Domestic dogs are the only population essential for persistence of rabies in Serengeti

Lembo, T., Hampson, K., Haydon, D. T., Craft, M., Dobson, A., Dushoff, J., ... & Mentzel, C. (2008). Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. Journal of Applied Ecology, 45(4), 1246-1257.

1. Knowledge of infection reservoir dynamics is critical for effective disease control, but identifying reservoirs of multi-host pathogens is challenging. Here, we synthesize several lines of evidence to investigate rabies reservoirs in complex carnivore communities of the Serengeti ecological region in northwest Tanzania, where the disease has been confirmed in 12 carnivore species.
2. Long-term monitoring data suggest that rabies persists in high-density domestic dog Canis familiaris populations (> 11 dogs/km²) and occurs less frequently in lower-density (< 5 dogs /km²) populations and only sporadically in wild carnivores.
3. Genetic data show that a single rabies virus variant belonging to the group of southern Africa canid-associated viruses (Africa 1b) circulates among a range of species, with no evidence of species-specific virus–host associations.
4. Within-species transmission was more frequently inferred from high-resolution epidemiological data than between-species transmission. Incidence patterns indicate that spill-over of rabies from domestic dog populations sometimes initiates short-lived chains of transmission in other carnivores.
5. Synthesis and applications. The balance of evidence suggests that the reservoir of rabies in the Serengeti ecosystem is a complex multi-host community where domestic dogs are the only population essential for persistence, although other carnivores contribute to the reservoir as non-maintenance populations. Control programmes that target domestic dog populations should therefore have the greatest impact on reducing the risk of infection in all other species including humans, livestock and endangered wildlife populations, but transmission in other species may increase the level of vaccination coverage in domestic dog populations necessary to eliminate rabies.

Distemper outbreak and its effect on African wild dog conservation

van de Bildt, M., Kuiken, T., Visee, A. M., Lema, S., Fitzjohn, A. R., & Osterhaus, A. (2002). Distemper outbreak and its effect on African wild dog conservation. Emerging Infectious Diseases (Print),8(2), 211-213.


In December 2000, an infectious disease spread through a captive breeding group of African wild dogs (Lycaon pictus) in Tanzania, killing 49 of 52 animals within 2 months. The causative agent was identified as Canine distemper virus (CDV) by means of histologic examination, virus isolation, reverse transcriptase-polymerase chain reaction analysis, and nucleotide sequencing. This report emphasizes the importance of adequate protection against infectious diseases for the successful outcome of captive breeding programs of endangered species.

Fatal canine distemper infection in a pack of African wild dogs in the Serengeti

Goller, K. V., Fyumagwa, R. D., Nikolin, V., East, M. L., Kilewo, M., Speck, S., ... & Wibbelt, G. (2010). Fatal canine distemper infection in a pack of African wild dogs in the Serengeti ecosystem, Tanzania. Veterinary microbiology, 146(3), 245-252.

In 2007, disease related mortality occurred in one African wild dog (Lycaon pictus) pack close to the north-eastern boundary of the Serengeti National Park, Tanzania. Histopathological examination of tissues from six animals revealed that the main pathologic changes comprised interstitial pneumonia and suppurative to necrotizing bronchopneumonia. Respiratory epithelial cells contained numerous eosinophilic intracytoplasmic inclusion bodies and multiple syncytial cells were found throughout the parenchymal tissue, both reacting clearly positive with antibodies against canine distemper virus (CDV) antigen. Phylogenetic analysis based on a 388 nucleotide (nt) fragment of the CDV phosphoprotein (P) gene revealed that the pack was infected with a CDV variant most closely related to Tanzanian variants, including those obtained in 1994 during a CDV epidemic in the Serengeti National Park and from captive African wild dogs in the Mkomazi Game Reserve in 2000. Phylogenetic analysis of a 335-nt fragment of the fusion (F) gene confirmed that the pack in 2007 was infected with a variant most closely related to one variant from 1994 during the epidemic in the Serengeti National Park from which a comparable fragment is available. Screening of tissue samples for concurrent infections revealed evidence of canine parvovirus, Streptococcus equi subsp. ruminatorum and Hepatozoon sp. No evidence of infection with Babesia sp. or rabies virus was found. Possible implications of concurrent infections are discussed. This is the first molecular characterisation of CDV in free-ranging African wild dogs and only the third confirmed case of fatal CDV infection in a free-ranging pack.

