Our epidemiologic, laboratory, and environmental investigations confirmed the existence of anthrax outbreaks in livestock populations in three Ugandan districts that reported human outbreaks. The outbreak in Arua District appeared to have been long-standing and continuous, at least dating back to 2016, whereas the outbreaks in Kiruhura and Kween districts appeared to have been smaller and more recent. Outbreaks in all three districts were associated with butchering dead livestock that died of suspected anthrax on/near the pastureland, and improper disposal of livestock carcasses. However, additional risk factors also differed to some extent between the districts: the Arua outbreak was associated with grazing livestock near the Nile River bank, the Kiruhura outbreak was associated with the construction of dams (not shown on the map), and the Kween outbreak was associated with having livestock pastureland close to a wildlife migration route.
Our findings of increased risk of livestock outbreaks after suspected anthrax-infected livestock were butchered on or disposed of on the pastureland are consistent with other studies (12,18,26). Due to the long survival time of anthrax spores, a contaminated carcass can serve as a continuous source of infections for livestock in the surrounding area. Thus, an area that has substantial numbers of anthrax cases among livestock, such as Arua District during our study period, may face difficulty ending an outbreak if proper carcass disposal practices are not consistently followed. Proper carcass disposal involves digging a six-foot-deep hole for burial, in which the uppermost part of the carcass is ≥ 3 feet below the original ground level. All the material around the carcass, including bedding, feed, and surrounding soil contaminated by the carcass are also put into the hole, followed by surface area disinfection with 10% formaldehyde. In Arua District in particular, the large number of suspected cases during 2016 may have served as sources of infection for the subsequent cases in 2017 and 2018. Because we did not assess cases beyond July 2018, it is not known if cases continued during that period.
Furthermore, in Arua District, grazing near the Nile riverbank during a drought was also associated with anthrax outbreaks. During drought, many livestock trek long distances and congregate at the Nile riverbank for pasture and water. It is possible that one animal could have died near the riverbank and contaminated the pastureland, making it a source of more widespread infections. The presence of carcasses in common areas where livestock mix widely – not just on their own pastureland – should be a signal to herders to avoid the area.
Our findings also indicated that anthrax exposures leading to the 2018 outbreaks in Kiruhura and Kween might have been fairly recent: although Kiruhura District has reported outbreaks previously (12), none had occurred during the past two years. However, during January 2018, a new dam was constructed in Kiruhura District, near pastureland. Digging of dams typically involves high levels of soil turnover, which can liberate buried anthrax spores (27). These spores could subsequently have contaminated the pastureland and served as sources of infection for both wildlife and domestic livestock in Kiruhura. The link between wildlife migration routes and infection observed in Kween District has also been demonstrated previously: other studies in Kenya and Tanzania have reported anthrax outbreaks at the human-livestock and livestock-wildlife interfaces (28,29). The reported introduction of livestock from Kenya to graze in Kween during the 2017 drought could also have served as a potential source of infections. During that time period, there was an ongoing anthrax outbreak in the region of origin in Kenya (28). It is possible that livestock coming in from Kenya during that time period died of anthrax in Uganda; however, that remains unconfirmed.
In our study, cattle were more affected than goats and sheep. This is consistent with studies in both Kenya and China that identified cattle as being more affected by anthrax than goats and sheep (26,28). Cattle ingest a large amount of soil from the ground when grazing, while goats typically browse on grass only; this may lead to higher levels of exposure among cattle, compared with goats. This characteristic is thought to be a major factor associated with different levels of infection among different species (9). Interestingly, the attack rates among male livestock were more than twice as high as among female livestock, and more than six times higher among domestic than imported livestock. The reasons for this are unknown, but may relate to the ways in which livestock ingest the spores during grazing or browsing, or variation in lethal doses among livestock (9).
Reported anthrax outbreaks among humans occurred concurrently with or subsequent to the start of the livestock outbreaks. Interestingly, in Arua district, human anthrax cases were not reported during 2016 or the first half of 2017, despite the deaths of many suspected case-livestock during this time. Indeed, in April 2016 alone, more than 200 livestock died of suspected anthrax in Arua. The reason for the lack of reported human cases during this time is unclear. It is possible that human cases – and, possibly, deaths – simply went unrecognized or unreported. It is also possible that at least some of the livestock deaths were due to other causes, or were due to anthrax but were not followed by human anthrax cases. Improved laboratory capacity to diagnose anthrax would facilitate improved understanding of the dynamics between livestock and human anthrax in Uganda.
Vaccination is generally considered a cost-effective prevention method for anthrax among livestock, and, as a result, among humans (4,16,17,30,31). Although farmers reported using antibiotic prophylaxis during outbreaks (with a protective outcome for their livestock), none of the case-kraals were reportedly vaccinated against anthrax. This finding suggests a possible opportunity to promote routine annual vaccination in Uganda. Studies evaluating the cost-effectiveness of vaccination may help guide policy decisions
In 2017, anthrax was categorized as the most important of seven priority zoonoses in Uganda (33), and in June 2019, a national symposium was held to enhance One Health efforts to combat anthrax in Uganda. The symposium included: i) sharing of up-to-date spatial and temporal data on anthrax outbreaks in both livestock and humans in Uganda; ii) validating the national anthrax control strategy; iii) forming a National Anthrax Prevention and Control Technical Working Group (NAPCTWG) and iv) developing a roadmap for National Anthrax Prevention and Control Technical Working Group. Part of validating the national anthrax control strategy involved determining the best approaches to livestock vaccination, and filling the gaps in laboratory capacity. At the time of writing this paper, only the National Livestock Reference Laboratory and Uganda Virus Research Institute laboratory were able to confirm anthrax in Uganda. In addition, although One Health is recognized as a priority in Uganda, there are still gaps in implementing a harmonized approach to anthrax outbreaks. For example, as soon as the human anthrax outbreaks were reported, both the human anthrax and livestock anthrax could have been investigated together rather than separately. Indeed, the recognition by either human or livestock health staff of an anthrax outbreak should trigger notification to the corresponding human or livestock health counterpart, to enable coordination of investigations and concerted efforts towards effective interventions. Future efforts in Uganda should focus on these issues as the country improves its approach to combating anthrax.
Our investigation had several limitations. Given that anthrax-infected livestock die suddenly, it is possible that livestock that may have died of anthrax in more rural areas went unnoticed. Additionally, some farmers may have failed to notice the absence of some members of their herd due to their large herd size. Failure to account for all anthrax-related livestock deaths in the area may have resulted in an underestimation of the scope of the outbreak. In addition, only a small subset of reported livestock deaths were tested, due to lack of available specimens and testing materials. Therefore, some of the suspected anthrax deaths might have been deaths due to other etiologies, and some anthrax deaths may have been unidentified.