The use of immunocontraception to improve rabies eradication in urban dog populations
Matthew J. Carroll A D , Alexander Singer B C , Graham C. Smith B , Dave P. Cowan B and Giovanna Massei BA Department of Biology (Area 18), University of York, Wentworth Way, Heslington YO10 5DD, United Kingdom.
B Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, United Kingdom.
C Present address: Helmholtz Centre for Environmental Research – UFZ, Department of Ecological Modelling, Permoserstraße 15, 04318 Leipzig, Germany.
D Corresponding author. Email: mjc510@york.ac.uk
Wildlife Research 37(8) 676-687 https://doi.org/10.1071/WR10027
Submitted: 16 February 2010 Accepted: 2 October 2010 Published: 22 December 2010
Abstract
Context: Rabies causes ~55 000 human deaths each year, primarily as a result of bites from dogs, which are the major rabies reservoir in the developing world. Current rabies control strategies include vaccination, culling and surgical sterilisation of dogs. However, recently developed immunocontraceptives could be used alongside vaccination to apply fertility control to more animals.
Aims: We used a modelling approach to explore (1) whether adding single-dose contraceptives to rabies vaccination would improve effectiveness of rabies eradication, (2) how sensitive control methods are to variation in population parameters and (3) the effects of applying control continuously or in pulses on rabies eradication.
Methods: A continuous time, compartmental model was created to describe canine rabies epidemiology. Parameters were derived from the literature. The following three control methods were applied at varying rates and durations: vaccination, vaccination plus fertility control (v + fc) and culling. Outcomes were classified into the following three categories: rabies persistence, rabies eradication and population extinction.
Key results: When control was applied continuously for up to 24 months, vaccination was least effective; the effort required to eradicate rabies was about twice that required with culling or v + fc. At realistic control rates, only v + fc consistently resulted in rabies eradication. Increasing population growth rate and city size made rabies eradication harder; for vaccination, considerably greater control rates and durations were required, whereas culling and v + fc showed only minor decreases in effectiveness. When control was applied for 1 or 2 months (for one month every 12 months or every 6 months) per year for up to 20 years, vaccination became less effective because of population turnover between control periods; v + fc lost little effectiveness, as decreased birth rates reduced the input of susceptible animals.
Conclusions: Using immunocontraception alongside vaccination could improve rabies control campaigns by reducing the proportion of the population that must be treated, or reducing the necessary duration of the campaign. It could also make control effective under larger population growths, in larger cities and when control is pulsed.
Implications: Immunocontraceptives could become a useful tool in canine rabies control by allowing fertility control to be applied on a large scale. Further work is required to improve understanding of dog ecology and parameterise location-specific models, which could be used to inform management plans.
References
Acosta-Jamett, G., Cleaveland, S., Cunningham, A. A., and Bronsvoort, B. M.deC. (2010). Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission. Preventive Veterinary Medicine 94, 272–281.| Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3hsFCnsg%3D%3D&md5=5438d15d8fe729b801ed5c679fc706cbCAS | 20096943PubMed |
Anderson, R. M. (1982). ‘The Population Dynamics of Infectious Diseases: Theory and Applications.’ (Chapman & Hall: London.)
Anderson, R. M., Jackson, H. C., May, R. M., and Smith, A. M. (1981). Population dynamics of fox rabies in Europe. Nature 289, 765–771.
| Population dynamics of fox rabies in Europe.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7itlWisg%3D%3D&md5=1d29903216b50369c85322ef06b5a264CAS | 7464941PubMed |
Barlow, N. D. (1996). The ecology of wildlife disease control: simple models revisited. Journal of Applied Ecology 33, 303–314.
| The ecology of wildlife disease control: simple models revisited.Crossref | GoogleScholarGoogle Scholar |
Barlow, N. D. (2000). The ecological challenge of immunocontraception: editor’s introduction. Journal of Applied Ecology 37, 897–902.
| The ecological challenge of immunocontraception: editor’s introduction.Crossref | GoogleScholarGoogle Scholar |
Bender, S. C., Berg, D. L., Wenning, K. M., Miller, L. A., Slate, D., Jackson, F. R., and Rupprecht, C. E. (2009). No adverse effects of simultaneous vaccination with the immunocontraceptive GonaCon™ and a commercial rabies vaccine on rabies virus neutralizing antibody production in dogs. Vaccine 27, 7210–7213.
