Abstract
Bovine tuberculosis (TB) poses a serious threat for agricultural industry in several countries, it involves potential interactions between wildlife and cattle and creates societal problems in terms of human-wildlife conflict. This study addresses connectedness network analysis, the spatial, and temporal dynamics of TB between cattle in farms and the European badger (Meles meles) using a large dataset generated by a calibrated agent based model. Results showed that infected network connectedness was lower in badgers than in cattle. The contribution of an infected individual to the mean distance of disease spread over time was considerably lower for badger than cattle; badgers mainly spread the disease locally while cattle infected both locally and across longer distances. The majority of badger-induced infections occurred when individual badgers leave their home sett, and this was positively correlated with badger population growth rates. Point pattern analysis indicated aggregation in the spatial pattern of TB prevalence in badger setts across all scales. The spatial distribution of farms that were not TB free was aggregated at different scales than the spatial distribution of infected badgers and became random at larger scales. The spatial cross correlation between infected badger setts and infected farms revealed that generally infected setts and farms do not coexist except at few scales. Temporal autocorrelation detected a two year infection cycle for badgers, while there was both within the year and longer cycles for infected cattle. Temporal cross correlation indicated that infection cycles in badgers and cattle are negatively correlated. The implications of these results for understanding the dynamics of the disease are discussed.
Similar content being viewed by others
References
Abernethy D, Upton P, Higgins I, McGrath G, Goodchild A, Rolfe S, Broughan J, Downs S, Clifton-Hadley R, Menzies F (2013) Bovine tuberculosis trends in the UK and the Republic of Ireland, 1995–2010. Vet Rec 172:312
Alvarez J, Goede D, Morrison R, Perez A (2016) Spatial and temporal epidemiology of porcine epidemic diarrhea (PED) in the Midwest and Southeast regions of the United States. Prev Vet Med 123:155–160
Athira P, Sudheer K (2015) A method to reduce the computational requirement while assessing uncertainty of complex hydrological models. Stoch Env Res Risk Assess 29:847–859
Augustijn EW, Doldersum T, Useya J, Augustijn D (in press) Agent-based modelling of cholera diffusion. Stoch Environ Res Risk Assess. doi: 10.1007/s00477-015-1199-x
Besag J (1977) Contribution to the discussion of Dr. Ripley’s paper. J R Stat Soc B 39:193–195
BjØrnstad ON, Falck W (2001) Nonparametric spatial covariance functions: estimation and testing. Environ Ecol Stat 8:53–70
Böhm M, Hutchings MR, White PCL (2009) Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle. PLoS One 4:e5016
Bourne J, Donnelly CA, Cox DR, Gettinby G, McInerney JP, Morrison WI, Woodroffe R (2007) Bovine TB: the scientific evidence. DEFRA, London, p 289
Brooks-Pollock E, Roberts GO, Keeling MJ (2014) A dynamic model of bovine tuberculosis spread and control in Great Britain. Nature 511:228–231
Brunton LA, Nicholson R, Ashton A, Alexander N, Wint W, Enticott G, Ward K, Broughan JM, Goodchild AV (2015) A novel approach to mapping and calculating the rate of spread of endemic bovine tuberculosis in England and Wales. Spat Spat Temp Epidemiol 13:41–50
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
Byrne AW, Acevedo P, Green S, O’Keeffe J (2014a) Estimating badger social-group abundance in the Republic of Ireland using cross-validated species distribution modelling. Ecol Ind 43:94–102
Byrne AW, Quinn JL, O’Keeffe JJ, Green S, Paddy Sleeman D, Wayne Martin S, Davenport J (2014b) Large-scale movements in European badgers: has the tail of the movement kernel been underestimated? J Anim Ecol 83:991–1001
Byrne AW, Kenny K, Fogarty U, O’Keeffe JJ, More SJ, McGrath G, Teeling M, Martin SW, Dohoo IR (2015) Spatial and temporal analyses of metrics of tuberculosis infection in badgers (Meles meles) from the Republic of Ireland: trends in apparent prevalence. Prev Vet Med 122:345–354
Caplan P (2012) Cull or vaccinate?: badger politics in Wales (respond to this article at http://www.therai.org.uk/at/debate). Anthropol Today 28:17–21
Carter SP, Delahay RJ, Smith GC, Macdonald DW, Riordan P, Etherington TR, Pimley ER, Walker NJ, Cheeseman CL (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 R Soc B 274:2769–2777
