The authors have declared that no competing interests exist.
Zoonotic diseases pose a significant health challenge at the human–wildlife interface, especially in Sub-Saharan Africa where ecosystem services contribute significantly to local livelihoods and individual well-being. In Uganda, the fragmented forests of Hoima district, form part of a “biodiversity and emerging infectious disease hotspot” composed of communities with high dependency on these wildlife protected areas, unaware of the associated health risks. We conducted a cross-sectional mixed methods study from March to May 2017 and interviewed 370 respondents, using a semi-structured questionnaire from eight villages neighbouring forest fragments in Hoima District, Uganda. Additionally, a total of ten (10) focus group discussions (FGDs) consisting of 6–10 men or women were conducted to further explore the drivers of hunting and perception of zoonotic disease risks at community level. Qualitative and quantitative data were analysed using content analysis and STATA version 12 respectively. We found twenty-nine percent (29.0%, CI: 24.4–33.9) of respondents were engaged in hunting of wildlife such as chimpanzee (
Zoonotic diseases are increasingly becoming an emerging public health threat, partially due to the risk of spillover events at the human-wildlife interface. This cross -sectional study was carried out among high-risk communities around forest fragments of Hoima District, Uganda, to describe activities that could lead to disease spillover in humans in order to inform public health practitioners of the potential risks at community level for preparedness and response efforts. The study also sought to gain an understanding of the community’s perception of the risk of zoonotic diseases, what activities could expose them to zoonoses, and whether the healthcare services are adequate to identify such diseases at community level. We found that most people were not aware of zoonotic diseases transmissible from wildlife to humans and this can partly be explained by lack of information filtering through to the grass root. It is important to note however, that the interaction between wildlife and humans, is largely driven by communities’ struggle to survive and meet their livelihood needs making it difficult to predict under what circumstances disease could emerge in the community. We need to remind ourselves that all major outbreaks have started at community level and well as the health experts are fast to diagnose the disease in question, some communities are hearing these diseases for the very first time. Quite often these outbreaks are putting the available alternative livelihood in question and demanding for quick unstainable changes that communities are quick to abandon once the outbreaks are over. We recommend that this is the time to invest in health education and create awareness about zoonotic diseases among communities at the human-wildlife interface. Health promotion and or livelihood-based intervention programs should use existing evidence and case studies implemented in collaboration with government agencies and partners.
All relevant data are within the manuscript.
Wildlife are known to be common reservoirs for some infectious diseases transmissible to humans [
Uganda’s vulnerability to climate change has been highlighted and is.bound to increase because many livelihood are dependent on natural resources [
There is a close link between emerging infectious disease spillover to humans and deforestation, biodiversity loss and forest invasions [
Human activities like encroachment on wildlife habitat for agriculture purpose has been highlighted as a risk of zoonotic transmission from wildlife to humans, for example, degradation that may result in higher contact within existing habitat or cause significant migration of wildlife out of the degraded environments into human settlements [
All participants provided informed consent. Ethics approval was obtained from School of Biomedical Sciences Institutional Review Board of Makerere University (SB-HDREC-412), University of Minnesota (STUDY00000469) and research permit issued by Uganda National Council of Science and Technology (UNCST HS2200). Written and oral informed consent was obtained from all participants. In some cases, willing participants were unable to sign because they were unable to read and write in which case oral consent was obtained. Oral consent was documented by; recording date and time of the interview on the consent form, indicating on the consent form “participant consented orally" in the space where the participant would have signed, interviewer and witness signing the consent form in their space. Both consent processes were approved by IRB and UNCST. Furthermore, local community approval was obtained from Hoima district local government and local village leaders.
