This was the first study looking at percentage of Brucella spp. positive samples in wildlife involving more than one national park in Uganda. In this study, the overall percentage of positive Brucella samples was 31.1% in the four major national parks. This is higher than the percentage of 2% recorded in wildlife in Queen Elizabeth National Park (19). The percentage in wildlife in this current study is also higher than that recorded in livestock in Uganda (17,20). What is interesting in this study is that parks such as Kidepo Valley National Park, and Murchison Falls National Park that have relatively low livestock-wildlife interaction had far higher percentage of positive samples than Lake Mburo and Queen Elizabeth National Parks which have a very close livestock-wildlife interaction.
Among the national parks studied, Kidepo Valley National Park had the highest percentage of positive samples at 55.9%. This percentage is higher than the 9.2% percentage recorded in cattle in Karamoja where the national park is situated (27). It is not clear what the source of brucellosis in Kidepo National Park may be. The park is located in north east Uganda, a very remote area that has been characterized by insecurity for a long time (28). There is less information available on the disease burden for the region. The veterinary extension services in the region have been almost non-existent with people relying on ethno-medicine to control cattle diseases (29). Frequent cattle incursion in the park, especially during long dry spells, in search of water and pasture is a big opportunity for sustained infection in wildlife and cattle. It is therefore not surprising to find that a disease like brucellosis may have found a suitable niche. According Serrano et al. (2), brucellosis is well maintained in wildlife when interventions to control the disease in livestock are poor. Areas around Kidepo Valley and Murchison Falls National Park have been recovering from the effects of Lords Resistance Army war which hindered agricultural extension services delivery in the region (30). Although the percentage of positive samples in wildlife is higher than in cattle in the areas surrounding these national parks (17,20), the direction of spread of brucellosis across wildlife and livestock is not clear and needs to be investigated. We did not detect any positives in the elephant or bushbuck samples, this agrees with previous studies that have not detected brucellosis in these animals (13).
The buffaloes in the four national parks sampled in Uganda had high s percentage of positive samples of 48.6% compared to the 2% previously reported by Kalema-Zikusoka et al. (19) in Queen Elizabeth National Park. The rise in percentage of positive samples could be due to increased interactions with cattle infected with brucellosis at the wildlife interface. However, as percentage of positive samples did not vary much between the four national parks and there were differences between the national parks in terms of cattle interaction this could suggest that buffaloes play a role as a reservoir species. These findings are consistent with results from other studies conducted elsewhere in east and southern Africa by Motsi et al. (11) Alexander et al. (13) and Waghela and Karstad (10) that showed a higher percentage in wildlife. It is believed that buffaloes harbor Brucella better than other species for reasons not well understood (11). Buffaloes are gregarious animals and usually live in big herds. Herd size has a big effect on the transmission of brucellosis (31). According to Dobson and Meagher (31), brucellosis is well maintained in herd sizes of greater than 200 individual animals per herd. The disease prevalence tends to be high in big herds because the small inter-animal distance helps to sustain transmission by contact (32). Therefore, herd sizes like those in Kidepo National Park (around 6,900 buffaloes) are likely to maintain infection for a very long time without showing any impact on the population.
Four out of six lions sampled were positive. This was the highest percentage of positive samples of all the wildlife in this study. However, it is difficult to conclude if this is representative of Brucella infection in lions due to the small sample size tested in the current study. They have been few previous studies investigating Brucella seropositivity in lions. However, a study in Tanzania did find one positive lion out of two tested (12). During field sample collection for the current study, one typical clinical case of brucellosis in lions was encountered. The affected lion had hygroma around joints and was always reluctant to move (Robert Aruho, Personal observation). This lion was positive in this study. From the observations in the field, lions usually choose prey on which they will not spend a lot of energy to hunt. Clinically, sick animals affected by brucellosis usually develop mobility challenges because of dysfunctional joints and usually tend to move behind the herds. This makes the animals, such as buffaloes, easy prey by predators especially the lions which thrive best at hunting solitary prey (33). Lions might also seroconvert due to exposure to Brucella through feeding on such infected animals. Previous work had shown that lions may become immune to Trypanosoma brucei rhodesiense infections due to being exposed to parasites through consumption of infected meat (34). Such a scenario could be responsible for high percentage of Brucella spp. positive samples in lions of Kidepo Valley National Park. According to Uganda Wildlife Authority in 2018, the lion population in Kidepo Valley National Park was about 132 individuals. We tested a few individuals compared to the population size. Therefore, this calls for more studies to be undertaken in this lion population of Kidepo Valley National Park and other national parks to determine the extent of infection and its impact on lion populations.
