The potential impact of infected wildlife on public health depends thus primarily on Brucella sustainability (spillover versus reservoir host) and prevalence in a given wildlife species. Human activities related to infected wildlife species such as hunting, dressing of carcasses, meat handling, consumption, wildlife sampling and management in more intensive settings contribute to transmission of the infection. Disease control must be focused where the greatest health benefit will be attained such as has been suggested with focused spatio-temporal vaccination for foot and mouth disease in Niger44. Vaccination can only be recommended for reservoir species, not for spillover species. In the African context, only vaccination in buffalo should be considered. However, this is not an option currently as there is no vaccine available for brucellosis in wildlife45. Therefore the focus should be on vaccination in domestic animals, testing and slaughter of infected domestic animals. The spatial and temporal separation management between wildlife and livestock is a sound management practice as highlighted in the Greater Yellowstone Area, USA35.
Kruger Park buffalo blamed for Limpopo foot and mouth outbreak
Dry seasons resulting in increased densities or animals, both wild and domestic, around water sources may have a positive influence in transmission within and between species39. We found individual studies showing that proximity to wildlife reserves and porous nature of fences of wildlife reserves to be significant risk factors for brucellosis in cattle4,53. In our meta-analysis livestock contact was found to be a significant risk factor for brucellosis infection in antelope and carnivore species, but not buffalo. This suggests that buffalo may sustain B. abortus infections within infected herds without transmission from other sources. We found less evidence of publication bias for buffalo than in other species, i.e. in buffalo serological studies for Brucella spp. were likely to be published irrespective of outcome, whereas in other species there was evidence that positive serological findings were more likely to be published than negative ones. This could be due to the particular research interest in buffalo due to controlled diseases such as foot and mouth disease and tuberculosis for which they are reservoir hosts. Four of the seven studies of only buffalo were on multiple diseases, whereas all of the other 17 studies that included buffalo were only on brucellosis.
The African buffalo (Syncerus caffer) is an iconic species of South African megafauna. As the farmed buffalo population expands, the potential impacts on population health and disease transmission warrant investigation. A retrospective study of skin biopsy and necropsy samples from 429 animals was performed to assess the spectrum of conditions seen in buffaloes in South Africa. Determination of the cause of death (or euthanasia) could not be made in 33.1% (136/411) of the necropsy cases submitted due to autolysis or the absence of significant lesions in the samples submitted. Infectious and parasitic diseases accounted for 53.5% (147/275) of adult fatal cases and non-infectious conditions accounted for 34.9% (96/275). Abortions and neonatal deaths made up 11.6% (32/275) of necropsy cases. Rift Valley fever, bovine viral diarrhoea, malignant catarrhal fever, tuberculosis, bacterial pneumonia, anaesthetic deaths, cachexia and hepatotoxic lesions were the most common causes of death. The range of infectious, parasitic and non-infectious diseases to which African buffaloes were susceptible was largely similar to diseases in domestic cattle which supports concerns regarding disease transmission between the two species. The similarity between diseases experienced in both species will assist wildlife veterinarians in the diagnosis and treatment of diseases in captive African buffaloes. The present study likely does not represent accurate disease prevalence data within the source population of buffaloes, and diseases such as anthrax, brucellosis and foot and mouth disease are under-represented in this study. Hepatic ductal plate abnormalities and haemorrhagic septicaemia have not, to our knowledge, been previously reported in African buffaloes.
As the farmed buffalo population expands, the potential impacts on population health and disease transmission are important. Standard farming practices may affect disease epidemiology via artificially increased population densities, intensive nutritional management, and increased contact between buffaloes, domestic cattle, and the human population. One example that highlights the potential for disease transmission is the outbreak of bovine tuberculosis (Mycobacterium bovis) in the free-ranging buffalo population in KNP. First diagnosed in KNP buffaloes in 1990 (Bengis et al. 1996), by 1998 the prevalence of tuberculosis in buffaloes had risen to 38.2% in the southernmost region of the park (De Vos et al. 2001; Rodwell et al. 2001). Bovine tuberculosis is now considered endemic within KNP and HiP, with infection documented in many other South African wildlife species, including a variety of ruminants, carnivores