| No adverse effects of simultaneous vaccination with the immunocontraceptive GonaCon™ and a commercial rabies vaccine on rabies virus neutralizing antibody production in dogs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVGlsbvM&md5=f32ad7f6a486b989a7aaa9e8cc6d9a60CAS | 19925955PubMed |
Beran, G. W., and Frith, M. (1988). Domestic animal rabies control: an overview. Reviews of Infectious Diseases 10, S672–S677.
| 3206079PubMed |
Bingham, J. (2005). Canine rabies ecology in southern Africa. Emerging Infectious Diseases 11, 1337–1342.
| 16229759PubMed |
Bögel, K., and Meslin, F. X. (1990). Economics of human and canine rabies elimination: guidelines for programme orientation. Bulletin of the World Health Organization 68, 281–291.
| 2118428PubMed |
Brooks, R. (1990). Survey of the dog population of Zimbabwe and its level of rabies vaccination. The Veterinary Record 127, 592–596.
| 1:STN:280:DyaK3M7msFaluw%3D%3D&md5=3124c558bb080fd46e19ab6d2615e8f0CAS | 2075689PubMed |
Carter, S. P., Delahay, R. J., Smith, G. C., Macdonald, D. W., Riordan, R., Etherington, T. R., Pimley, E. R., Walker, N. J., and Cheeseman, C. L. (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. Proceedings of the Royal Society of London. Series B. Biological Sciences 274, 2769–2777.
| 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.Crossref | GoogleScholarGoogle Scholar |
Cleaveland, S. (1998). Epidemiology and control of rabies. The growing problem of rabies in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 131–134.
| Epidemiology and control of rabies. The growing problem of rabies in Africa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1cvjs1yjtg%3D%3D&md5=c06f6333fb544315f27acc324080f16bCAS | 9764313PubMed |
Cleaveland, S., and Dye, C. (1995). Maintenance of a microparasite infecting several host species: rabies in the Serengeti. Parasitology 111, 33–47.
| Maintenance of a microparasite infecting several host species: rabies in the Serengeti.Crossref | GoogleScholarGoogle Scholar |
Cleaveland, S., Kaare, M., Knobel, D., and Laurenson, M. K. (2006). Canine vaccination – providing broader benefits for disease control. Veterinary Microbiology 117, 43–50.
| Canine vaccination – providing broader benefits for disease control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsVOhsbs%3D&md5=217025b6a48412867e0e51c3070ed1beCAS | 16701966PubMed |
Coleman, P. G., and Dye, C. (1996). Immunization coverage required to prevent outbreaks of dog rabies. Vaccine 14, 185–186.
| Immunization coverage required to prevent outbreaks of dog rabies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FnvVWgsg%3D%3D&md5=19b9c9b45ab0cade5aac791b3f735344CAS | 8920697PubMed |
Courchamp, F., and Cornell, S. J. (2000). Virus-vectored immunocontraception to control feral cats on islands: a mathematical model. Journal of Applied Ecology 37, 903–913.
| Virus-vectored immunocontraception to control feral cats on islands: a mathematical model.Crossref | GoogleScholarGoogle Scholar |
Cowan, D. P., and Massei, G. (2008). Wildlife contraception, individuals and populations: how much fertility control is enough? In ‘Proceedings of the 23rd Vetebrate Pest Conference’. (Eds R. M. Timm and M. B. Madon.) pp. 220–228. (University of California: Davis, CA.)
Cowan, D. P., Massei, G., and Mellows, R. J. B. (2006). A modeling approach to evaluating potential applications of emerging fertility control technologies in the UK. In ‘Proceedings of the 22nd Vertebrate Pest Conference’. (Eds R. M. Timm and J. M. O’Brien.) pp. 55–62. (University of California: Davis, CA.)