The study was carried out in the sub counties of Kitoba and Kiziranfumbi. Kitoba sub-county has a total 34,810 human population, land area of 195.5 square kilometers and population density of 344 persons per square kilometer of land area. Kiziranfumbi has a population of 35,814, land area of 223.3 square kilometers and population density of 345 persons per square kilometer of land area. Overall, Hoima is ranked among the top ten most heavily populated districts of Uganda (population 572,986), of which 81.5% live in rural areas (
To infer potential risk of exposure to wildlife-associated zoonotic diseases, a cross-sectional ethnographic mixed-method study was undertaken to describe the interface between wildlife and people in and around forest fragments in Hoima district. Data were collected from eight rural communities (villages) located within 1-2km of forest fragments in two sub-counties (Kitoba and Kiziranfumbi) (
Within fragments, villages were selected based on reports from the local vermin control office, which represent a higher level of human-wildlife contact or conflict (ranging from crop raids to human attacks). A semi-structured questionnaire was administered using face-to-face interviews to 370 participants (46 respondents per village) from eight villages. Within villages, participants were randomly selected with the goal of a male: female ratio of approximately 1:1. The number of total participants was derived using a list of household provided by the local leader and using formula = RANDBETWEEN(1,60)) to generate household random numbers in Microsoft Excel version 2016. To further explore communities perception on human-wildlife interaction, a total of ten (10) focus group discussions (FGDs) consisting of 6–10 men or women were conducted. Inclusion criteria for focus group participation included: use of forest services like hunting, fetching of firewood, water, and agriculture and timber harvest, willingness to participate and resident of the village.
Focus group discussions were conducted in a local language (
Quantitative data was collected using services of trained interviewers using face to face semi- structured questionnaire that included information on socio-demographic factors, activities that characterize human-wildlife interaction, knowledge and practices regarding zoonotic disease and existence/use of healthcare services (availability of health centers within 15km).
The translator transcribed recordings to word transcripts in Microsoft Word. This was checked by employing a second person from the team of interviewers who together with the first author, listened to the recordings while reading the word transcripts to ensure that that transcripts were a true recording of the FGDs Transcripts were analyzed using content analysis by coding, categorizing of related codes and identification of themes. To ensure that coding and resulting patterns reflected the experience of the interviewees, the first author together with translator reviewed the coded documents in Microsoft Word. Validity of the data was established through maintaining an audit trail of audiotapes, field notes, participant observation, translator making a follow up call to an interviewee identified during FGD session and use of analysis memos written during the coding process. The unit of analysis was the group and units of coding were phrases, sentences or paragraphs. Two broad themes related to the aim of the study emerged “human-wildlife interaction” and “health”.
Quantitative survey data was collected and cleaned using EpiData 3.0 and analyzed using Stata version 12 (StataCorp LP). Descriptive statistics on demographic characteristics of respondents were summarized using frequencies and percentages. Pearson chi-square test was used to find if there was a significant association among the independent variables taking the location as dependent variable and their significance levels at 95% level of confidence. Binary logistic regression was used to analyze the factors associated with illness after consumption of bush meat. At bivariate level, crude odds ratios (cOR) and their p-values with a statistical significance of 0.05 are presented to measure the association between each independent and dependent variable. The independent variables included Sex, age groups, household size, knowledge of diseases transmitted by wild animals to human, ever heard of Ebola or Marburg, mostly frequently hunted animals and Number of people involved in preparation of hunted animals. The dependent variable was defined as a person feeling unwell after consumption of bushmeat, transmitting a similar condition to other household members and or presenting himself or herself for medical care after consumption of bush meat.
At multivariate level, independent variables with p-values less than 0.5 at bi-variate level were included in the regression model and after adjusting for confounding, adjusted odds, ratios (aOR) and their p-values are presented. Using forward selection of variables, model was built using a step-wise procedure for selecting independent variables by adding and removing variables from the model until a good simple model was obtained. The model fit was assessed using log-likelihood chi-square and the stepwise model selection was done manually.
Two major themes emerged from the focus group discussions; human-wildlife interaction and health. Increased interaction of humans with wildlife occurs (content and context) within boundaries of several livelihood activities and this includes encroachment on forest reserves for crop farming and human settlement. Settlement around forest patches was found to be motivated by easily accessible resources like firewood, local weaving material, hunting and water. Wildlife on the other hand, also infringe upon human settlement to forage and through sharing of open water sources (rivers and wells) and fruits, providing an intersection where both humans and wild animals often interact. Occasionally there are attacks on humans by wildlife at these intersections.
