Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-30T15:27:41.979Z Has data issue: false hasContentIssue false
  • English
  • Français

Maintenance of a microparasite infecting several host species: rabies in the Serengeti

Published online by Cambridge University Press:  06 April 2009

S. Cleaveland  and
C. Dye
S. Cleaveland
Affiliation:
Institute of Zoology, Zoological Society of London, Regent's Park, London NW1 4RY, UK Vector Biology and Epidemiology Unit, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, U.K.
C. Dye
Affiliation:
Vector Biology and Epidemiology Unit, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, U.K.
Get access Rights & Permissions [Opens in a new window]

Summary

Whether and how microparasites such as rabies persist in their host populations are among the fundamental questions of infectious disease epidemiology. Rabies is a fatal disease of all mammalian species, but not all mammalian species can maintain the infection as reservoirs. The approach to control depends on which of the affected species do act as reservoirs. Bringing together old and new data, we examine here the role of wild and domestic animals in maintaining rabies in the Serengeti region of Tanzania, presenting our findings in two parts. In Part I, we argue that domestic dogs are the likely reservoirs because: (1) rabies has been continuously present in the dog population since its (re)introduction in 1977, whilst (2) wildlife cases have been very rare over this period, despite intensive study of Serengeti carnivores; (3) outbreaks of rabies in wild canids (jackals) elsewhere in Africa (Zimbabwe) have followed, rather than preceded, outbreaks in the dog population; (4) all viruses isolated from wild carnivores in the Serengeti ecosystem (including the Kenyan Masai Mara) are antigenically and genetically indistinguishable from the typical domestic dog Strain; (5) dog rabies control in the Serengeti between 1958–77 apparently eliminated the disease from both dogs and wildlife. Having identified dogs as reservoirs, Part II explores some possible mechanisms of maintenance in dog populations. In theory, infection is more likely to be maintained at higher dog densities, and we provide evidence that rabies is maintained in one district with a dog density > 5/km2, but not in two other districts with densities < 1/km2. Because 5 dogs/km2 is much lower than the expected density required for persistence, we go on to investigate the role of atypical infections, showing: (1) from serology, that a substantial proportion of healthy dogs in the Serengeti have detectable serum levels of rabies-specific antibody; (2) from mathematical models that, whilst we cannot be sure what seropositivity means, persistence in low-density dog populations is more likely if seropositives are infectious carriers, rather than slow-incubators or immunes.

Keywords

rabiesepidemiologyserologydogswildlifeSerengetiTanzania
Type
Research Article
Information
Parasitology , Volume 111 , Supplement S1: Ecology of wildlife host-parasite interactions , January 1995 , pp. S33 - S47
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aghomo, H. O., Oduye, O. O., Tomori, I. & Ibe, M. (1989). Isolation of rabies virus from clinically healthy and previously unvaccinated dogs. Bulletin of Animal Health and Production in Africa 37, 131–5.Google Scholar
Alexander, K. A., Smith, J. S., Macharia, M. J. & King, A. A. (1993). Rabies in the Masai Mara, Kenya: preliminary report. Onderstepoort Journal of Veterinary Research 60, 411–14.Google ScholarPubMed
Alexander, K. A., Smith, J. S., Macharia, M. J. & Kitala, P. (1994). Molecular epidemiology of rabies in Kenya. In: Proceedings of the Ninth International Conference on Negative Strand Viruses, Portugal. p. 180.Google Scholar
Anderson, R. M. & May, R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press. p. 20.Google Scholar