Daniels, T. J., and Bekoff, M. (1989). Population and social biology of free-ranging dogs, Canis familiaris. Journal of Mammalogy 70, 754–762.
| Population and social biology of free-ranging dogs, Canis familiaris.Crossref | GoogleScholarGoogle Scholar |
Earn, D. J. D., Rohani, P., and Grenfell, B. T. (1998). Persistence, chaos and synchrony in ecology and epidemiology. Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 7–10.
| Persistence, chaos and synchrony in ecology and epidemiology.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7jtV2ruw%3D%3D&md5=fa403a9e46bba36b43556f324bbbf7ccCAS |
Fagerstone, K. A., Miller, L. A., Bynum, K. S., Eisemann, J. D., and Yoder, C. (2006). When, where and for what wildlife species will contraception be a useful management approach? In ‘Proceedings of the 22nd Vertebrate Pest Conference’. (Eds R.M. Timm and J. M. O’Brien.) pp. 55–62. (University of California: Davis, CA.)
Foggin, C. M. (1988). Rabies and rabies-related viruses in Zimbabwe: historical, virological and ecological aspects. Ph.D. Thesis, University of Zimbabwe, Harare.
Hampson, K., Dushoff, J., Bingham, J., Brückner, G., Ali, Y. H., and Dobson, A. (2007). Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts. Proceedings of the National Academy of Sciences, USA 104, 7717–7722.
| Synchronous cycles of domestic dog rabies in sub-Saharan Africa and the impact of control efforts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslahtro%3D&md5=14b76d9cb088c1aef2429c097e86731aCAS |
Hampson, K., Dushoff, J., Cleaveland, S., Haydon, D. T., Kaare, M., Packer, C., and Dobson, A. (2009). Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biology 7, e1000053.
| Transmission dynamics and prospects for the elimination of canine rabies.Crossref | GoogleScholarGoogle Scholar |
Hemachudha, T. (2005). Rabies and dog population control in Thailand: success or failure? Journal of the Medical Association of Thailand 88, 120–123.
| 15960231PubMed |
Kato, M., Yamamoto, H., Inukai, Y., and Kira, S. (2003). Survey of the stray dog population and the health education program on the prevention of dog bites and dog-acquired infections: a comparative study in Nepal and Okayama Prefecture, Japan. Acta Medica Okayama 57, 261–266.
| 14679405PubMed |
Killian, G., Miller, L., Rhyan, J., and Doten, H. (2006). Immunocontraception of Florida feral swine with a single-dose GnRH vaccine. American Journal of Reproductive Immunology 55, 378–384.
| Immunocontraception of Florida feral swine with a single-dose GnRH vaccine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xltlehtr4%3D&md5=7dd009c3b143ef233270846a1b9f6cf1CAS | 16635212PubMed |
Kitala, P. M., McDermott, J. J., Coleman, P. G., and Dye, C. (2002). Comparison of vaccination strategies for the control of dog rabies in Machakos District, Kenya. Epidemiology and Infection 129, 215–222.
| Comparison of vaccination strategies for the control of dog rabies in Machakos District, Kenya.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38vlt1Sitw%3D%3D&md5=493f9ec6d06f4cf02ff2d8d3d5ac6dc8CAS | 12211590PubMed |
Knobel, D. L., Cleaveland, S., Coleman, P. G., Fèvre, E. M., Meltzer, M. I., Miranda, M. E. G., Shaw, A., Zinsstag, J., and Meslin, F. X. (2005). Re-evaluating the burden of rabies in Africa and Asia. Bulletin of the World Health Organization 83, 360–368.
| 15976877PubMed |
Knobel, D. L., Kaare, M., Fèvre, E., and Cleaveland, S. (2007). Dog rabies and its control. In ‘Rabies’. (Eds A. C. Jackson and W. H. Wunner.) pp. 573–594. (Elsevier Academic Press: London.)
Kutzler, M., and Wood, A. (2006). Non-surgical methods of contraception and sterilization. Theriogenology 66, 514–525.
| Non-surgical methods of contraception and sterilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XntVyrt74%3D&md5=af8ea049473102c0e18612bf7fe0d906CAS | 16757019PubMed |
Leney, J., and Remfry, J. (2000). Dog population management. In ‘Dogs, Zoonoses and Public Health’. (Eds C. N. L. Macpherson, F. X. Meslin and A. I. Wandeler.) pp. 299–331. (CABI Publishing: Wallingford, UK.)