Carter SP, Chambers MA, Rushton SP, Shirley MDF, Schuchert P, Pietravalle S, Murray A, Rogers F, Gettinby G, Smith GC, Delahay RJ, Hewinson RG, McDonald RA (2012) BCG vaccination reduces risk of tuberculosis infection in vaccinated badgers and unvaccinated badger cubs. PLoS One 7:e49833
Christakos G, Olea RA, Serre ML, Yu HL, Wang LL (2006) Interdisciplinary public health reasoning and epidemic modelling: the case of black death: the case of black death. Springer, Berlin
Christakos G, Wang J-F, Wu J (2014) Space–time medical mapping and causation modeling. In: Christakos G, Wang J, Wu J (eds) Stochastic medical reasoning and environmental health exposure. World Scientific, Singapore, pp 249–292
Christley R, Robinson S, Lysons R, French N (2005) Network analysis of cattle movement in Great Britain. Proc Soc Vet Epidemiol Prev Med, pp 234–243
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
Clifton-Hadley R (1993) The use of a geographical information system (GIS) in the control and epidemiology of bovine tuberculosis in south-west England. In: Thrusfield MV (ed) Proceedings of the society for veterinary epidemiology and preventive medicine, Roslin
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
Cowie CE, Gortázar C, White PCL, Hutchings MR, Vicente J (2015) Stakeholder opinions on the practicality of management interventions to control bovine tuberculosis. Vet J 204:179–185
DEFRA (2014) Request for information: bovine TB control costs. REF: 6505. https://www.gov.uk/government/uploads/system/uploads/attachment_data/file/323911/RFI_6505.pdf
DEFRA (2015) Monthly publication of national statistics on the incidence of tuberculosis (TB) in cattle to end September 2015 for Great Britain. https://www.gov.uk/government/statistics/incidence-of-tuberculosis-tb-in-cattle-in-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
Desouza K, Yuan L (2013) Towards evidence-driven policy design: complex adaptive systems and computational modeling. Annu Rev Policy Des 1:1–19
Donnelly CA, Nouvellet P (2013) The contribution of badgers to confirmed tuberculosis in cattle in high-incidence areas in England. PLoS Curr Outbreaks. doi:10.1371/currents.outbreaks.097a904d3f3619db2fe78d24bc776098
Donnelly CA, Woodroffe R (2015) Bovine tuberculosis: badger-cull targets unlikely to reduce TB. Nature 526:640
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 (2006) Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439:843–846
Donnelly CA, Wei G, Johnston WT, Cox DR, Woodroffe R, Bourne FJ, Cheeseman CL, Clifton-Hadley RS, Gettinby G, Gilks P, Jenkins HE, Le Fevre AM, McInerney JP, Morrison ES (2007) Impacts of widespread badger culling on cattle tuberculosis: concluding analysis from a large-scale field trial. Int J Infect Dis 11:300–308
Donnelly CA, Bento AI, Goodchild AV, Downs SH (2015) Exploration of the power of routine surveillance data to assess the impacts of industry-led badger culling on bovine tuberculosis incidence in cattle herds. Vet Rec 177:417
Drewe J, O’Connor H, Weber N, McDonald R, Delahay R (2013) Patterns of direct and indirect contact between cattle and badgers naturally infected with tuberculosis. Epidemiol Infect 141:1467–1475
Eisinger D, Thulke H-H (2008) Spatial pattern formation facilitates eradication of infectious diseases. J Appl Ecol 45:415–423
Enticott G (2001) Calculating nature: the case of badgers, bovine tuberculosis and cattle. J Rural Stud 17:149–164
Enticott G (2015) Public attitudes to badger culling to control bovine tuberculosis in rural Wales. Eur J Wildl Res 61:387–398
Enticott G, Maye D, Carmody P, Naylor R, Ward K, Hinchliffe S, Wint W, Alexander N, Elgin R, Ashton A, Upton P, Nicholson R, Goodchild T, Brunton L, Broughan J (2015) Farming on the edge: farmer attitudes to bovine tuberculosis in newly endemic areas. Vet Rec 177:439
Eurostat (2009) Farm Structure Survey in the United Kingdom—2007. In: 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 (2013) Predictive systems ecology. Proc R Soc B 280:20131452
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
Fan J, Han F, Liu H (2014) Challenges of big data analysis. Natl Sci Rev 1:293–314
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
Goodchild AV, Downs SH, Upton P, Wood JLN, de la Rua-Domenech R (2015) Specificity of the comparative skin test for bovine tuberculosis in Great Britain. Vet Rec 177:258
Gopal R, Goodchild A, Hewinson G, de la Rua Domenech R, Clifton-Hadley R (2006) Introduction of bovine tuberculosis to north-east England by bought-in cattle. Vet Rec 159:265–271