Andral, L. (1964). Une maladie comme les autres: la rage. Dix annees d'experimentation sur la rage en Ethiopie. Annales de l' Institut Pasteur Ethiopie 1, 58–65.Google Scholar
Andral, L. & Serie, C. (1957). Etudes experimentale sur la rage en Ethiopie. Annales de l' Institut Pasteur (Paris) 93, 475–88.Google Scholar
Artois, M., Aubert, M., Blancou, J., Barrat, J., Poulle, M. L. & Stahl, P. (1991). Ecologie des comportements de transmission de la rage. Annales Recherches Veterinaires 22, 163–72.Google Scholar
Aubert, M. F. A., Blancou, J., Barrat, J., Artois, M. & Barrat, M.-J. (1991). Transmission et pathogenie chez le renard roux de deux isolats a dix ans d'intervalle du virus de la rage vulpine. Annales Recherches Veterinaires 22, 77–93.Google Scholar
Bacon, P. J. (1985 a). Ed. Population Dynamics of Rabies in Wildlife. London: Academic Press.Google Scholar
Bacon, P. J. (1985 b). A systems analysis of wildlife rabies epizootics. In: Population Dynamics of Rabies in Wildlife (ed. Bacon, P. J.), pp. 109–130. London: Academic Press.Google Scholar
Barlow, N. D. (1995). Critical evaluation of wildlife disease models. In: Ecology of Infectious Diseases in Natural Populations (ed. Grenfell, B. T. & Dobson, A. P.), pp. 230–259. Cambridge, U.K.: Cambridge University Press.CrossRefGoogle Scholar
Barrat, J., Barrat, M. J., Picard, J. & Aubert, M. F. A. (1988). Diagnostic de la rage sur cultures cellulaires. Comparaison des resultats de l'inoculation au neuroblastome murin et de l'inoculation a la souris. Comparative Immunology Microbiology and Infectious Diseases 11, 207–14.CrossRefGoogle Scholar
Barrat, J. & Blancou, J. (1988). Simplified technique for the collection, storage and shipment of brain specimens for rabies diagnosis. WHO/Rabies Research 88.27. Geneva, Switzerland: World Health Organization.Google Scholar
Bell, J. F., Sancho, M. I., Diaz, A. M. & Moore, G. J. (1972). Nonfatal rabies in an enzootic area: results of a survey and evaluation of techniques. American Journal of Epidemiology 95, 190–8.CrossRefGoogle Scholar
Beran, G. W. (1991). Urban rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baer, G. M.), pp. 427–443. Boca Raton: CRC Press.Google Scholar
Beran, G. W. & Frith, M. (1988). Domestic animal rabies control: an overview. Reviews of Infectious Diseases 10 (Suppl 4), S672–7.CrossRefGoogle ScholarPubMed
Bingham, J. (1993). Rabies in Zimbabwe. In: Proceedings of the International Conference on Epidemiology, Control and Prevention of Rabies in Eastern and Southern Africa, Lusaka, Zambia, 1992. (ed. King, A. A.), pp. 29–33. Lyon: Editions Fondation Marcel Merieux.Google Scholar
Bingham, J. & Foggin, C. M. (1993). Jackal rabies in Zimbabwe. Onderstepoort Journal of Veterinary Research 60, 365–6.Google ScholarPubMed
Bingham, J., Hill, F. W. G. & Matema, R. (1994). Rabies incubation in an Africa civet (Civettictis civetta). Veterinary Record 134, 528.CrossRefGoogle Scholar
Blancou, J. (1988). Ecology and epidemiology of fox rabies. Reviews of Infectious Diseases 10, S606–14.CrossRefGoogle ScholarPubMed
Blancou, J., Aubert, M. F. A. & Artois, M. (1991). Fox Rabies. In: The Natural History of Rabies. 2nd ed. (ed. Baer, G. M.), pp. 257–290. Boca Raton: CRC Press.Google Scholar
Bourhy, H., Kissi, B. & Tordo, N. (1993). Taxonomy and evolutionary studies on Lyssaviruses with special reference to Africa. Onderstepoort Journal of Veterinary Research 60, 277–82.Google ScholarPubMed
Brooks, R. (1990). Survey of the dog population of Zimbabwe and its level of rabies vaccination. Veterinary Record 127, 592–6.Google ScholarPubMed
Bureau Of Statistics (1991). Tanzania Sensa 1988. Bureau of Statistics. President's Office, Planning Commission, Dar es Salaam, Tanzania.Google Scholar
Bwangamoi, O., Rottcher, D. & Wekesa, C. (1990). Rabies, microbesnoitiosis, and sarcocystosis in a lion. Veterinary Record 127, 411.Google Scholar
