The Afya Serengeti Project
World Small Animal Veterinary Association World Congress Proceedings, 2014
Sarah Cleaveland, BSc, BA, VetMB, PhD, MRCVS, FRSE
Boyd Orr Centre for Population and Ecosystem Health; Institute of Biodiversity, Animal Health and Comparative Medicine; College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK

Afya Serengeti, meaning health for the Serengeti in Swahili, is a program that aims to support the health of the Serengeti ecosystem through domestic dog vaccination campaigns. The program was initiated in response to outbreaks of rabies and canine distemper, diseases that pose a threat to the health of people, domestic animals and wildlife in the Serengeti.

Rabies is a devastating and fatal disease caused by neurotropic RNA viruses in the Lyssavirus genus. Rabies is a globally distributed zoonosis that can infect and be transmitted from all mammal species, but the vast majority of human deaths worldwide result from the bite of rabid dogs. Although rabies has been successfully controlled in many parts of the world, it is estimated that at least 55,000 people still die every year from rabies, mostly children in Asia and Africa, where canine rabies remains endemic (Knobel et al. 2005; WHO 2013). As with many neglected tropical diseases, rabies suffers from a cycle of neglect because few human or animal cases are ever reported officially, and it is almost only ever the poor who will die from rabies - people living in marginalized communities with little access to health or veterinary services. In these communities, rabies also has a major psychological impact, traumatising those who witness a case, and causing profound anxiety for those needing the costly post-exposure prophylaxis after the bite of a suspected rabid dog.

Rabies has also raised concerns among conservationists, with outbreaks of disease causing major declines in some of the world's most endangered species, including African wild dogs (Lycaon pictus) and Ethiopian wolves (Canis simensis) (Woodroffe et al. 2004). In the Serengeti, the small population of wild dogs that survived on the plains and in the western corridor of the park, declined to the brink of local extinction following epidemics of rabies in the late 1980s and early 1990s, caused by a strain of virus that was indistinguishable from that isolated from domestic dogs (Lembo et al. 2007). Subsequently, epidemiological studies indicated that domestic dogs were likely to be the only maintenance host of rabies in the Serengeti and principal source of infection for both people and wildlife (Lembo et al. 2008; Hampson et al. 2009; Beyer et al. 2011).

Canine distemper virus (CDV) is a member of the morbillivirus family, which comprises viruses of medical and veterinary importance, including measles, rinderpest, and peste de petits ruminants (PPR). CDV was one of the first carnivore diseases to emerge as a concern for conservation, causing outbreaks that led to the near-extinction of the black-footed ferret (Mustela nigripes) in North America (Williams et al. 1988). A particular concern has been the propensity of CDV for host-switching, with outbreaks documented in a range of non-canid wildlife hosts, including seals in Lake Baikal and the Caspian Sea and several species of large felids (Terio, Craft 2013). In the Serengeti-Mara ecosystem, CDV came to prominence in 1994 following a devastating in which a third of Serengeti's lions (approximately 1,000 animals) died (Roelke-Parker et al. 1996; Kock et al. 1999). As with rabies, domestic dogs were implicated as the source of the epidemic (Cleaveland et al. 2000).

Afya Serengeti. The rationale for Afya Serengeti was therefore to establish a programme of mass dog vaccination in areas bordering the Serengeti National Park in order to prevent transmission of disease from domestic dogs to people and wildlife. Furthermore, given research findings indicating that domestic dogs are the only maintenance population for rabies in the Serengeti, the program aimed to demonstrate that the elimination of canine rabies in the Serengeti was feasible through mass dog vaccination, despite the abundance and diversity of susceptible wild carnivores within the ecosystem.

The vaccination program is implemented in ~ 160 villages adjacent to the boundaries of the Serengeti National Park, involving project teams working with local government veterinary and livestock officers from the Ministry of Livestock and Fisheries Development. Villages within the vaccination zone are visited a few days prior to the campaign to advertise the programme, with visits being made to community leaders and primary schools. Schools are extremely important because it is often the children who bring dogs to the vaccination points. Furthermore, visiting schools allows the Afya Serengeti team to provide public health information to high-risk groups about the appropriate treatment of dog bite injuries.

