Impact of external sources of infection on the dynamics of bovine tuberculosis in modelled badger populations
The persistence of bovine TB (bTB) in various countries throughout the world is enhanced by the existence of wildlife hosts for the infection. In Britain and Ireland, the principal wildlife host for bTB is the badger (Meles meles). The objective of our study was to examine the dynamics of bTB in badgers in relation to both badger-derived infection from within the population and externally-derived, trickle-type, infection, such as could occur from other species or environmental sources, using a spatial stochastic simulation model.
The presence of external sources of infection can increase mean prevalence and reduce the threshold group size for disease persistence. Above the threshold equilibrium group size of 6–8 individuals predicted by the model for bTB persistence in badgers based on internal infection alone, external sources of infection have relatively little impact on the persistence or level of disease. However, within a critical range of group sizes just below this threshold level, external infection becomes much more important in determining disease dynamics. Within this critical range, external infection increases the ratio of intra- to inter-group infections due to the greater probability of external infections entering fully-susceptible groups. The effect is to enable bTB persistence and increase bTB prevalence in badger populations which would not be able to maintain bTB based on internal infection alone.
External sources of bTB infection can contribute to the persistence of bTB in badger populations. In high-density badger populations, internal badger-derived infections occur at a sufficient rate that the additional effect of external sources in exacerbating disease is minimal. However, in lower-density populations, external sources of infection are much more important in enhancing bTB prevalence and persistence. In such circumstances, it is particularly important that control strategies to reduce bTB in badgers include efforts to minimise such external sources of infection.
- Cleaveland S, Laurenson MK, Taylor LH: Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Phil Trans R Soc Lond B 2001, 356:991–999. CrossRef
- Daszak P, Tabour GM, Epstein J, Plowright R: Conservation medicine and a new agenda for emerging diseases. Annals New York Acad Sci 2004, 1026:1–11. CrossRef
- Gortazar C, Ferroglio E, Hofle U, Frolich K, Vicente J: Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 2007, 53:241–256. CrossRef
- Delahay RJ, Cheeseman CL, Clifton-Hadley RS: Wildlife disease reservoirs: the epidemiology of Mycobacterium bovis infection in the European badger (Meles meles) and other British mammals. Tuberculosis 2001, 81:43–49. CrossRef
- European Food Safety Authority: The community summary report on trends and sources of zoonoses and zoonotic agents in the European Union in 2007. The EFSA Journal 2009. http://www.efsa.europa.eu/de/scdocs/doc/223r.pdf
- Krebs JR, Anderson RM, Clutton-Brock T, Donnelly CA, Frost S, Morrison WI, Woodroffe R, Young D: Badgers and bovine TB: Conflicts between conservation and health. Science 1998, 279:817–818. CrossRef
- Da Silva J, Woodroffe R, Macdonald DW: Habitat, food availability and group territoriality in the European badger, Meles meles. Oecologia 1993, 95:558–564.
- Palphramand KL, Newton-Cross G, White PCL: Spatial organization and behavior of badgers (Meles meles) in a moderate-density population. Behav Ecol Sociobiol 2007, 61:401–413. CrossRef
- Delahay RJ, Langton S, Smith GC, Cheeseman CL: The spatio-temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high-density badger population. J Anim Ecol 2000, 69:428–441. CrossRef
- Rogers LM, Cheeseman CL, Mallinson PJ, Clifton-Hadley R: The demography of a high-density badger (Meles meles) population in the southwest of England. J Zool 1997, 242:705–728. CrossRef
- Revilla E, Palomares F: Spatial organization, group living and ecological correlates in low-density populations of Eurasian badgers, Meles meles. J Anim Ecol 2002, 71:497–512. CrossRef
- Kowalczyk R, Zalewski A, Jedrzejewska B, Jedrzejewski W: Spatial organization and demography of badgers (Meles meles) in Bialowieza Primeval Forest, Poland, and the influence of earthworms on badger densities in Europe. Can J Zool 2003, 81:74–87. CrossRef
- Rosalino LM, Macdonald DW, Santos-Reis M: Spatial structure and land-cover use in a low-density Mediterranean population of Eurasian badgers. Can J Zool 2004, 82:1493–1502. CrossRef
- Smith GC, Richards MS, Clifton-Hadley RS, Cheeseman CL: Modelling bovine tuberculosis in badgers in England: Preliminary results. Mammalia 1995, 59:639–650.