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
Judge J, Wilson GJ, Macarthur R, Delahay RJ, McDonald RA (2014) Density and abundance of badger social groups in England and Wales in 2011–2013. Sci Rep 4:3809
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
King HC, Murphy A, James P, Travis E, Porter D, Hung Y-J, Sawyer J, Cork J, Delahay RJ, Gaze W (2015) The variability and seasonality of the environmental reservoir of Mycobacterium bovis shed by wild European badgers. Sci Rep 5:12318
Knox E, Bartlett M (1964) The detection of space-time interactions. J R Stat Soc Ser C 13:25–30
Krackhardt D (1994) Graph theoretical dimensions of informal organizations. Comput Organ Theory 89:123–140
Krebs JR, Anderson R, Clutton-Brock T, Morrison I, Young D, Donnelly CA, Frost S, Woodroffe R (1997) Bovine tuberculosis in cattle and badgers. Report to the Rt Hon Dr Jack Cunningham MP by The Independent Scientific Review Group, London
Krebs JR, Anderson RM, Clutton-Brock T, Donnelly CA, Frost S, Morrison WI, Woodroffe R, Young D (1998) Badgers and bovine TB: conflicts between conservation and health. Science 279:817–818
Lange M, Siemen H, Blome S, Thulke HH (2014) Analysis of spatio-temporal patterns of African swine fever cases in Russian wild boar does not reveal an endemic situation. Prev Vet Med 117:317–325
Little T, Naylor P, Wilesmith J (1982) Laboratory study of Mycobacterium bovis infection in badgers and calves. Vet Rec 111:550–557
Lonergan M (2014) Data availability constrains model complexity, generality, and utility: a response to Evans et al. Trends Ecol Evol 29:301–302
Louca M, Vogiatzakis IN, Moustakas A (2015) Modelling the combined effects of land use and climatic changes: coupling bioclimatic modelling with Markov-chain cellular automata in a case study in Cyprus. Ecol Inform 30:241–249
Macdonald DW, Feber RE (2015) Wildlife conservation on farmland volume 2: conflict in the countryside. Oxford University Press, Oxford
Macdonald DW, Newman C, Buesching CD, Johnson PJ (2008) Male-biased movement in a high-density population of the Eurasian Badger (Meles meles). J Mammal 89:1077–1086
McKay MD, Beckman RJ, Conover WJ (1979) A comparison of three methods for selecting values of input variables in the analysis of output from a computer code. Technometrics 21:239–245
Mitchell A, Bourn D, Mawdsley J, Wint W, Clifton-Hadley R, Gilbert M (2005) Characteristics of cattle movements in Britain: an analysis of records from the cattle tracing system. Anim Sci 80:265–273
Moustakas A (2015) Fire acting as an increasing spatial autocorrelation force: implications for pattern formation and ecological facilitation. Ecol Complex 21:142–149
Moustakas A, Evans MR (2013) Integrating evolution into ecological modelling: accommodating phenotypic changes in agent based models. PLoS One 8:e71125
Moustakas A, Evans M (2015) 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
Moustakas A, Evans MR (2016) Regional and temporal characteristics of bovine tuberculosis of cattle in Great Britain. Stoch Environ Res Risk Assess 30:989–1003
Mullen EM, MacWhite T, Maher PK, Kelly DJ, Marples NM, Good M (2015) The avoidance of farmyards by European badgers Meles meles in a medium density population. Appl Anim Behav Sci 171:170–176
Najafabadi MM, Villanustre F, Khoshgoftaar TM, Seliya N, Wald R, Muharemagic E (2015) Deep learning applications and challenges in big data analytics. J Big Data 2:1–21
Naylor R, Manley W, Maye D, Enticott G, Ilbery B, Hamilton-Webb A (2015) The framing of public knowledge controversies in the media: a comparative analysis of the portrayal of badger vaccination in the english national, Regional and Farming Press. Sociol Ruralis
Nisbet MC, Markowitz EM (2015) Expertise in an age of polarization evaluating scientists’ political awareness and communication behaviors. Ann Am Acad Polit Soc Sci 658:136–154
O’Mahony DT (2015) Badger (Meles meles) contact metrics in a medium-density population. Mamm Biol Zeitschrift für Säugetierkunde 80:484–490
O’Hagan MJH, Matthews DI, Laird C, McDowell SWJ (in press) Farmer beliefs about bovine tuberculosis control in Northern Ireland. Vet J 10.1016/j.tvjl.2015.10.038
Parlane NA, Buddle BM (2015) Immunity and Vaccination against tuberculosis in Cattle. Curr Clin Microbiol Rep 2:44–53
Pfeiffer DU, Stevens KB (2015) Spatial and temporal epidemiological analysis in the big data era. Prev Vet Med 122:213–220