Vaccination stations are set up in a central village location and people bring dogs to this station for registration and vaccination. In the more dispersed and remote Maasai pastoralist communities (to the east of the Serengeti National Park), teams also need to travel to households, sometimes on foot, to reach every household.

For each dog, a record of ownership, age, name and previous vaccination history is taken, and a vaccination certificate issued. Blood samples are collected from dogs in a proportion of villages for serological monitoring of CDV infection patterns. Rabies is not easily monitored using blood samples, so a surveillance network has been established using village-based livestock officers to follow up any suspected cases of rabies reported in the village, as well as park rangers and research scientists to report suspect cases of wildlife rabies in the Serengeti National Park. Animal bite-injuries from hospital records also provide a valuable source of data for monitoring the incidence of dog rabies in communities.

The Afya Serengeti project has generated valuable information on key aspects of rabies epidemiology, including disease burden (Hampson et al. 2008), rabies transmission dynamics (Hampson et al. 2009) and reservoir dynamics (Lembo et al. 2009). The project has demonstrated not only the epidemiological and logistic feasibility of canine rabies elimination in Africa through mass dog vaccination (Lembo et al. 2010), but also that dog vaccination is a cost-effectiveness means of preventing human rabies deaths (Fitzpatrick et al. 2014) and for reducing demand for costly human vaccine for post-exposure prophylaxis (Cleaveland et al. 2003). Furthermore, these studies have contributed to a growing awareness that dog population density is not an important factor in the spread of rabies, and therefore measures used to reduce dog population density (e.g., culling) contribute little to the effective control of rabies, which can be achieved through vaccination of 70% of the dog population.

The control and elimination of canine rabies is an exemplar of a disease that demands a One Health approach, with interventions in animal populations (domestic dogs) generating health and economic benefits for the human health, veterinary and wildlife sectors. The veterinary profession has a critical role to play in implementation of mass dog vaccination campaigns, which are the mainstay of effective control of canine rabies, and could lead to elimination of the one of the world's most ancient, deadly and horrifying diseases.

Afya Serengeti has also generated important insights into the pathogenesis, epidemiology and control of CDV. Analysis of a long-term (> 20 years) serological data set using Bayesian state-space modelling has demonstrated complex transmission pathways between dogs and wildlife. In contrast to rabies, mass vaccination of domestic dogs has not prevented transmission of CDV to wildlife, however, recent infection peaks in lions have not been associated with clinical disease or mortality, in contrast to the 1994 epidemic, and it has been suggested that co-infections and other co-factors may be important determinants of CDV pathogenicity in lions (Munson et al. 2008). The study has also highlighted the importance of geographic scale in terms of CDV control measures, with small-scale dog vaccination campaigns having little effect on overall dynamics, but ecosystem-wide impacts reducing the size of outbreaks in dogs.

References

1.  Beyer HL, Hampson K, Lembo T, Cleaveland S, Haydon DT. Metapopulation dynamics of rabies and the efficacy of vaccination. In: Proceedings of the Royal Society B. 2011;278:2182–2190.

2.  Cleaveland S, Appel MGA, Chalmers WSK, Chillingworth C, Kaare M, Dye C. Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Veterinary Microbiology. 2000;72:217–227.

3.  Cleaveland S, Kaare M, Tiringa P, Mlengeya M, Barrat J. A dog rabies vaccination campaign in rural Africa: impact on the incidence of dog rabies and human dog-bite injuries. Vaccine. 2003;21:1965–1973.

4.  Fitzpatrick MC, Hampson K, Cleaveland S, Mzimbiri I, Lankester F, Lembo T, et al. Cost-effectiveness of canine vaccination to prevent human rabies in rural tanzania. Annals of Internal Medicine. 2014; 160:91–100.

