: culling, vaccination and fertility control. Ecol Model 150:45–53

    Article  Google Scholar 

  • Smith GC, Cheeseman CL, Wilkinson D, Clifton-Hadley RS (2001) A model of bovine tuberculosis in the badger Meles meles: the inclusion of cattle and the use of a live test. J Appl Ecol 38:520–535

    Article  Google Scholar 

  • Smith GC, McDonald RA, Wilkinson D (2012) Comparing badger (Meles meles) management strategies for reducing tuberculosis incidence in cattle. PLoS ONE 7:e39250

    Article  CAS  Google Scholar 

  • Szmaragd C, Green LE, Medley GF, Browne WJ (2012) Impact of imperfect test sensitivity on determining risk factors: the case of bovine tuberculosis. PLoS One 7:e43116

    Article  CAS  Google Scholar 

  • Thibier M, Wagner HG (2002) World statistics for artificial insemination in cattle. Livest Prod Sci 74:203–212

    Article  Google Scholar 

  • Tolhurst BA, Delahay RJ, Walker NJ, Ward AI, Roper TJ (2009) Behaviour of badgers (Meles meles) in farm buildings: opportunities for the transmission of Mycobacterium bovis to cattle? Appl Anim Behav Sci 117:103–113

    Article  Google Scholar 

  • Verdin A, Rajagopalan B, Kleiber W, Katz R (2014) Coupled stochastic weather generation using spatial and generalized linear models. Stoch Environ Res Risk Assess. doi:10.1007/s00477-014-0911-6

    Google Scholar 

  • Welch BL (1947) The generalisation of student’s problems when several different population variances are involved. Biometrika 34:28–35

    CAS  Google Scholar 

  • Wilkinson D, Smith GC, Delahay RJ, Cheeseman CL (2004) A model of bovine tuberculosis in the badger Meles meles: an evaluation of different vaccination strategies. J Appl Ecol 41:492–501

    Article  Google Scholar 

  • Wilkinson D, Bennett R, McFarlane I, Rushton S, Shirley M, Smith GC (2009) Cost-benefit analysis model of badger (Meles meles) culling ot reduce cattle herd tuberculosis breakdowns, with particular reference to badger perturbation. J Wildl Dis 45:1062–1088

    Article  CAS  Google Scholar 

  • Wilson G, Harris S, McLaren G (1997) Changes in the British Badger Population, 1988 to 1997. People’s Trust for Endangered Species, London

    Google Scholar 

  • Woodroffe R, Donnelly CA, Johnston WT, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Cox DR, Gettinby G, Hewinson RG, Fevre AML, McInerney JP, Morrison WI (2005) Spatial association of Mycobacterium bovis infection in cattle and badgers Meles meles. J Appl Ecol 42:852–862

    Article  Google Scholar 

  • Woodroffe R, Donnelly CA, Cox DR, Bourne FJ, Cheeseman CL, Delahay RJ, Gettinby G, McInerney JP, Morrison WI (2006a) Effects of culling on badger Meles meles spatial organisation: implications for the control of bovine tuberculosis. J Appl Ecol 43:1–10

    Article  Google Scholar 

  • Woodroffe R, Donnelly CA, Jenkins HE, Johnston WT, Cox DR, Bourne FJ, Cheeseman CL, Delahay RJ, Clifton-Hadley RS, Gettinby G, Gilks P, Hewinson RG, McInerney JP, Morrison WI (2006b) Culling and cattle controls influence tuberculosis risk for badgers. Proc Natl Acad Sci 103:14713–14717

    Article  CAS  Google Scholar 

  • Zhang H, Jin X, Wang L, Zhou Y, Shu B (2014) Multi-agent based modeling of spatiotemporal dynamical urban growth in developing countries: simulating future scenarios of Lianyungang city, China. Stoch Environ Res Risk Assess 29:63–78

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Ian Boyd for comments on an earlier draft, and William Wint for providing us data on cattle movement. We also thank Harry Constantinides for invaluable help during model coding in C#. Comments from two anonymous reviewers considerably improved an earlier manuscript draft.

Author information

Authors and Affiliations

  1. School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK

    Aristides Moustakas & Matthew R. Evans

Authors
  1. Aristides Moustakas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew R. Evans
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aristides Moustakas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 22 kb)

Supplementary material 2 (DOCX 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moustakas, A., Evans, M.R. Coupling models of cattle and farms with models of badgers for predicting the dynamics of bovine tuberculosis (TB). Stoch Environ Res Risk Assess 29, 623–635 (2015). https://doi.org/10.1007/s00477-014-1016-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00477-014-1016-y

Keywords

Search

Navigation