Genetics of CDV in East African carnivores

Carpenter, M. A., Appel, M. J., Roelke-Parker, M. E., Munson, L., Hofer, H., East, M., & O'Brien, S. J. (1998). Genetic characterization of canine distemper virus in Serengeti carnivores. Veterinary immunology and immunopathology, 65(2), 259-266.

The lion (Panthera leo) population in the Serengeti ecosystem was recently afflicted by a fatal epidemic involving neurological disease, encephalitis and pneumonia. The cause was identified as canine distemper virus (CDV). Several other species in the Serengeti were also affected. This report presents CDV H and P gene sequences isolated from Serengeti lions (Panthera leo), spotted hyenas (Crocuta crocuta), bat-eared fox (Otocyon megalotis) and domestic dog (Canis familiaris). Sequence analyses demonstrated that the four Serengeti species carry closely related CDV isolates which are genetically distinct from other CDV isolates from various species and locations. The results are consistent with the conclusions that: (1) a particularly virulent strain of CDV emerged among Serengeti carnivores within the last few years; (2) that strain has recognizable shared-derived (synapomorphic) genetic differences in both H and P genes when compared to CDV from other parts of the world; and (3) that the CDV strain has frequently crossed host species among Serengeti carnivores.

A CDV epidemic in Serengeti

Roelke-Parker, M. E., Munson, L., Packer, C., Kock, R., Cleaveland, S., Carpenter, M., ... & Mwamengele, G. L. (1996). A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature, 379(6564), 441-445.

CANINE distemper virus (CDV) is thought to have caused several fatal epidemics in canids within the Serengeti–Mara ecosystem of East Africa, affecting silver-backed jackals (Canis mesomelas) and bat-eared foxes (Otocyon megalotis) in 1978 (ref. 1), and African wild dogs (Lycaon pictus) in 1991 (refs 2, 3). The large, closely monitored Serengeti lion population4,5 was not affected in these epidemics. However, an epidemic caused by a morbillivirus closely related to CDV emerged abruptly in the lion population of the Serengeti National Park, Tanzania, in early 1994, resulting in fatal neurological disease characterized by grand mal seizures and myoclonus; the lions that died had encephalitis and pneumonia. Here we report the identification of CDV from these lions, and the close phylogenetic relationship between CDV isolates from lions and domestic dogs. By August 1994, 85% of the Serengeti lion population had anti-CDV antibodies, and the epidemic spread north to lions in the Maasai Mara National reserve, Kenya, and uncounted hyaenas, bat-eared foxes, and leopards were also affected.

Evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife

Cleaveland, S., Appel, M. G. J., Chalmers, W. S. K., Chillingworth, C., Kaare, M., & Dye, C. (2000). Serological and demographic evidence for domestic dogs as a source of canine distemper virus infection for Serengeti wildlife. Veterinary microbiology, 72(3), 217-227.

