We conducted a cross-sectional, interviewer-administered household survey in 3 villages with access to riverbeds where hippopotamuses died: Chikwa, Chigoma, and Chimpamaba. These villages’ estimated combined population of adults >15 years of age is 6,553 (12). A questionnaire (Technical Appendix) was developed in English and translated into Senga, the local language spoken in these areas. The questionnaire was designed to complement and expand on the data initially collected in the district by local public health officials. It captured age, sex, and occupation and yes/no responses to several questions about symptoms, exposure to hippopotamuses, food sources, and whether respondents would eat meat from an animal they found dead. Those who responded that they would eat animals they found dead were asked an open-ended question to elucidate their reasons for doing so. Interviewers and supervisors were trained on procedures for conducting the survey before fieldwork commenced. Interviewers and supervisors tested questions on each other, which resulted in improvements to question wording. They also practiced administering the survey on one another before interviewing community participants.

Three teams administered the questionnaire, each team made up of a trained District Health Office staff supervisor and 6 trained volunteer interviewers. Each team was assigned to 1 of the 3 communities. Interviewers selected every fifth household they encountered in each village for inclusion and interviewed all adults >15 years of age living in selected households. No incentives were offered for participation. Interviewers read each prospective participant a description of the survey, highlighting that it was voluntary and could be stopped at any time by request. The Zambia Ministry of Health deemed this outbreak investigation to be exempt from Research Ethics Committee review. The investigation protocol was reviewed by the CDC-Zambia office and CDC’s National Center for Emerging and Zoonotic Infectious Diseases, in accordance with institutional review policies. The protocol was determined to be nonresearch under 45 CFR 46 §102(d) and therefore did not require Institutional Review Board review.

Data from completed questionnaires were entered into an Access database (Microsoft, Redmond, WA, USA) and analyzed by using Epi Info version 3.5.1 (CDC, Atlanta, GA, USA). We defined a case as illness in a respondent who reported having had anthrax infection diagnosed by a healthcare worker since July 2011 and compared demographic characteristics and risk factors by case status by using χ² and t tests. Associations were quantified with simple and multivariable logistic regression.

Figure 3

Figure 3. Hippopotamus bones and hides left behind after butchering of animals that were found dead on a river bank and later identified as the source of anthrax causing an outbreak among humans...

Figure 4

Figure 4. A dead hippopotamus floating down the South Luangwa River in northeastern Zambia during an anthrax outbreak in 2011.

The second part of the investigation involved going into the field to view 3 of the areas where most of the infected hippopotamuses were found. The site visits occurred within about a month after the outbreak and were conducted to better understand the topography and the range of the animals and to identify any additional animal species affected by anthrax. All sites were areas frequented by the exposed human populations and were <1 km from residents’ homes. The site surveys were not exhaustive; they focused on areas with known human-animal interaction (Figure 3) and recently discovered dead hippopotamuses (Figure 4). N95 masks, Tyvek suits, and rubber boots were worn during site visits when members exited vehicles. We used these observations and the results of the household-level surveys to develop recommendations to mitigate and control future spread of the infection to humans, animals, and the environment.

All 284 household members (≈4% of the population of the villages) in the 87 households selected agreed to be interviewed (mean 3 participants per household). In total, 31 (11%) of participants reported having anthrax infection diagnosed by a healthcare worker since July 2011; another 137 (48%) reported not having anthrax infection diagnosed, and 116 (41%) did not know whether they had anthrax infection diagnosed. We assumed that those who did not know did not have anthrax infection diagnosed. Male respondents accounted for 48% (n = 136) of total participants but 68% (n = 21) of those reporting having anthrax infection diagnosed, compared with 36% of cases occurring among female respondents (p<0.001) (Table 1). Of the 96 persons who answered the occupation-related question, 91 (95%) listed their occupation as farmer. This finding was not surprising given the rural setting of the outbreak. Because the responses for occupation were so homogenous, occupation was not evaluated as a risk factor. The median age of persons having received an anthrax diagnosis since July 2011 was 33 years, similar to the median age of all participants (32 years) (Table 1). The most common signs and symptoms reported by those reporting having been diagnosed with anthrax included myalgia, skin lesions, fatigue, diarrhea, and fever (Table 2).

Most participants (238 [84%]) reported having eaten hippopotamus meat at the time of the outbreak. Participants who ate the meat were 9 times (95% CI 1.3–369.3 times) more likely to report having had anthrax than those who did not eat the meat. Carrying hippopotamus meat (odds ratio 5.3, 95% CI 2.0–15.4) and preparing it for cooking (odds ratio 3.3, 95% CI 1.1–13.7) were also significantly associated with anthrax infection. After controlling for having eaten the hippopotamus meat, 3 activities (skinning, carrying, and cutting the meat) were all still significantly associated with reported anthrax infection (Table 3).

Most people surveyed (216 [76%]) reported they would not eat meat from a dead hippopotamus knowing now that it can cause anthrax infection, but 65 (23%) of all respondents and 5 (16%) of the 31 respondents in whom cases were reported said that they would eat meat from a dead hippopotamus despite this knowledge. Of the 65 participants saying they would eat the meat if given the chance again, reasons given were because they lacked other options for a side dish (“relish”) to Nshima, the maize-based staple food (44 [73%]); lacked meat (14 [22%]); suffered from hunger (4 [7%]); or lacked protein (3 [5%]), in addition to other less commonly reported reasons (Table 4).

