Emergency rabies control in a community of two high-density hosts

BMC Veterinary Research

Graham C Smith¹  Alexander Singer² 

[1] Food and Environment Research Agency, Sand Hutton, York, YO41 1LZ, UK;Present address: Department of Ecological Modelling, Helmholtz Centre for Environmental Research – UFZ, Permoserstr. 15, 04318, Leipzig, Germany

关键词: Vaccination;    Simulation;    Population control;    Multi-host disease;    Model;    Fox;    Exotic disease;    Epidemiology;    Cross species infection;    Badger;   

Others  :  1119808
DOI  :  10.1186/1746-6148-8-79

 received in 2011-09-14, accepted in 2012-05-30,  发布年份 2012

【 摘 要 】

Background

Rabies is a fatal viral disease that potentially can affect all mammals. Terrestrial rabies is not present in the United Kingdom and has been eliminated from Western Europe. Nevertheless the possibility remains that rabies could be introduced to England, where it would find two potentially suitable hosts, red foxes and badgers. With the aim to analyse the spread and emergency control of rabies in this two species host community, a simulation model was constructed. Different control strategies involving anti-rabies vaccination and population culling were developed, considering control application rates, spatial extent and timing. These strategies were evaluated for efficacy and feasibility to control rabies in hypothetical rural areas in the South of England immediately after a disease outbreak.

Results

The model confirmed that both fox and badger populations, separately, were competent hosts for the spread of rabies. Realistic vaccination levels were not sufficient to control rabies in high-density badger populations. The combined species community was a very strong rabies host. However, disease spread within species appeared to be more important than cross-species infection. Thus, the drivers of epidemiology depend on the potential of separate host species to sustain the disease. To control a rabies outbreak in the two species, both species had to be targeted. Realistic and robust control strategies involved vaccination of foxes and badgers, but also required badger culling. Although fox and badger populations in the UK are exceptionally dense, an outbreak of rabies can be controlled with a higher than 90% chance, if control response is quick and follows a strict regime. This requires surveillance and forceful and repeated control campaigns. In contrast, an uncontrolled rabies outbreak in the South of England would quickly develop into a strong epizootic involving tens of thousands of rabid foxes and badgers.

Conclusions

If populations of both host species are sufficiently large, epizootics are driven by within-species transmission, while cross-species-infection appears to be of minor importance. Thus, the disease control strategy has to target both host populations.