Following an epidemic of canine distemper virus (CDV) in Serengeti lions in 1994, the role of domestic dogs in the epidemiology of the disease was investigated by serological and demographic analyses. From 1992 to 1994, data were collected from two domestic dog populations bordering the Serengeti National Park. Several lines of evidence indicated that patterns of CDV infection differed significantly between higher-density dog populations of Serengeti District to the west of the park and lower-density populations of Ngorongoro District to the south-east: (a) CDV age-seroprevalence patterns differed significantly between years in Ngorongoro District populations but not in Serengeti District populations; (b) CDV seropositive pups (<12 months of age) were detected in Ngorongoro District only in 1994, whereas a proportion of pups in Serengeti District were seropositive in each year of the study; (c) in Ngorongoro District, the proportion of deaths attributed to disease was significantly higher in 1994 than in 1993, whereas in Serengeti District, there was no significant difference in disease-related mortality between years; (d) in Ngorongoro District, significantly more CDV seronegative dogs than seropositive dogs died in 1994, whereas there was no difference in survival of CDV seropositives and seronegatives between years in Serengeti District. We concluded that, between 1992 and 1994, CDV persisted in higher-density dog populations of Serengeti District, but occurred only sporadically in lower-density Ngorongoro District populations. Data from Ngorongoro District are consistent with exposure of dogs to CDV in 1991 and 1994, but not in 1992 and 1993. These findings suggest that higher-density domestic dog populations to the west of the Serengeti National Park were a more likely source of CDV infection for wildlife during 1994 than lower-density pastoralist dogs to the south and east of the park.

Eliminating Rabies in Tanzania?

Bardosh, K., Sambo, M., Sikana, L., Hampson, K., & Welburn, S. C. (2014). Eliminating Rabies in Tanzania? Local Understandings and Responses to Mass Dog Vaccination in Kilombero and Ulanga Districts. PLOS Neglected Tropical Diseases, 8(6), e2935.

Background

With increased global attention to neglected diseases, there has been a resurgence of interest in eliminating rabies from developing countries through mass dog vaccination. Tanzania recently embarked on an ambitious programme to repeatedly vaccinate dogs in 28 districts. To understand community perceptions and responses to this programme, we conducted an anthropological study exploring the relationships between dogs, society, geography and project implementation in the districts of Kilombero and Ulanga, Southern Tanzania.

Methodology/Principal Findings

Over three months in 2012, we combined the use of focus groups, semi-structured interviews, a household questionnaire and a population-based survey. Willingness to participate in vaccination was mediated by fear of rabies, high medical treatment costs and the threat of dog culling, as well as broader notions of social responsibility. However, differences between town, rural and (agro-) pastoralist populations in livelihood patterns and dog ownership impacted coverage in ways that were not well incorporated into project planning. Coverage in six selected villages was estimated at 25%, well below official estimates. A variety of problems with campaign mobilisation, timing, the location of central points, equipment and staff, and project organisation created barriers to community compliance. Resource-limitations and institutional norms limited the ability for district staff to adapt implementation strategies.

Conclusions and Significance

In the shadows of resource and institutional limitations in the veterinary sector in Africa, top-down interventions for neglected zoonotic diseases likes rabies need to more explicitly engage with project organisation, capacity and community participation. Greater attention to navigating local realities in planning and implementation is essential to ensuring that rabies, and other neglected diseases, are controlled sustainably.

Author Summary

Mass vaccination of dogs is the most effective strategy to eliminate dog-mediated human rabies from developing countries. In 2009, a large-scale elimination demonstration project was funded and coordinated by the Bill and Melinda Gates Foundation (BMGF) and the World Health Organisation (WHO) in three southern countries, including the United Republic of Tanzania. This paper explores community perceptions and responses to this programme in the districts of Kilombero and Ulanga, Southern Tanzania. The study was based on focus groups and interviews in 16 villages as well as a household questionnaire (n = 113), a population-based survey (n = 6,157 households) and key informant interviews (n = 24). The study showed that fear of rabies, the threat of dog culling and broader ideas of community responsibility drove compliance. However differences in local livelihoods shaped dog ownership patterns and the distribution of dogs in ways that were not explicitly addressed by project strategies. A survey in six villages found that only 25% of dogs had been vaccinated in 2011. We discuss the operational constraints and problems that lowered coverage as viewed by different actors at the district and village-level. A more explicit engagement with project organisation, capacity and community involvement are needed to address this low coverage.