- White PCL, Harris S: Bovine tuberculosis in badger (Meles meles) populations in south-west England: the use of a spatial stochastic simulation model to understand the dynamics of the disease. Phil Trans R Soc Lond B 1995, 349:391–413. CrossRef
- Smith GC, Cheeseman CL, Clifton-Hadley RS: Modelling the control of bovine tuberculosis in badgers in England: culling and the release of lactating females. J Appl Ecol 1997, 34:1375–1386. CrossRef
- Sleeman DP, Davenport J, More SJ, Clegg TA, Collins JD, Martin SW, Williams DH, Griffin JM, O’Boyle I: How many Eurasian badgers Meles meles L. are there in the Republic of Ireland. Eur J Wildl Res 2009, 55:333–334. CrossRef
- Olea-Popelka FJ, Griffin JM, Collins JD, McGrath G, Martin SW: Bovine tuberculosis in badgers in four areas in Ireland: does tuberculosis cluster? Prev Vet Med 2003, 59:103–111. CrossRef
- Hutchings MR, White PCL: Mustelid scent-marking in managed ecosystems: implications for population management. Mammal Rev 2000, 30:157–169. CrossRef
- Almberg ES, Cross PC, Smith DW: Persistence of canine distemper virus in the Greater Yellowstone Ecosystem’s carnivore community. Ecol Appl 2010, 20:2058–2074. CrossRef
- Salkeld DJ, Salathe M, Stapp P, Holland-Jones J: Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance. PNAS 2010, 107:14247–14250. CrossRef
- Nugent G: Maintenance, spillover and spillback transmission of bovine tuberculosis in multi-host complexes: A New Zealand case study. Vet Microbiol 2011, 151:34–42. CrossRef
- Côté IM, Poulin R: Parasitism and group size in social animals – a meta-analysis. Behav Ecol 1995, 6:159–165. CrossRef
- Woodroffe R, Donnelly CA, Wei G, Cox DR, Bourne FJ, Burke T, Butlin RK, Cheeseman CL, Gettinby G, Gilks P, Hedges S, Jenkins HE, Johnston WT, McInerney JP, Morrison WI, Pope LC: Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). J Anim Ecol 2009, 78:818–827. CrossRef
- Böhm M, Hutchings MR, White PCL: Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle. PLoS One 2009,4(4):e5016. CrossRef
- Cohen T, Colijn C, Finklea B, Murray M: Exogenous re-infection and the dynamics of tuberculosis epidemics: local effects in a network model of transmission. J R Soc Interface 2007, 4:523–531. CrossRef
- Martin-Atance P, Leon-Vizcaino L, Palomares F, Revilla E, Gonzalez-Candela M, Calzada J, Cubero-Pablo MJ, Delibes M: Antibodies to Mycobacterium bovis in wild carnivores from Donana national park (Spain). J Wildl Dis 2006, 42:704–708.
- Lugton IW, Wilson PR, Morris RS, Nugent G: Epidemiology and pathogenesis of Mycobacterium bovis infection of red deer (Cervus elaphus) in New Zealand. New Zeal Vet J 1998, 46:147–156. CrossRef
- McCorry T, Whelan AO, Welsh MD, McNair J, Walton E, Bryson DG, Hewinson RG, Vordermeier HM, Pollock JM: Shedding of Mycobacterium bovis in the nasal mucus of cattle infected experimentally with tuberculosis by the intranasal and intratracheal routes. Vet Rec 2005, 157:613–618.
- Michel AL, De Klerk L, Van Pittius NC, Warren RM, Van Helden PD: Bovine tuberculosis in African buffaloes: observations regarding Mycobacterium bovis shedding into water and exposure to environmental mycobacteria. BMC Vet Res 2007, 3:23–30. CrossRef
- Cheeseman CL, Wilesmith JW, Stuart FA: Tuberculosis: the disease and its epidemiology in the badger, a review. Epidemiol Inf 1989, 103:113–125. CrossRef
- Ward AI, Smith GC: Predicting the status of wild deer as hosts of Mycobacterium bovis infection in Britain. Eur J Wildl Res 2012, 58:127–135. CrossRef
- Delahay RJ, Smith GC, Barlow AM, Walker N, Harris A, Clifton-Hadley RS, Cheeseman CL: 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 2007, 173:287–301. CrossRef
- Ward AI, Smith GC, Etherington TR, Delahay RJ: Estimating the risk of cattle exposure to tuberculosis posed by wild deer relative to badgers in England and Wales. J Wildl Dis 2009, 45:1104–1120.
- Garnett BT, Delahay RJ, Roper TJ: Ranging behaviour of European badgers (Meles meles) in relation to bovine tuberculosis (Mycobacterium bovis) infection. Appl Anim Behav Sci 2005, 94:331–340. CrossRef
- Chapman N, Claydon K, Claydon M, Forde PG, Harris S: Sympatric populations of muntjac (Muntiacus reevesi) and Roe deer (Capreolus capreolus): a comparative analysis of their ranging behaviour, social aggregation and activity. J Zool 1993, 229:623–640. CrossRef
- Palmer MV, Whipple DL: Survival of Mycobacterium bovis on feedstuffs commonly used as supplemental feed for white-tailed deer (Odocoileus virginianus). J Wildl Dis 2006, 42:853–858.
- Witmer G, Fine AE, Gionfriddo J, Pipas M, Shively K, Piccolo K, Burke P: Epizootiologic survey of Mycobacterium bovis in wildlife and farm environments in Northern Michigan. J Wildl Dis 2010, 46:368–378.