5.  Knobel D, Cleaveland S, Coleman PG, Fèvre E, Meltzer MI, Miranda MEG, Shaw A, Zinsstag J, Meslin F-X. Re-evaluating the burden of rabies in Asia and Africa. Bulletin of the World Health Organization. 2005;83:360–368.

6.  Lembo T, Haydon DT, Velasco-Villa A, Rupprecht CE, Packer C, Brandoi PE, Kuzmin IV, Fooks AR, Barrat J, Cleaveland S. Molecular epidemiology identifies only a single rabies virus variant circulating in complex carnivore communities of the Serengeti. In: Proceedings of the Royal Society B. 2007;274:2123–2130.

7.  Lembo T, Hampson K, Haydon D, Dobson A, Dushoff J, Hoare R, Kaare M, Mlengeya T, Mentzel C, Cleaveland S. Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. Journal of Applied Ecology. 2008;45(4):1246–1257.

8.  Lembo T, Hampson K, et al. The feasibility of canine rabies elimination in Africa: dispelling doubts with data. PLoS Neglected Tropical Diseases. 2010;4:e626.

9.  Deaths in a Region of endemic canine rabies. PLoS Neglected Tropical Diseases. 2008;2(11):e339.

10. Hampson K, Dobson A, Kaare M, Dushoff J, Magoto M, Sindoya E, Cleaveland S. Rabies exposures, post-exposure prophylaxis and deaths in a region of endemic canine rabies. PLoS Neglected Tropical Diseases. 2008;2(11):e339.

11. Hampson K, Dushoff J, Cleaveland S, Haydon DT, Kaare M, Packer C, Dobson A. Transmission dynamics and prospects for the elimination of canine rabies. PLoS Biology. 2009;7(3):e53.

12. Kock R, Chalmers WS, Mwanzia J, Chillingworth C, Wambua J, Coleman PG, Baxendale W. Canine distemper antibodies in lions of the Masai Mara. The Veterinary Record. 1998;142(24):662–665.

13. Munson L, Terio KA, Kock R, Mlengeya T, Roelke ME, Dubovi E, Summers B, Sinclair AR, Packer C. Climate extremes promote fatal co-infections during canine distemper epidemics in African lions. PLoS One. 2008;3(6):e2545. doi:10.1371/journal.pone.0002545.

14. Roelke-Parker ME, Munson L, Packer C, Kock R, Cleaveland S, Carpenter M, O'Brien SJ, Pospischil A, Hofmann-Lehmann R, Lutz H, Mwamengele GLM, Mgasa MN, Machange GA, Summers BA, Appel MJG. A canine distemper epidemic in East African lions (Panthera leo). Nature. 1996;379:441–445.

15. Terio K, Craft ME. Canine distemper virus (CDV) in another big cat: should CDV be renamed carnivore distemper virus? MBio. 2013;4(5):e00702–00713.

16. Williams ES, Thorne ET, Appel MJ, Belitsky DW. Canine distemper in black- footed ferrets (Mustela nigripes) from Wyoming. Journal of Wildlife Diseases. 1988;24(3):385–398.

17. WHO. WHO expert consultation on rabies. Second report. WHO Technical Report Series. Geneva, Switzerland: World Health Organization; 2013;82.

18. Woodroffe R, Cleaveland S, Courtenay O, Laurenson M, Artois M. Infectious disease in the management and conservation of wild canids. In: Macdonal DW, Sillero-Zubiri C, eds. The Biology and Conservation of Wild Canids. Oxford: Oxford University Press; 2004:123–142.

  

Speaker Information
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Sarah Cleaveland, BSc, BA, VetMB, PhD, MRCVS, FRSE
Boyd Orr Centre for Population and Ecosystem Health; Institute of Biodiversity, Animal Health and Comparative Medicine
College of Medical, Veterinary and Life Sciences, University of Glasgow
Glasgow, UK


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