Porphyre T, McKenzie J, Stevenson MA (2011) Contact patterns as a risk factor for bovine tuberculosis infection in a free-living adult brushtail possum Trichosurus vulpecula population. Prev Vet Med 100:221–230
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0
Reis S, Seto E, Northcross A, Quinn NWT, Convertino M, Jones RL, Maier HR, Schlink U, Steinle S, Vieno M, Wimberly MC (2015) Integrating modelling and smart sensors for environmental and human health. Environ Model Softw 74:238–246
Ribeiro-Lima J, Enns EA, Thompson B, Craft ME, Wells SJ (2015) From network analysis to risk analysis: an approach to risk-based surveillance for bovine tuberculosis in Minnesota, US. Prev Vet Med 118:328–340
Schmitt SM, Fitzgerald SD, Cooley TM, Bruning-Fann CS, Sullivan L, Berry D, Carlson T, Minnis RB, Payeur JB, Sikarskie J (1997) Bovine tuberculosis in free-ranging white-tailed deer from Michigan. J Wildl Dis 33:749–758
Schumm P, Scoglio C, Scott HM (2015) An estimation of cattle movement parameters in the Central States of the US. Comput Electron Agric 116:191–200
Smith GC, Cheeseman CL (2007) Efficacy of trapping during the initial proactive culls in the randomised badger culling trial. Vet Rec 160:723–726
Smith CM, Downs SH, Mitchell A, Hayward AC, Fry H, Le Comber SC (2015) Spatial targeting for bovine tuberculosis control: can the locations of infected cattle be used to find infected badgers? PLoS One 10:e0142710
Stoyan D, Stoyan H (1994) Fractals, random shapes and point fields: methods of geometrical statistics. Wiley, Chichester
Torgerson P, Torgerson D (2008) Does risk to humans justify high cost of fighting bovine TB? Nature 455:1029
Touloudi A, Valiakos G, Athanasiou LV, Birtsas P, Giannakopoulos A, Papaspyropoulos K, Kalaitzis C, Sokos C, Tsokana CN, Spyrou V, Petrovska L, Billinis C (2015) A serosurvey for selected pathogens in Greek European wild boar. Vet Rec Open 2:e000077
Tweddle NE, Livingstone P (1994) Bovine tuberculosis control and eradication programs in Australia and New Zealand. Vet Microbiol 40:23–39
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York. ISBN 0-387-95457-0
Vicente J, Delahay RJ, Walker NJ, Cheeseman CL (2007) Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badger Meles meles population. J Anim Ecol 76:348–360
Vordermeier HM, Jones GJ, Buddle BM, Hewinson RG, Villarreal-Ramos B (2016) Bovine tuberculosis in cattle: vaccines, DIVA tests, and host biomarker discovery. Annu Rev Anim Biosci 4:87–109
Walpole J, Papin JA, Peirce SM (2013) Multiscale computational models of complex biological systems. Annu Rev Biomed Eng 15:137–154
Weber N, Carter SP, Dall SRX, Delahay RJ, McDonald JL, Bearhop S, McDonald RA (2013) Badger social networks correlate with tuberculosis infection. Curr Biol 23:R915–R916
Wiegand T, Moloney KA (2004) Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104:209–229
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
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
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
Woodroffe R, Gilks P, Johnston WT, Le Fevre AM, Cox DR, Donnelly CA, Bourne FJ, Cheeseman CL, Gettinby G, McInerney JP, Morrison WI (2008) Effects of culling on badger abundance: implications for tuberculosis control. J Zool 274:28–37
Woodroffe R, Donnelly CA, Wei G, Cox D, Bourne FJ, Burke T, Butlin RK, Cheeseman C, Gettinby G, Gilks P (2009) Social group size affects Mycobacterium bovis infection in European badgers (Meles meles). J Anim Ecol 78:818–827
Wright DM, Reid N, Ian Montgomery W, Allen AR, Skuce RA, Kao RR (2015) Herd-level bovine tuberculosis risk factors: assessing the role of low-level badger population disturbance. Sci Rep 5:13062
Zhang H, Jin X, Wang L, Zhou Y, Shu B (2015) 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
Acknowledgments
Comments of three anonymous reviewers have been exceptionally thorough and helpful. This paper is part of the special issue in Spatio-temporal Data Mining in Ecological and Veterinary Epidemiology. AM has been the guest editor for the special issue and declares that this submission was handled by regular member of the editorial board.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Moustakas, A., Evans, M.R. A big-data spatial, temporal and network analysis of bovine tuberculosis between wildlife (badgers) and cattle. Stoch Environ Res Risk Assess 31, 315–328 (2017). https://doi.org/10.1007/s00477-016-1311-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00477-016-1311-x