and primates (Michel et al. 2006). As members of the family Bovidae, African buffaloes are susceptible to many of the same economically important infectious diseases as domestic cattle (Caron et al. 2016; Michel & Bengis 2012). Most of the published literature on diseases in buffaloes therefore describe the epidemiology and seroprevalence of infectious diseases relevant to cattle including foot and mouth disease (Thomson & Bastos 2004; Wekesa et al. 2015); arboviruses (Kading et al. 2013); Rift Valley fever (Beechler et al. 2015; Jori et al. 2015); lumpy skin disease (Fagbo, Coetzer & Venter 2014); bovine viral diarrhoea virus (BVDV) (Kabongo & Van Vuuren 2004); malignant catarrhal fever (MCF) (Pfitzer et al. 2015); tuberculosis (Kalema-Zikusoka et al. 2005; Tavalire et al. 2018); non-tuberculous mycobacteria (Gcebe et al. 2013); brucellosis (Alexander et al. 2012; Gradwell et al. 1977; Herr & Marshall 1981; Motsi et al. 2013; Tanner et al. 2014); anthrax (Cossaboom et al. 2019; De Vos & Turnbull 2004; Ebedes 1976); leptospirosis (Atherstone, Picozzi & Kalema-Zikusoka 2014); Q-fever (Ndeereh et al. 2017) and theileriosis (Chaisi et al. 2011). Parasite surveys and case reports are also recorded including infestations with coccidia (Gorsich et al. 2014); giardia (Hogan et al. 2014); ixodid ticks (Moyo, Chakuya & Sungirai 2018); haemoparasites (Eygelaar et al. 2015; Gonçalves et al. 2018; Sisson et al. 2017); nematodes (Taylor, Skinner & Boomker 2013); sarcocysts (Dubey et al. 2014; Quant et al. 1997); sarcoptes (Munang'andu et al. 2010); demodex (Dräger & Paine 1980; Wolhuter et al. 2009); schistosomes (Beechler et al. 2017); taenia (Muma et al. 2014); and thelazia (Ayebazibwe et al. 2010). Very little information is present on non-infectious conditions (Lawrence, Foggin & Prozesky 2010). Vigilant disease surveillance and studies on the interface between such diseases in cattle and buffaloes are invaluable in protecting both animal and public health as well as food security (Ritz et al. 2013). If current and future disease surveillance programmes are to be successful, it is first necessary to fully understand the range of diseases to which buffaloes are susceptible. For these reasons, a retrospective study was performed to assess the spectrum of conditions seen in African buffaloes in South Africa, and to provide a frame of reference for veterinarians, pathologists, wildlife biologists, and managers of game reserves.
Some diseases to which buffaloes are susceptible were under-represented in this study. Diseases such as anthrax, brucellosis and foot and mouth disease (FMD) are endemic in buffaloes in KNP and other locations (Cossaboom et al. 2019; De Vos & Turnbull 2004; Gradwell et al. 1977; Herr & Marshall 1981; Motsi et al. 2013; Vosloo et al. 2009) and are diagnosed by experienced field staff without submitting samples for pathological examination. In addition, the transport of samples out of FMD endemic areas to regional laboratories is restricted. Ticks, internal parasites, haemoparasites and Bartonella spp. (Gonçalves et al. 2018) were likely similarly under-represented as blood or cytology samples were rarely submitted.
Alexander, K.A., Blackburn, J.K., Vandewalle, M.E., Pesapane, R., Baipoledi, E.K. & Elzer, P.H., 2012, 'Buffalo, bush meat, and the zoonotic threat of brucellosis in Botswana', PLoS One 7(3), 1-11. [ Links ]Atherstone, C., Picozzi, K. & Kalema-Zikusoka, G., 2014, 'Seroprevalence of Leptospira hardjo in cattle and African buffaloes in south western Uganda', American Journal of Tropical Medicine and Hygiene 90(2), 288-290. -0466 [ Links ]Ayebazibwe, C., Mwiine, F.N., Tjørnehøj, K., Balinda, S.N., Muwanika, V.B., Ademun Okurut, A.R. et al., 2010, 'The role of African buffaloes (Syncerus caffer) in the maintenance of foot-and-mouth disease in Uganda', BMC Veterinary Research 6, 54. -6148-6-54 [ Links ]Beechler, B.R., Bengis, R., Swanepoel, R., Paweska, J.T., Kemp, A., Van Vuren, P.J. et al., 2015, 'Rift Valley fever in Kruger National Park: Do buffalo play a role in the inter-epidemic circulation of virus?', Transboundary and Emerging Diseases 62(1), 24-32. [ Links ]Beechler, B.R., Jolles, A.E., Budischak, S.A., Corstjens, P.L.A.M., Ezenwa, V.O., Smith, M. et al., 2017, 'Host immunity, nutrition and coinfection alter longitudinal infection patterns of schistosomes in a free ranging African buffalo population', PLoS Neglected Tropical Diseases 11(12), e0006122. [ Links ]Bengis, R., Govender, D., Lane, E., Myburgh, J., Oberholster, P., Buss, P. et al., 2016, 'Eco-epidemiological and pathological features of wildlife mortality events related to cyanobacterial bio-intoxication in the Kruger National Park, South Africa', Journal of the South African Veterinary Association 87(1), e1-e9. [ Links ]Bengis, R.G., Kriek, N.P.J., Keet, D.F., Raath, P., De Vos, V. & Huchzermeyer, H.F., 1996, 'An outbreak of bovine tuberculosis in a free-living African buffalo (Syncerus caffer-Sparrman) population in the Kruger National Park: A preliminary report', Onderstepoort Journal of Veterinary Research 63(1), 15-18. [ Links ] 2ff7e9595c
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