Massei, G., Killian, G., and Miller, L. A. (2008a). Immunocontraception to control dog populations. In ‘WHO–OIE Intercountry Expert Workshop on protecting humans from domestic and wildlife rabies in the Middle East’. (Eds F. X. Meslin, A. Seimenis, G. Yehia and H. Imam.) pp. 33–35. (WHO/Mediterranean Zoonoses Control Programme: Athens, Greece.)
Massei, G., Cowan, D. P., Coats, J., Gladwell, F., Lane, J. E., and Miller, L. A. (2008b). Effect of the GnRH vaccine GonaConTM on the fertility, physiology and behaviour of wild boar. Wildlife Research 35, 540–547.
| Effect of the GnRH vaccine GonaConTM on the fertility, physiology and behaviour of wild boar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1KrtLjP&md5=4490e4008ec6b3ecb6831494b84fbdbaCAS |
Massei, G., Miller, L. A., and Killian, G. (2010). Immunocontraception to control rabies in dog populations. Human–Wildlife Interactions 4, 20–22.
Matter, H. C., and Daniels, T. J. (2000). Dog ecology and population biology. In ‘Dogs, Zoonoses and Public Health’. pp. 17–62. (Eds C. N. L. Macpherson, F. X. Meslin and A. I. Wandeler.) (CABI Publishing: Wallingford, UK.)
Merrill, J. A., Cooch, E. G., and Curtis, P. D. (2003). Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer. The Journal of Wildlife Management 67, 267–279.
| Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer.Crossref | GoogleScholarGoogle Scholar |
Meslin, F. X., Miles, M. A., Vexenat, J. A., and Gemmell, M. A. (2000). Zoonoses control in dogs. In ‘Dogs, Zoonoses and Public Health’. (Eds C. N. L. Macpherson, F. X. Meslin and A. I. Wandeler.) pp. 335–372. (CABI Publishing: Wallingford, UK.)
Miller, L. A., Gionfriddo, J. P., Fagerstone, K. A., Rhyan, J. C., and Killian, G. J. (2008a). The single-shot GnRH immunocontraceptive vaccine (GonaCon™) in white-tailed deer: comparison of several GnRH preparations. American Journal of Reproductive Immunology 60, 214–223.
| The single-shot GnRH immunocontraceptive vaccine (GonaCon™) in white-tailed deer: comparison of several GnRH preparations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKrsbzP&md5=66115397852b0d6287e1000b36f7c66cCAS | 18782282PubMed |
Miller, L. A., Gionfriddo, J. P., Rhyan, J. C., Fagerstone, K. A., Wagner, D. C., and Killian, G. J. (2008b). GnRH immunocontraception of male and female white-tailed deer fawns. Human–Wildlife Conflicts 2, 93–101.
Perry, B. D. (1993). Dog ecology in eastern and southern Africa: implications for rabies control. The Onderstepoort Journal of Veterinary Research 60, 429–436.
| 1:STN:280:DyaK2M3ps1Whsw%3D%3D&md5=7de0473c94edd14a30af2253a73918b5CAS | 7777332PubMed |
R Development Core Team (2008). ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna.)
Ramsey, D. (2007). Effects of fertility control on behavior and disease transmission in brushtail possums. The Journal of Wildlife Management 71, 109–116.
| Effects of fertility control on behavior and disease transmission in brushtail possums.Crossref | GoogleScholarGoogle Scholar |
Reece, J. F., and Chawla, S. K. (2006). Control of rabies in Jaipur, India, by the sterilisation and vaccination of neighbourhood dogs. The Veterinary Record 159, 379–383.
| Control of rabies in Jaipur, India, by the sterilisation and vaccination of neighbourhood dogs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD28rlsFGrtA%3D%3D&md5=59699828046d2255a2706b659104141aCAS | 16980523PubMed |
Sallum, P. C., Almeida, M. F., and Massad, E. (2000). Rabies seroprevalence of street dogs from São Paulo City, Brazil. Preventive Veterinary Medicine 44, 131–139.
| Rabies seroprevalence of street dogs from São Paulo City, Brazil.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c3is1WrsA%3D%3D&md5=5b0fe2287afb05abbeb3f3038e166545CAS | 10760397PubMed |
Schmidt, P. M., Swannack, T. M., Lopez, R. R., and Slater, M. R. (2009). Evaluation of euthanasia and trap–neuter–return (TNR) programs in managing free-roaming cat populations. Wildlife Research 36, 117–125.