【 授权许可】

   
2012 Singer and Smith; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Haydon DT, Cleaveland S, Taylor LH, Laurenson MK: Identifying reservoirs of infection: A conceptual and practical challenge. Emerg Infect Dis 2002, 8:1468-1473.
• [2]Lembo T, Hampson K, Haydon DT, Craft M, Dobson A, Dushoff J, Ernest E, Hoare R, Kaare M, Mlengeya T, Mentzel C, Cleaveland S: Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. J Appl Ecol 2008, 45:1246-1257.
• [3]Smith GC: The role of the badger (Meles meles) in rabies epizootiology and the implications for Great Britain. Mammal Rev 2002, 32:13-26.
• [4]WHO: WHO expert consulatation on rabies. Geneva: World Health Organisation; 2004.
• [5]Holmala K, Kauhala K: Ecology of wildlife rabies in Europe. Mammal Rev 2006, 36:17-36.
• [6]Bögel K, Schaal E, Moegle H: The significance of martens as transmitters of wildlife rabies in Europe. Zbl Bakteriol 1977, 238:184.
• [7]Wandeler A, Wachendörfer G, Förster U, Krekel H, Müller J, Steck F: Rabies in wild carnivores in central Europe II. Virological and serological examinations. Zbl Vet Med B 1974, 21:757-764.
• [8]Smith GC, Wilkinson D: Modelling disease spread in a novel host: rabies in the European badger Meles meles. J Appl Ecol 2002, 39:865-874.
• [9]Macdonald DW, Newman C: Population dynamics of badgers (Meles meles) in Oxfordshire, U.K.: numbers, density and cohort life histories, and a possible role of climate change in population growth. J Zool 2002, 256:121-138.
• [10]Rogers LM, Delahay RJ, Cheeseman CL, Smith GC, Clifton-Hadley RS: The increase in badger (Meles meles) density at Woodchester Park, south-west England: implications for disease (Mycobacterium bovis) prevalence. Mammalia 1999, 63:183-192.
• [11]Kauhala K, Holmala K, Lammers W, Schregel J: Home ranges and densities of medium-sized carnivores in south-east Finland with special reference to rabies spread. Acta Theriol 2006, 51:1-13.
• [12]Goszczynski J: Fox, raccoon dog and badger densities in North Eastern Poland. Acta Theriol 1999, 44:413-420.
• [13]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.
• [14]Kosmider RD, Kelly L, Laurenson K, Coleman P, Fooks AR, Woolhouse M, Wooldridge M: Risk assessments to inform policy decisions regarding importation of pets from North America. Vet Rec 2006, 158:694-695.
• [15]Müller W, Cox J, Müller T: Rabies in Germany, Denmark and Austria. In Historical perspectives of rabies in Europe and the Mediterranean basin. Edited by King AA, Fooks AR, Aubert M, Wandeler AI. Paris: OIE; 2004:79-92.
• [16]Aubert MF, Cliquet F, Smak JA, Brochier B, Schon J, Kappeler A: Rabies in France, The Netherlands, Belgium, Luxembourg and Switzerland. In Historical perspectives of rabies in Europe and the Mediterranean basin. Edited by King AA, Fooks AR, Aubert M, Wandeler AI. Paris: OIE; 2004:129-145.
• [17]Smith GC, Fooks AR: Wildlife rabies control policy in Great Britain. Develop Biologicals 2006, 125:113-118.
• [18]Kauhala K, Holmala K: Contact rate and risk of rabies spread between medium-sized carnivores in southeast Finland. Ann Zool Fenn 2006, 43:348-357.
• [19]Macdonald DW, Buesching CD, Stopka P, Henderson J, Ellwood SA, Baker SE: Encounters between two sympatric carnivores: red foxes (Vulpes vulpes) and European badgers (Meles meles). J Zool 2004, 263:385-392.
• [20]Keesing F, Holt RD, Ostfeld RS: Effects of species diversity on disease risk. Ecol Lett 2006, 9:485-498.
• [21]Singer A, Kauhala K, Holmala K, Smith GC: Rabies in northeastern europe–the threat from invasive raccoon dogs. J Wildl Dis 2009, 45:1121-1137.
• [22]Webbon CC, Baker PJ, Harris S: Faecal density counts for monitoring changes in red fox numbers in rural Britain. J Appl Ecol 2004, 41:768-779.
• [23]Rogers LM, Cheeseman CL, Mallinson PJ, Clifton-Hadley R: The demography of a high-density badger (Meles meles) population in the west of England. J Zool 1997, 242:705-728.
• [24]Singer A, Kauhala K, Holmala K, Smith GC: Rabies risk in raccoon dogs and foxes. Develop Biologicals 2008, 131:213-222.
• [25]Jackson V, Huntley S, Tomlinson A, Smith GC, Taylor MA, Delahay RJ: Risk assessment and contingency planning for exotic disease introductions. In Management of Disease in Wild Mammals. Edited by Delahay RJ, Smith GC, Hutchings MR. Tokyo: Springer; 2009:169-185.
• [26]Smith GC, Harris S: Rabies in urban foxes (Vulpes vulpes) in Britain: the use of a spatial stochastic simulation model to examine the pattern of spread and evaluate the efficacy of different control regimes. Phil Trans R Soc Lond B 1991, 334:459-479.
• [27]Smith GC, Wilkinson D: Modeling control of rabies outbreaks in red fox populations to evaluate culling, vaccination, and vaccination combined with fertility control. J Wildl Dis 2003, 39:278-286.
• [28]Thulke HH, Eisinger D: The strength of 70% - after revision of a standard threshold of rabies control. Develop Biologicals 2008, 131:291-298.