“We share fruits like mangoes with monkeys. We even find them on the road and at wells. Snakes bite people. Baboons bit someone and they escaped. I think the person annoyed them or something like that. Wild pig bit me 7 years ago and the site itches me up to now. A chimpanzee slapped someone. Am telling you we have lived and have suffered with these animals, but this is where we live” (Women’s’ FGD Kaigo)
Most commonly hunted and consumed wild animals in the community included edible cane rats (
The animals we eat are cane rats (emisu), bushbucks (ensa) and other antelopes. They bring roasted meat and you may never know what it is. We get wild meat from hunters. They bring it in and say this is such and such meat. When it is roasted, you eat straight away. Sometimes we try to put in groundnuts. They sometimes bring fresh meat. There is a man who always brings in fresh antelope meat. It is common and there are people who eat it daily. It is common if you have money and are interested you can’t take a week without eating it. It is just lovely; it is more delicious and increases after preparing (Women’s FGD Kibanjwa).
However, other wildlife types in addition to those consumed, are also hunted for various reasons contributing to persistent hunting behavior in these communities. Participants described different ways wildlife and wildlife parts are used as shown in
Wild animal | Quotes from FGDs |
---|---|
Edible cane rats ( | |
Colobus monkeys | |
Porcupine ( | Porcupine pins [are used]to prick on swollen breasts (mastitis) to cure them |
Some communities had to say why they continued hunting
” In hunting, we give security for our gardens. When you eat game meat you gain your immunity. In hunting you even do exercise”. (Men’s FGD Rwemisaga)
Most respondents discussed that there were strange diseases, with fever and diarrhea as the main symptoms in the community. The majority could not explain whether these diseases were related to close contact with wildlife; in part, due to the fact that there is no linkage between health testing services and wildlife interaction at health facilities
In some cases, people mentioned that diseases like Ebola, Brucellosis, Tuberculosis (TB) and Rabies are spread from animals in rather unsure ways.
“I have suffered Brucellosis; another woman went as far as Kampala due to Brucellosis and jiggers from pigs. People can also get rabies say when you are bitten by squirrels, eating half cooked pork, eating monkeys all have been said that can cause disease although we have not had any serious disease that has caused death of many people but who knows these diseases don’t announce when they are coming. Their only announcement is when you wake up and people are falling sick one after another and you don’t know why” (Women’s FGD Kaigo)
Although there are heath centers within the area, communities feel that the healthcare services are not adequate; drugs not enough, long waiting hours and health workers rarely ask about any possible contact with wildlife or even domestic animals. Consequently, communities’ use traditional means to treat diseases when the illness is suspected to be as results of contact with wildlife. This method only offers temporary relief, leading to persistent ill health or death among those affected.
“Some people go to health centers; others use herbs the one who provided herb for rabies died. Herbs are just what we use because we do not have alternative. Even when you go to hospital, they will just give you Panadol after staying there for the whole day. We prevent diseases by avoiding interaction or going to infected people, following advice staying clean using, mosquito nets, prevention measures found in healthy centers, observing what is necessary and you do, on radio, in workshops”
A total of 370 individuals were interviewed (response rate 96.1%, 370/385). Majority of the respondents were selected from Kiziranfumbi sub-county (51.6%). The percentage of men and women who participated in the study was 56.6% and 43.8% respectively. Education level of respondents was low, with only 18.7% having attained a secondary education and 19.5% having not attended school. Less than a half (40.8%) of those interviewed lived in permanent housing and the majority (80.8%) were married. The majority (54.1%) of respondents were 36 years of age and above. Majority of respondents were Catholics and Protestants (46.2% each) with Muslims forming a small proportion (2.2%).