Carey, A. B. (1985). Multispecies rabies in the eastern United States. In: Population Dynamics of Rabies in Wildlife (ed. Bacon, P. J.), pp. 23–41. London: Academic Press.Google Scholar
Carey, A. B., Giles, R. H. & McLean, R. G. (1978). The landscape epidemiology of rabies in Virginia. American Journal of Tropical Medicine and Hygiene 27, 573–80.CrossRefGoogle ScholarPubMed
Caro, T. M. & Durant, S. M. (1995). The importance of behavioural ecology for conservation biology: examples from Serengeti carnivores. In: Serengeti II: Research, Management and Conservation of an Ecosystem (ed. Sinclair, A. R. E. & Arcese, P.), pp. 451–472. The University of Chicago Press.Google Scholar
Chaparro, F. & Esterhuysen, J. J. (1993). The role of the yellow mongoose (Cynictis penicillata) in the epidemiology of rabies in South Africa – preliminary results. Onderstepoort Journal of Veterinary Research 60, 373–7.Google ScholarPubMed
Charlton, K. M., Webster, W. A. & Casey, G. A. (1991). Skunk Rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baer, G. M.), pp. 307–324. Boca Raton: CRC Press.Google Scholar
Coleman, P. G. & Dye, C. (1995). Immunization coverage required to prevent outbreaks of dog rabies. Vaccine (in press).Google Scholar
Coyne, M. J., Smith, G. & McAllister, F. E. (1989). Mathematic model for the population biology of rabies in raccoons in the mid-Atlantic states. American Journal of Veterinary Research 50, 2148–54.Google ScholarPubMed
Crandell, R. A. (1991). Arctic fox rabies. In: The Natural History of Rabies. 2nd ed. (ed. Baer, G. M.), pp. 291–306. Boca Raton: CRC Press.Google Scholar
Cummings, D. H. M. (1982). A case history of the spread of rabies in an African country. South African Journal of Science 78, 443–7.Google Scholar
Dean, A. G., Dean, J. A., Burton, A. H. & Dicker, R. C. (1990). Epi Info, Version 5: A Word Processing, Database and Statistics Program for Epidemiology on Microcomputers. USD, Incorporated, Stone Mountain, Georgia.Google Scholar
Esterhuysen, J. J., Prehaud, C. & Thomson, G. R. (1995). A liquid-phase blocking ELISA for the detection of antibodies to rabies virus. Journal of Virological Methods 51, 31–42.CrossRefGoogle ScholarPubMed
Everard, C. O. R. & Everard, J. D. (1985). Mongoose rabies in Grenada. In: Population Dynamics of Rabies in Wildlife (ed. Bacon, P. J.), pp. 43–69. London: Academic Press.Google Scholar
Farro, M. M., Dighe, P. Y. & Nanavati, A. N. D. (1974). Investigation for rabies carriers among dogs. Indian Journal of Medical Research 62, 349–53.Google ScholarPubMed
Fekadu, M. (1972). Atypical rabies in Ethiopia. Ethiopian Medical Journal 10, 79–86.Google ScholarPubMed
Fekadu, M. (1991). Latency and aborted rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baier, G. M.), pp. 191–198. Boca Raton: CRC Press.Google Scholar
Fekadu, M. & Shaddock, J. H. (1984). Peripheral distribution of virus in dogs inoculated with two strains of rabies virus. American Journal of Veterinary Research 45, 724–9.Google ScholarPubMed
Fekadu, M., Shaddock, J. H. & Baer, G. M. (1981). Intermittent excretion of rabies virus in the saliva of a dog and two and six months after it had recovered from experimental rabies. American Journal of Tropical Medicine and Hygiene 30, 1113–15.CrossRefGoogle ScholarPubMed
Foggin, C. M. (1988). Rabies and Rabies-related Viruses in Zimbabwe: Historical, Virological and Ecological Aspects. PhD thesis, University of Zimbabwe, Harare.Google Scholar
Gascoyne, S. C., King, A. A., Laurenson, M. K., Borner, M., Schildger, B. & Barrat, J. (1993). Aspects of rabies infection and control in the conservation of the African wild dog (Lycaon pictus) in the Serengeti Region, Tanzania. Onderstepoort Journal of Veterinary Research 60, 415–20.Google ScholarPubMed