The investigation team also visited several field sites. At 1 of the sites, previous human interaction with dead hippopotamuses was evident. Bones and hides were strewn across a large area. Evidence of multiple campfires were found in the vicinity of the hippopotamus remains (Figure 3). According to a Zambia Ministry of Health official and others on the investigation team who had visited the site earlier, the strewn animal parts appeared to have been from the initial human contact with the dead hippopotamuses. Residents appeared to stop handling dead hippopotamuses after human anthrax cases were detected and linked to contact with hippopotamus carcasses.

A large outbreak of cutaneous anthrax among humans in the Chama District of Zambia was associated with physical contact with meat from hippopotamuses that had died of anthrax, specifically skinning, carrying, or cutting the meat. Food insecurity was thought to have been the major factor driving the local population to consume meat from dead animals.

Large outbreaks affecting hippopotamus herds occurred within the Luangwa River Valley during 1987–1988 (7). Although no human infections were reported in relation to these outbreaks, positive results with low antibody titers against B. anthracis were obtained during a 1989 follow-up study from half of the subjects in a small sample of unvaccinated healthy volunteers from Luangwa River Valley villages, suggesting previous exposures in those persons through handling or consumption of meat from anthrax-infected animal carcasses (7).

Our findings are subject to a few limitations. In the household surveys, we used self-report of anthrax diagnosis to define a case; however, 41% of participants indicated they did not know whether they had received an anthrax diagnosis. We assumed that these respondents might not have understood the question and had probably not had anthrax diagnosed. Although this assumption is a limitation, it would probably bias our associations toward the null. We also had to use self-report of diagnosis rather than laboratory confirmation. However, separately some hippopotamus and human samples were confirmed in the laboratory as positive for B. anthracis, which does strengthen the epidemiologic linkage (14). Finally, slight discrepancies can be noted in the number of cases and hippopotamus deaths in this and the 2 other reports describing other aspects of the outbreak and response that have been published; specifically, the numbers of human cases vary from 511 to 521, and the numbers of hippopotamus deaths vary from 81 to 85 (14,15). This discrepancy likely illustrates the difficulty in describing events in very remote areas.

From this investigation we found that the greatest risk for having anthrax diagnosed came from carrying, skinning, or butchering hippopotamuses. This finding is consistent with other anthrax outbreaks associated with contaminated meat (11,16).

Recommendations from this investigation built on the initial response of the Zambia Ministry of Health and included community education, enhanced surveillance in human and animal populations, and resolution of food insecurities by working with governmental and nongovernmental agencies. The message to not eat meat from animals found dead was communicated at the time of the initial investigation. On the basis of survey responses indicating persons were no longer touching the meat and that carcasses were no longer being butchered, we think the messages were received and understood by the communities affected. Because the handling of the carcasses proved to be the most important risk factor for anthrax infection, future education campaigns should also focus on avoiding handling animals that have died of unknown causes. In rural Zimbabwe communities where anthrax awareness was high (71.5%) in a 2013 survey, 41% of persons surveyed reported “forgetting about anthrax,” a major reason for consuming meat from anthrax-infected animals (17). Residents should be reminded by community-based awareness campaigns or other means of the hazards of consuming meat from animals that have died of unknown causes (15).

To inform planning, wildlife authorities should identify high-risk periods and locations for naturally occurring animal outbreaks through ecologic studies that identify conditions favoring anthrax infection among animal populations (18–20). Wildlife and public health authorities should work together to ensure that community-based campaigns proactively prepare communities for possible outbreaks according to their risk profile (20). Community-based interventions should involve residents in addressing communitywide food insecurity and in educating neighbors on the hazards of consuming meat from animals that die of unknown causes (16). These interventions should begin before the dry season in outbreak-prone areas.

Questionnaire responses showed that food insecurities appear to be the primary reason for handling and consuming meat from animals found dead. Other countries in Africa have undertaken successful programs to distribute meat from trophy animals to feed communities with limited access to protein while also reducing poaching by local communities (21). Such an approach might be considered as a component of a multisectoral solution to address food insecurity and consumption of unsafe foods in Zambia.

Overall, food insecurity throughout sub-Saharan Africa has improved throughout recent years; however, hunger and malnutrition continue to be concerns in many sub-Saharan countries including Zambia. Zambia maintains a food reserve of maize, and it was suggested throughout the investigation that officials should provide additional corn meal as a possible solution for the food shortage. However, populations at risk for food insecurity need better access to balanced diets rather than more carbohydrates (22). Our survey respondents highlighted the desire for more fresh fruits and vegetables, which suggests more balanced diets would be welcomed.

Most of the crops grown in this region were cotton and other nonedible, exportable crops. Assistance is needed to help the population better balance subsistence farming with cash crops on small family farms to improve the overall diversity of crops and ultimately mitigate the risk for food insecurity (22).

Our household survey aimed to determine the main risk factors for anthrax transmission and the underlying factors driving those infected to risk exposure. Our results suggest the need to address long-standing political and economic issues related to food insecurity in protected areas, as well as an urgent need for better coordination between wildlife management and public health authorities. A more proactive approach could help prevent future outbreaks.