This is the first study of Brucella percentage of positive samples in Uganda kob. The percentage of positive samples in Uganda kob (11.1%) was higher than that observed in other medium sized antelopes such as impala (1.4%) in similar ranging conditions in Zimbabwe (11) and black lechwe (Kobus leche smithemani) (0%) in Zambia (35). The percentage in the Uganda kob was lower than that found in Kafue lechwe (Kobus leche kafuensis) which was estimated at 42.9% (35). In this case, the higher prevalence in the Kafue lechwe was related to interaction with positive cattle and infection might now be endemic within the antelope population. Positives in Uganda kob could be due to fact that Uganda kob are found in areas where they are likely to interact with livestock. Uganda kob are most likely to be taken for bushmeat. In Uganda, bushmeat consumption especially along major transit routes is becoming a serious threat to public health (22). However, there is insufficient data on the trends of bushmeat consumption in Uganda but studies within the East African region indicating increasing incidences of bushmeat consumption in East Africa with antelopes being the most preferred source of bushmeat (36,37). This high percentage observed in Uganda kob could result in several human cases of infection unless mitigation measures are put in place to deter entry of bushmeat into the human food chain.
Several studies have detected positives in African giraffe populations and in this study, giraffes had the third highest percentage of positive samples of 31.7% in this study. The percentage of positive samples in giraffes in Uganda is higher than in other African giraffe range states such as Botswana and Zimbabwe that had prevalence values of 11% and 3.7% respectively (13,38). Although there is no evidence of bushmeat consumption of giraffe meat in Uganda, there has been a notable increase on the number of snaring cases of giraffes in Murchison Falls National Park (39). In the majority of the cases, snaring in Uganda is closely associated with bushmeat consumption (40).
Brucellosis has been recorded in domestic equids as far early 1970s. Study in wild equids have been very limited (41). In our study only one out of the 25 tested zebra was positive (4%). There have not been many studies investigating brucellosis in zebra. Assenga et al (12) found no positives in the two animals they sampled in Tanzania and Alexander et al. (13) found no positives in 21 zebras from Botswana. The only study where positives were found were in what was Rhodesia in the 1960s, where 24% of 50 tested animals were positive (42)
Recently, the Uganda Wildlife Authority launched ambitious plans to restock several protected areas with wildlife especially with those species that are threatened or pose a considerable human-wildlife conflict (43,44). Recently, Uganda translocated several giraffes from Murchison Falls National Park to Lake Mburo National Park and other areas (39,45). A study by Caron et al. (46) shows that movement of wildlife provides a conduit for the spread of disease to new susceptible populations. Therefore, interventions that involve movement of wildlife present a considerable risk of disease spread to other new areas (47). This calls for regular screening of wildlife before undertaking translocations.
This study capitalized on using the archived wildlife samples that were already collected during the previous disease surveillance in the four major national parks. This affected the sample size and the sampling strategy that could be used to collect samples and therefore could have let to over- or under-estimating of the percentage of positive samples. Archived samples were used because the cost of sample collection in wildlife is prohibitive (48). It involves purchase of immobilization drugs and requires experienced veterinary expertise to immobilize wildlife. Secondly, the ethical justification of the immobilization of wildlife to collect samples requires a lot of explanation because of the risk involved. Therefore, this may be one of the most available opportunities to determine percentage of positive samples in wildlife. All the national parks have some form of livestock-wildlife interaction. However, this study did not determine the level of interaction, in which location and how the interaction occurs. These reasons limited this study to use only available archived samples. Therefore, the results of the study will apply only to those parks and species sampled. In future, as samples for study of brucellosis are being collected, concurrent samples could be collected from livestock. In addition, geographical position system could be used to collect information on location and possible interaction between wildlife and livestock
In this study, we utilized Rose Bengal plate test (RBPT) to analyze percentage of positive samples in the wildlife samples. In African buffaloes the sensitivity and specificity of RBPT has been estimated as 98.6% and 99.2% respectively (49). However, validation in other wildlife species has not been carried out. This may have led to some false positives and false negatives. Future studies should consider using more specific and sensitive tests such as polymerase chain reaction.