Hiscocks, K. & Perrin, M. R. (1988). Home range and movements of black-backed jackals at Cape Cross Seal Reserve, Namibia. South African Journal of Wildlife Research 18, 97–100.Google Scholar
Hofer, H. & East, M. L. (1993). The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. I. Social organization. Animal Behaviour 46, 547–57.CrossRefGoogle Scholar
Kaplan, M. M. & Koprowski, H. (1973). La Rage – Techniques de Laboratoire. 3rd Ed., Monograph Series no. 23, pp. 75–87. Geneva, Switzerland: World Health Organization.Google Scholar
King, A. A. (1991). Studies of the Antigenic Relationships of Rabies and Rabies-related Viruses Using Anti-nucleoprotein Monoclonal Antibodies. PhD thesis, University of Surrey, U.K.Google Scholar
King, A. A. (1993). Ed. Proceedings of the International Conference on Epidemiology, Control and Prevention of Rabies in Eastern and Southern Africa, Lusaka, Zambia, 1992. Lyon: Editions Fondation Marcel Merieux.Google Scholar
King, A. A., Meredith, C. D. & Thomson, G. R. (1994). The biology of Southern African lyssavirus variants. In: Lyssaviruses (eds. Rupprecht, C. E., Dietzschold, B. & Koprowski, H.), pp. 267–295. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Last, R. D., Jardine, J. E., Smit, M. M. E. & Van Der Lugt, J. J. (1994). Application of immunoperoxidase techniques to formalin-fixed brain tissue for the diagnosis of rabies in southern Africa. Onderstepoort Journal of Veterinary Research 61, 183–7.Google ScholarPubMed
Loretu, K. (1993). Rabies in Tanzania. In: Proceedings of the International Conference on Epidemiology, Control and Prevention of Rabies in Eastern and Southern Africa, Lusaka, Zambia, 1992 (ed. King, A. A.), pp. 17–18. Lyon: Editions Fondation Marcel Merieux.Google Scholar
Maas, B. (1993). The Behavioural Ecology and Social Organization of the Bat-eared Fox in the Serengeti National Park, Tanzania. PhD thesis, University of Cambridge, U.K.Google Scholar
Macdonald, D. W. (1993). Rabies and wildlife: a conservation problem? Onderstepoort Journal of Veterinary Research 60, 351–5.Google ScholarPubMed
Magembe, S. R. (1985). Epidemiology of rabies in the United Republic of Tanzania. In: Rabies in the Tropics (ed. Kuwert, E., Merieux, C., Koprowski, H. & Bogel, K.), pp. 392–398. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Malcolm, J. R. (1986). Socio-ecology of bat-eared foxes (Otocyon megalotis). Journal of Zoology 208, 457–68.CrossRefGoogle Scholar
McKenzie, A. A. (1993). Biology of the black-backed jackal Canis mesomelas with reference to rabies. Onderstepoort Journal of Veterinary Research 60, 367–71.Google ScholarPubMed
Mebatsion, T., Sillero-Zubiri, C., Gotelli, D. & Cox, J. H. (1992). Detection of rabies antibody by ELISA and RFFIT in unvaccinated dogs and in the endangered Simien jackal (Canis simensis) of Ethiopia. Journal of Veterinary Medicine B 39, 233–5.CrossRefGoogle ScholarPubMed
Meslin, F.-X., Fishbein, D. B. & Matter, H. C. (1994). Rationale and prospects for rabies elimination in developing countries. In: Lyssaviruses (ed. Rupprecht, C. E., Dietzschold, B. & Koprowski, H.), pp. 1–26. Berlin: Springer-Verlag.Google Scholar
Mills, M. G. L. (1993). Social systems and behaviour of the African wild dog Lycaon pictus and the spotted hyaena Crocuta crocuta with special reference to rabies. Onderstepoort Journal of Veterinary Research 60, 405–9.Google ScholarPubMed
Nel, J. A. J. (1993). The bat-eared fox: a prime candidate for rabies vector? Onderstepoort Journal of Veterinary Research 60, 395–7.Google Scholar
Nokes, J. D. (1992). Microparasites: Viruses and Bacteria. In: Natural Enemies: the Population Biology of Predators, Parasites and Diseases (ed. Crawley, M. J.), pp. 349–374. London: Blackwell Scientific Publications.CrossRefGoogle Scholar
Ogunkoya, A. B., Beran, G. W., Umoh, J. Y., Gomwalk, N. E. & Abdulkadir, A. (1990). Serological evidence of infection of dogs and man in Nigeria by Lyssaviruses (family Rhabdoviridae). Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 842–5.CrossRefGoogle ScholarPubMed