• [29]Smith GC, Cheeseman CL: A mathematical model for control of diseases in wildlife populations: culling, vaccine and fertility control. Ecol Model 2002, 150:45-53.
• [30]Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS: Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 2010, 468:647-652.
• [31]Wilson GJ, Carter SP, Delahay RJ: Advances and prospects for management of TB transmission between badgers and cattle. Vet Microbiol 2011, 151:43-50.
• [32]Lewis DB: Avian Flu to Human Influenza. Annual Review of Medicine 2006, 57:139-154.
• [33]Wandeler A, Wachendörfer G, Förster U, Krekel H, Schale W, Müller J, Steck F: Rabies in wild carnivores in central Europe I. Epidemiological studies. Zbl Vet Med B 1974, 21:735-756.
• [34]Guerra MA, Curns AT, Rupprecht CE, Hanlon CA, Krebs JW, Childs JE: Skunk and raccoon rabies in the Eastern United States: temporal and spatial analysis. Emerg Infect Dis 2003, 9:1143-1150.
• [35]Craft ME, Hawthorne PL, Packer C, Dobson AP: Dynamics of a multihost pathogen in a carnivore community. J Anim Ecol 2008, 77:1257-1264.
• [36]Eisinger D, Thulke HH: Spatial pattern formation facilitates eradication of infectious diseases. J Appl Ecol 2008, 45:415-423.
• [37]Woodroffe R, Donnelly CA, Cox DR, Bourne FJ, Cheeseman CL, Delahay RJ, Gettinby G, McInerney JP, Morrison WI: Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis. J Appl Ecol 2006, 43:1-10.
• [38]European Commission: The oral vaccination of foxes against rabies. European Commission: Health & Consumer Protection Directorate-General; 2002.
• [39]Thulke H-H, Eisinger D, Freuling C, Fröhlich A, Globig A, Grimm V, Müller T, Selhorst T, Staubach C, Zips S: Situation-based surveillance: adapting investigations to actual epidemic situations. J Wildl Dis 2009, 45:1089-1103.
• [40]Slate D, Algeo TP, Nelson KM, Chipman RB, Donovan D, Blanton JD, Niezgoda M, Rupprecht CE: Oral Rabies Vaccination in North America: Opportunities, Complexities, and Challenges. PLoS Negl Trop Dis 2009, 3:e549.
• [41]Broadfoot JD, Rosatte RC, O'Leary DT: Raccoon and skunk population models for urban disease control planning in Ontario, Canada. Ecol Appl 2001, 11:295-303.
• [42]Grimm V, Berger U, Bastiansen F, Eliassen S, Ginot V, Giske J, Goss-Custard J, Grand T, Heinz SK, Huse G, Huth A, Jepsen J, Jørgensen C, Mooij WM, Müller B, Robbins A, Robbins M, Rossmanith E, Rüger N: Pe’er G, Railsback SF, Strand E, Souissi S, Stillmann R, Vabø R, Visser U, DeAngelis DL: A standard protocol for describing individual-based and agent-based models. Ecol Model 2006, 198:115-126.
• [43]Holland EP, Aegerter J, Dytham C, Smith GC: Landscape as a model: the importance of geometry. PLoS Computational Biol 2007, 3:e200.
• [44]Harris S, Yalden DW: Mammals of the British Isles: Handbook. 4th edition. Southampton: The Mammal Society; 2008.
• [45]Trewby ID, Wilson GJ, Delahay RJ, Walker NJ, Young RP, Davison J, Cheeseman CL, Robertson PA, Gorman ML, McDonald RA: Experimental evidence of competitive release in sympatric carnivores. Biol Lett 2008, 4:170-172.
• [46]Trewhella WJ, Harris S, McAllister FE: Dispersal distance, home-range size and population density in the red fox (Vulpes vulpes): a quantitative analysis. J Appl Ecol 1988, 25:423-434.
• [47]Rogers LM, Delahay R, Cheeseman CL, Langton S, Smith GC, Clifton-Hadley RS: Movement of badgers (Meles meles) in Woodchester Park, south west England: individual, population and disease effects. Proc R Soc B 1998, 265:1269-1276.
• [48]Wilkinson D, Bennett R, McFarlane I, Rushton S, Shirley M, Smith GC: Cost-benefit analysis model of badger (Meles meles) culling to reduce cattle herd tuberculosis breakdowns in Britain, with particular reference to badger perturbation. J Wildl Dis 2009, 45:1062-1088.
• [49]Macdonald DW: Wildlife rabies: the implications for Britain. Unresolved questions for the control of wildlife rabies: social perturbation and interspecific interactions. In Rabies in a changing world. Edited by Beynon PH, Ednay ATB. Cheltenham: British Small Animal Veterinary Association; 1995:33-48.
• [50]Carter SP, Delahay RJ, Smith GC, Macdonald DW, Riordan P, Etherington TR, Pimley E, Walker NJ, Cheeseman CL: 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 2007, 274:2769-2777.
• [51]Smith GC, Cheeseman CL, Wilkinson D, Clifton-Hadley RS: A model of bovine tuberculosis in the badger Meles meles: the inclusion of cattle and the use of a live test. J Appl Ecol 2001, 38:520-535.
• [52]Insley H: An estimate of the population density of the red fox (Vulpes vulpes) in the New Forest, Hampshire. J Zool 1977, 183:549-553.
• [53]Saltelli A, Chan K: Scott EM: Sensitivity analysis. Chichester, England: John Wiley and Sons Ltd; 2000.
• [54]Kennedy MC, Anderson CW, Conti S, O'Hagan A: Case studies in Gaussian process modelling of computer codes. Reliab Eng Syst Saf 2006, 91:1301-1309.