| Evaluation of euthanasia and trap–neuter–return (TNR) programs in managing free-roaming cat populations.Crossref | GoogleScholarGoogle Scholar |
Smith, G. C., and Cheeseman, C. L. (2002). A mathematical model for the control of diseases in wildlife populations: culling, vaccination and fertility control. Ecological Modelling 150, 45–53.
| A mathematical model for the control of diseases in wildlife populations: culling, vaccination and fertility control.Crossref | GoogleScholarGoogle Scholar |
Smith, G. C., and Harris, S. (1989). The control of rabies in urban fox populations. In ‘Mammals as Pests’. (Ed. R. J. Putnam.) pp. 209–224. (Chapman and Hall: London.)
Smith, G. C., and Harris, S. (1991). 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. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 334, 459–479.
| 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.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK387ltVGgsg%3D%3D&md5=d2c7ef95e6099f8abd8b72b19f84515aCAS | 1686115PubMed |
Smith, G. C., and Wilkinson, D. (2003). Modeling control of rabies outbreaks in red fox populations to evaluate culling, vaccination, and vaccination combined with fertility control. Journal of Wildlife Diseases 39, 278–286.
| 1:STN:280:DC%2BD3szns1Gksg%3D%3D&md5=9734de4b47b74b7e3d8d41c62c523f14CAS | 12910754PubMed |
Smith, G. C., Parrott, D., and Robertson, P. A. (2008). Managing wildlife populations with uncertainty: cormorants Phalacrocorax carbo. Journal of Applied Ecology 45, 1675–1682.
| Managing wildlife populations with uncertainty: cormorants Phalacrocorax carbo.Crossref | GoogleScholarGoogle Scholar | 19536342PubMed |
Thulke, H. H., and Eisinger, D. (2008). The strength of 70%: revisions of a standard threshold of rabies control. Developments in Biologicals 131, 291–298.
| 18634491PubMed |
Wandeler, A. I., and Bingham, J. (2000). Dogs and rabies. In ‘Dogs, Zoonoses and Public Health’. (Eds C. N. L. Macpherson, F. X. Meslin and A. I. Wandeler.) pp. 63–90. (CABI Publishing: Wallingford, UK.)
Wandeler, A. I., Matter, H. C., Kappeler, A., and Budde, A. (1993). The ecology of dogs and canine rabies: a selective review. Revue Scientifique et Technique (International Office of Epizootics) 12, 51–71.
| 1:STN:280:DyaK3s3pvFSjsA%3D%3D&md5=052aa739664b979be67f05f516d01a9eCAS | 8518447PubMed |
White, P. C. L., Lewis, A. J. G., and Harris, S. (1997). Fertility control as a means of controlling bovine tuberculosis in badger (Meles meles) populations in south-west England: predictions from a spatial stochastic simulation model. Proceedings of the Royal Society of London. Series B. Biological Sciences 264, 1737–1747.
| Fertility control as a means of controlling bovine tuberculosis in badger (Meles meles) populations in south-west England: predictions from a spatial stochastic simulation model.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c7gvFSgtA%3D%3D&md5=8810dccf9ca0ea50b3242cd5d0079e5fCAS |
WHO (2004). ‘WHO Expert Consultation on Rabies: First Report.’ (WHO: Geneva, Switzerland.)
Williams, C. K., Davey, C. C., Moore, R. J., Hinds, L. A., Silvers, L. E., Kerr, P. J., French, N., Hood, G. M., Pech, R. P., and Krebs, C. J. (2007). Population responses to sterility imposed on female European rabbits. Journal of Applied Ecology 44, 291–301.
| Population responses to sterility imposed on female European rabbits.Crossref | GoogleScholarGoogle Scholar |
Woodroffe, R., Donnelly, C. A., Cox, D. R., Bourne, F. J., Cheeseman, C. L., Delahay, R. J., Gettinby, G., McInerney, J. P., and Morrison, W. I. (2006). Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis. Journal of Applied Ecology 43, 1–10.
| Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis.Crossref | GoogleScholarGoogle Scholar |