Perry, B. D. (1993). Dog ecology in eastern and southern Africa: implications for rabies control. Onderstepoort Journal of Veterinary Research 60, 429–36.Google ScholarPubMed
Rupprecht, C. E., Dietzschold, B., Wunner, W. H. & Koprowski, H. (1991). Antigenic relationships of Lyssaviruses. In: The Natural History of Rabies. 2nd Ed. (ed. Baer, G. M.), pp. 69–100. Boca Raton: CRC Press.Google Scholar
Rweyemamu, M. M., Loretu, K., Jakob, H. & Gorton, E. (1973). Observations on rabies in Tanzania. Bulletin of Epizootic Diseases in Africa 21, 19–27.Google Scholar
Smith, A. D. M. (1985). A continuous time deterministic model of temporal rabies. In: Population Dynamics of Rabies in Wildlife (ed. Bacon, P. J.), pp. 131–146. London: Academic Press.Google Scholar
Smith, J. S. (1989). Rabies ectopic variation: use in ecologic studies. Advances in Virus Research 36, 215–54.CrossRefGoogle Scholar
Swanepoel, R., Barnard, B. J. H., Meredith, C. D., Bishop, G., Bruckner, G. K., Foggin, C. M. & Hubschle, O. J. B. (1993). Rabies in southern Africa. Onderstepoort Journal of Veterinary Research 60, 325–46.Google ScholarPubMed
Taylor, P. J. (1993). A systematic and population genetic approach to the rabies problem in the yellow mongoose (Cynictis penicillata). Onderstepoort Journal of Veterinary Research 60, 379–87.Google Scholar
Thomson, G. R. & Meredith, C. D. (1993). Rabies in bat-eared foxes in South Africa. Onderstepoort Journal of Veterinary Research 60, 399–403.Google ScholarPubMed
Tordo, N., Badrane, H., Bourhy, H. & Sacramento, D. (1993). Molecular epidemiology of Lyssaviruses: focus on the glycoprotein and pseudogenes. Onderstepoort Journal of Veterinary Research 60, 315–23.Google ScholarPubMed
Veeraraghavan, N. (1973). Annual Report of the Director 1971 and Scientific Report 1972, p. 38. Coonor, India: Pasteur Institute of Southern India.Google Scholar
Voigt, D. R., Tinline, R. R. & Broekhoven, L. H. (1985). A spatial simulation model for rabies control. In: Population Dynamics of Rabies in Wildlife (ed. Bacon, P. J.), pp. 311–349. London: Academic Press.Google Scholar
Wandeler, A. I. (1991). Carnivore rabies: ecological and evolutionary aspects. Hystrix 3, 121–35.Google Scholar
Wandeler, A. I., Capt, S., Kappeler, A. & Hauser, R. (1988). Oral immunization of wildlife against rabies: concept and first field experiments. Reviews of Infectious Diseases 10, S649–53.CrossRefGoogle ScholarPubMed
Wandeler, A. I., Nadin-Davis, S. A., Tinline, R. R. & Rupprecht, C. E. (1994). Rabies epidemiology: some ecological and evolutionary perspectives. In: Lyssaviruses (ed. Rupprecht, C. E., Dietzschold, B. & Koprowski, H.), pp. 297–324. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Wandeler, A. I., Wachendorfer, G., Forster, U., Krekel, H., Schale, W., Muller, J. & Steck, F. (1974). Rabies in wild carnivores in central Europe 1. Epidemiological studies. Zentralblatt fur Veterinarmedizin Reihe B 21, 735–56.CrossRefGoogle Scholar
Winkler, W. G. & Jenkins, S. R. (1991). Raccoon rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baer, G. M.), pp. 325–340. Boca Raton: CRC Press.Google Scholar
World Health Organization (1987). Guidelines for Dog Rabies Control. WHO/VPH/83.43. Geneva, Switzerland: World Health Organization.Google Scholar
World Health Organization (1992). World Survey of Rabies, No. 25. WHO/Rabies/92.203. Geneva, Switzerland: World Health Organization.Google Scholar
Yasmuth, C., Nelson, K. E., Laima, T., Supawadee, J. & Thaiyanant, P. (1983). Prevalence of abortive canine rabies in Chiang Mai, Thailand. Journal of the Medical Association of Thailand 66, 169–75.Google ScholarPubMed
Zumpt, I. (1982). The yellow mongoose as a rabies vector on the central plateau of South Africa. South African Journal of Science 78, 417–18.Google Scholar