Rabies vaccination in rural Tanzania

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

Despite the availability of safe and effective rabies vaccines, the incidence of dog rabies has been increasing throughout much of sub-Saharan Africa. Here we describe a vaccination strategy that has resulted in successful control of rabies in a rural dog population of Northwestern Tanzania. From October 1996 to February 2001, four central-point dog vaccination campaigns were conducted in villages within Serengeti District with a mean interval between campaigns of 338, 319 and 456 days. Vaccination coverage of the dog population was estimated from household questionnaires as 64.5, 61.1, 70.6 and 73.7% following each of the four campaigns, respectively. The incidence of dog rabies declined significantly in Serengeti District falling by 70% after the first campaign and by 97% after the second campaign. Over the same period, the incidence of dog rabies did not differ significantly in unvaccinated control villages of Musoma District. The incidence
of human bite injuries from suspected rabid dogs declined significantly in Serengeti District after dog vaccination but not in adjacent unvaccinated districts. Vaccination of 60–70% of dogs has been sufficient to control dog rabies in this area and to significantly reduce demand for human post-exposure rabies treatment. Dog-bite injuries can provide a valuable and accessible source of data for surveillance in countries where case incidence data are difficult to obtain.

Rabies in Tanzania / Rabia en Tanzania

Cleaveland,S., E.M. Fèvre, M. Kaare & P.G. Coleman. 2002. Estimating human rabies mortality in the United Republic of Tanzania from dog bite injuries. Bulletin of the World Health Organization, 80: 304-310.


Objective: To make quantitative predictions about the magnitude of underreporting of human rabies deaths in the United Republic of Tanzania.
Methods: Human rabies deaths were estimated by using a series of probability steps to calculate the likelihood of rabies developing
after the bite of a suspected rabid dog, incorporating field data on the incidence of animal bite injuries, the accuracy of rabies
recognition, the distribution of bite wounds, and post-exposure treatment.
Findings: Predicted human rabies mortality was estimated to be (a) 1499 deaths per year (95% confidence interval 891–2238),
equivalent to an annual incidence of 4.9 (2.9–7.2) deaths/100 000, when active surveillance data on bite incidence were used, and
(b) 193 deaths per year (32–409), corresponding to an annual incidence of 0.62 (0.1–1.32) deaths/100 000, when national bite
statistics were used. The annual mean number of rabies deaths officially recorded for the same period was 10.8 (7.7–14.0).
Conclusion: In the United Republic of Tanzania, cases of rabies in humans have been greatly underreported. Dog bite injuries are an accessible source of epidemiological data that may be used to estimate the public health burden of rabies and to monitor epidemiological trends in developing countries.

Estimación de la mortalidad por rabia humana causada por mordeduras de perro en la República Unida de Tanzanıa.

Objetivo: Hacer predicciones cuantitativas sobre la magnitud de la subnotificación de las defunciones por rabia humana en la República Unida de Tanzania.
Métodos: Se estimó la mortalidad por rabia humana usando una serie de pasos probabilísticos para calcular el riesgo de desarrollar rabia tras la mordedura de un perro presuntamente rabioso; a ese fin, se incorporaron datos de campo sobre la incidencia de mordeduras, la precisión del diagnóstico de la rabia, la distribución de las mordeduras y el tratamiento posterior a la exposición.
Resultados: Según las predicciones efectuadas, usando los datos aportados por la vigilancia activa de las mordeduras la mortalidad ascendía a (a) 1499 defunciones al año (intervalo de confianza (IC) 95%: 891–2238), lo que equivale a una incidencia anual de 4,9 (2,9–7,2) defunciones/100 000; al emplear las estadísticas nacionales sobre mordeduras, en cambio, se obtenían 193 defunciones anuales (32–409), lo que se traduce en una incidencia anual de 0,62 (0,1–1,32) defunciones /100 000. La media anual oficial para el mismo periodo fue de 10,8 (7,7–14,0) muertes por rabia.
Conclusión: En la República Unida de Tanzania, la notificación de los casos de rabia humana ha estado muy por debajo de las cifras reales. La información sobre las lesiones por mordedura de perro es una fuente accesible de datos epidemiológicos que pueden utilizarse para estimar la carga de salud pública que supone la rabia y para vigilar las tendencias epidemiológicas en los países en desarrollo.