Skip to main content
×
Home

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

  • S. Cleaveland (a1) (a2) and C. Dye (a2)
Summary
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.

Copyright
References
Hide All
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.
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.
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.
Anderson R. M. & May R. M. (1992). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press. p. 20.
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, 5865.
Andral L. & Serie C. (1957). Etudes experimentale sur la rage en Ethiopie. Annales de l' Institut Pasteur (Paris) 93, 475–88.
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.
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, 7793.
Bacon P. J. (1985 a). Ed. Population Dynamics of Rabies in Wildlife. London: Academic Press.
Bacon P. J. (1985 b). A systems analysis of wildlife rabies epizootics. In: Population Dynamics of Rabies in Wildlife (ed. Bacon P. J.), pp. 109130. London: Academic Press.
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. 230259. Cambridge, U.K.: Cambridge University Press.
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.
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.
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.
Beran G. W. (1991). Urban rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baer G. M.), pp. 427443. Boca Raton: CRC Press.
Beran G. W. & Frith M. (1988). Domestic animal rabies control: an overview. Reviews of Infectious Diseases 10 (Suppl 4), S6727.
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. 2933. Lyon: Editions Fondation Marcel Merieux.
Bingham J. & Foggin C. M. (1993). Jackal rabies in Zimbabwe. Onderstepoort Journal of Veterinary Research 60, 365–6.
Bingham J., Hill F. W. G. & Matema R. (1994). Rabies incubation in an Africa civet (Civettictis civetta). Veterinary Record 134, 528.
Blancou J. (1988). Ecology and epidemiology of fox rabies. Reviews of Infectious Diseases 10, S60614.
Blancou J., Aubert M. F. A. & Artois M. (1991). Fox Rabies. In: The Natural History of Rabies. 2nd ed. (ed. Baer G. M.), pp. 257290. Boca Raton: CRC Press.
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.
Brooks R. (1990). Survey of the dog population of Zimbabwe and its level of rabies vaccination. Veterinary Record 127, 592–6.
Bureau Of Statistics (1991). Tanzania Sensa 1988. Bureau of Statistics. President's Office, Planning Commission, Dar es Salaam, Tanzania.
Bwangamoi O., Rottcher D. & Wekesa C. (1990). Rabies, microbesnoitiosis, and sarcocystosis in a lion. Veterinary Record 127, 411.
Carey A. B. (1985). Multispecies rabies in the eastern United States. In: Population Dynamics of Rabies in Wildlife (ed. Bacon P. J.), pp. 2341. London: Academic Press.
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.
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. 451472. The University of Chicago Press.
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.
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. 307324. Boca Raton: CRC Press.
Coleman P. G. & Dye C. (1995). Immunization coverage required to prevent outbreaks of dog rabies. Vaccine (in press).
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.
Crandell R. A. (1991). Arctic fox rabies. In: The Natural History of Rabies. 2nd ed. (ed. Baer G. M.), pp. 291306. Boca Raton: CRC Press.
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.
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.
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, 3142.
Everard C. O. R. & Everard J. D. (1985). Mongoose rabies in Grenada. In: Population Dynamics of Rabies in Wildlife (ed. Bacon P. J.), pp. 4369. London: Academic Press.
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.
Fekadu M. (1972). Atypical rabies in Ethiopia. Ethiopian Medical Journal 10, 7986.
Fekadu M. (1991). Latency and aborted rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baier G. M.), pp. 191198. Boca Raton: CRC Press.
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.
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.
Foggin C. M. (1988). Rabies and Rabies-related Viruses in Zimbabwe: Historical, Virological and Ecological Aspects. PhD thesis, University of Zimbabwe, Harare.
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.
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, 97100.
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.
Kaplan M. M. & Koprowski H. (1973). La Rage – Techniques de Laboratoire. 3rd Ed., Monograph Series no. 23, pp. 7587. Geneva, Switzerland: World Health Organization.
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.
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.
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. 267295. Berlin: Springer-Verlag.
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.
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. 1718. Lyon: Editions Fondation Marcel Merieux.
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.
Macdonald D. W. (1993). Rabies and wildlife: a conservation problem? Onderstepoort Journal of Veterinary Research 60, 351–5.
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. 392398. Berlin: Springer-Verlag.
Malcolm J. R. (1986). Socio-ecology of bat-eared foxes (Otocyon megalotis). Journal of Zoology 208, 457–68.
McKenzie A. A. (1993). Biology of the black-backed jackal Canis mesomelas with reference to rabies. Onderstepoort Journal of Veterinary Research 60, 367–71.
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.
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. 126. Berlin: Springer-Verlag.
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.
Nel J. A. J. (1993). The bat-eared fox: a prime candidate for rabies vector? Onderstepoort Journal of Veterinary Research 60, 395–7.
Nokes J. D. (1992). Microparasites: Viruses and Bacteria. In: Natural Enemies: the Population Biology of Predators, Parasites and Diseases (ed. Crawley M. J.), pp. 349374. London: Blackwell Scientific Publications.
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.
Perry B. D. (1993). Dog ecology in eastern and southern Africa: implications for rabies control. Onderstepoort Journal of Veterinary Research 60, 429–36.
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. 69100. Boca Raton: CRC Press.
Rweyemamu M. M., Loretu K., Jakob H. & Gorton E. (1973). Observations on rabies in Tanzania. Bulletin of Epizootic Diseases in Africa 21, 1927.
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. 131146. London: Academic Press.
Smith J. S. (1989). Rabies ectopic variation: use in ecologic studies. Advances in Virus Research 36, 215–54.
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.
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.
Thomson G. R. & Meredith C. D. (1993). Rabies in bat-eared foxes in South Africa. Onderstepoort Journal of Veterinary Research 60, 399403.
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.
Veeraraghavan N. (1973). Annual Report of the Director 1971 and Scientific Report 1972, p. 38. Coonor, India: Pasteur Institute of Southern India.
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. 311349. London: Academic Press.
Wandeler A. I. (1991). Carnivore rabies: ecological and evolutionary aspects. Hystrix 3, 121–35.
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, S64953.
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. 297324. Berlin: Springer-Verlag.
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.
Winkler W. G. & Jenkins S. R. (1991). Raccoon rabies. In: The Natural History of Rabies. 2nd Ed. (ed. Baer G. M.), pp. 325340. Boca Raton: CRC Press.
World Health Organization (1987). Guidelines for Dog Rabies Control. WHO/VPH/83.43. Geneva, Switzerland: World Health Organization.
World Health Organization (1992). World Survey of Rabies, No. 25. WHO/Rabies/92.203. Geneva, Switzerland: World Health Organization.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 43 *
Loading metrics...

Abstract views

Total abstract views: 250 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd November 2017. This data will be updated every 24 hours.