- Sweeney FP, Courtenay O, Hibberd V, Reilly LA, Wellington EMH: Immunomagnetic recovery of Mycobacterium bovis from naturally infected environmental samples. Lett Appl Microbiol 2006, 43:364–369. CrossRef
- Sweeney FP, Courtenay O, Hibberd V, Hewinson RG, Reilly LA, Gaze WH, Wellington EMH: Environmental monitoring of Mycobacterium bovis in badger faeces and badger sett soil by real-time PCR, as confirmed by immunofluorescence, immunocapture and cultivation. Appl Env Microbiol 2007, 73:7471–7473. CrossRef
- Young JS, Gormley E, Wellington EMH: Molecular detection of Mycobacterium bovis and Mycobacterium bovis BCG (Pasteur) in soil. Applied and Environmental Mircrobiology 2005, 71:1946–1952. CrossRef
- Jackson R, De Lisle GW, Morris RS: A study of the environmental survival of Mycobacterium bovis on a farm in New Zealand. New Zeal Vet J 1995, 43:346–352. CrossRef
- Zanella G, Durand B, Hars J, Moutou F, Garin-Bastuli B, Duvauchelle A, Ferme M, Karoui C, Boschiroli ML: Premier foyer de tuberculose a M. bovis dans une population de cerfs et de sangliers sauvages en France. Bull Epidemiol 2008, 29:1–5.
- Young JS, Gormley E, Wellington EMH: Molecular detection of Mycobacterium bovis and Mycobacterium bovis BGC (Pasteur) in soil. Appl Environ Microbiol 2005, 71:1936–1952. CrossRef
- Sweeney FP, Courtenay O, Ul-Hassan A, Hibberd V, Reilly LA, Wellington EMH: Immunomagnetic recovery of Mycobacterium bovis from naturally infected environmental sample. Lett Appl Microbiol 2006, 43:364–369. CrossRef
- Donnelly CA, Woodroffe R, Cox DR, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Wei G, Gettinby G, Gilks P, Jenkins H, Johnston WT, Le Fevre AM, McInerney JP, Morrison WI: Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 2006, 439:843–846. CrossRef
- Mairtin DO, Williams DH, Griffin JM, Dolan LA, Eves JA: The effect of a badger removal programme on the incidence of tuberculosis in an Irish cattle population. Prev Vet Med 1998, 34:47–56. CrossRef
- Donnelly CA, Woodroffe R, Cox DR, Bourne FJ, Gettinby G, Le Fevre AM, McInerney JP, Morrison WI: Impact of localised badger culling on tuberculosis incidence in British cattle. Nature 2003, 426:834–837. CrossRef
- Jenkins HE, Woodroffe R, Donnelly CA, Cox DR, Johnston WT, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Gettinby G, Gilks P, Hewinson RG, McInerney JP, Morrison WI: Effects of culling on spatial associations of Mycobacterium bovis infections in badgers and cattle. J Appl Ecol 2007, 44:897–908. CrossRef
- White PCL, Benhin J: Factors influencing the incidence and scale of bovine tuberculosis in cattle in Southwest England. Prev Vet Med 2004, 63:1–7. CrossRef
- 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: Culling and cattle controls influence tuberculosis risk for badgers. Proc Natl Acad Sci 2006, 103:14713–14717. CrossRef
- Clegg TA, More SJ, Higgins IM, Good M, Blake M, Williams DH: Potential infection-control benefit for Ireland from pre-movement testing of cattle for tuberculosis. Prev Vet Med 2008, 84:91–11. CrossRef
- Tolhurst BA, Delahay RJ, Walker NJ, Ward AI, Roper TJ: Behaviour of badgers (Meles meles) in farm buildings: Opportunities for the transmission of Mycobacterium bovis to cattle? Appl Anim Behav Sci 2009, 117:103–113. CrossRef
- Wilkinson D, Smith GC, Delahay RJ, Cheeseman CL: A model of bovine tuberculosis in the badger Meles meles: an evaluation of different vaccination strategies. J Appl Ecol 2009, 41:492–501. CrossRef
- Woodroffe R, Macdonald DW, da Silva J: Dispersal and philopatry in the European badger, Meles meles. J Zool 1995, 237:227–239. CrossRef
- Cresswell WJ, Harris S, Cheeseman CL, Mallinson PJ: To breed or not to breed: an analysis of the social and density-dependent constraints on the fecundity of female badgers (Meles meles). Phil Trans R Soc Lond B 1992, 338:393–407. CrossRef
- Wilkinson D, Smith GC, Delahay RJ, Rogers LM, Cheeseman CL, Clifton-Hadley RS: The effects of bovine tuberculosis (Mycobacterium bovis) on mortality in a badger (Meles meles) population in England. J Zool 2000, 250:389–395. CrossRef
- Impact of external sources of infection on the dynamics of bovine tuberculosis in modelled badger populations
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BMC Veterinary Research
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- June 2012
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- 1. Environment Department, University of York, York, YO10 5DD, UK
- 4. Biological Sciences, University of Derby, Kedleston Road, Derby, DE22 1 GB, UK
- 2. Biomathematics and Statistics Scotland, James Clerk Maxwell Building, Kings Buildings, Edinburgh, EH9 3HH, UK
- 3. Disease Systems, Scottish Agricultural College, West Mains Road, Edinburgh, EH9 3JG, UK