Respondents reported increased interaction with wildlife at the forest edge (n = 179, 48.5%) and maize was the crop most commonly shared among humans and wildlife 80% (n = 295). Almost half of the respondents (n = 162, 43.8%) reported sorting and using leftovers from wildlife as food. Respondents reported staying in houses with poor ventilation (n = 174, 47.0%) and most people (n = 317, 88.1%) had bats and rats in their houses. Also, 33% (n = 122) of the respondents used open water sources that they shared with wildlife. The majority of respondents (n = 302, 81.6%) neither treated nor boiled water before drinking.
Overall, respondents participated in hunting and or consumption of wildlife. Majority of respondents (64.7%, CI: 59.6–69.6) agreed that hunted meat is shared with the community, while 29% (CI: 24.4–33.9) of the respondents’ hunted non-human primates such as monkeys and baboons, 45.8% (CI: 40.6–51.0) hunted (edible) rodents. According to 55.3% (CI: 50.1–60.4) of the respondents, search for animal protein is the main reason why communities hunt, followed by cultural practices and medicinal use (22.7%, CI: 18.6–27.4). Consumption of bush-meat is practiced and 7.9% (CI: 5.3–11.1) of the respondents had a self-reported history of falling sick after bush meat consumption; 10.9% (CI: 6.3–17.4) and 68.6% (CI: 60.1–76.2) of respondents reported occurrence of illness within the past year and last month respectively. About five percent (5.3% CI: 2.60–9.60) of respondents who fell sick reported that some family members also showed similar signs at that time. Generally, respondents were less aware (37.0%, CI: 32.1–42.2) of diseases transmissible from wildlife to humans even though majority (88.7%, CI: 85.0–92.0) had heard of Ebola or Marburg (see
Characteristic(s) | Response | Location | Chi-Sq.(P-Value) | |||||
---|---|---|---|---|---|---|---|---|
Kitoba (N) | % (95% CI) | Kiziranfumbi (N) | % (CI) | Overall (N) | % (CI) | |||
Fall sick | Yes | 10 | 34.5 (19.6–53.2) | 19 | 65.5 (46.8–80.4) | 29 | 7.9 (5.3–11.1) | 2.48 (0.289) |
No | 169 | 49.7 (44.4–55.0) | 171 | 50.3 (45.0–55.6) | 340 | 92.1 (88.9–94.7) | ||
Duration of occurrence | Years back | 5 | 33.3 (14.6–59.5) | 10 | 66.7 (40.5–85.4) | 15 | 10.9 (6.3–17.4) | |
Months back | 63 | 67.0 (56.9–75.8) | 31 | 33.0 (24.2–43.1) | 94 | 68.6 (60.1–76.2) | ||
Can’t recall | 10 | 10.7 (3.5–28.5) | 25 | 89.3 (71.5–96.5) | 28 | 20.4 (14.0–28.2) | ||
Similar signs in some family members | Yes | 1 | 10 (1.4–46.9) | 9 | 90 (53.1–98.6) | 10 | 5.3 (2.60–9.60) | |
No | 78 | 44.1 (36.9–51.5) | 99 | 55.9 (48.5–63.1) | 177 | 94.7 (90.4–97.4) | ||
Aware of wildlife diseases transmissible to humans | Yes | 59 | 43.1 (35.0–51.5) | 78 | 56.9 (48.5–65.0) | 137 | 37 (32.1–42.2) | |
No | 118 | 53.2 (46.6–59.6) | 104 | 46.8 (40.4–53.4) | 222 | 60 (54.8–65.0) | ||
Unknown | 2 | 18.2 (4.6–50.8) | 9 | 81.8 (49.2–95.4) | 11 | 3 (1.5–5.3) | ||
Heard of Ebola and or Marburg | Yes | 155 | 47.3 (41.9–52.7) | 173 | 52.7 (47.3–58.1) | 328 | 88.7 (85.0–92.0) | 3.29 (0.193) |
No | 23 | 60.5 (44.4–74.7) | 15 | 39.5 (25.3–55.6) | 38 | 10.3 (7.4–13.8) | ||
Unknown | 1 | 25.0 (3.3–76.4) | 3 | 75.0 (23.6–96.7) | 4 | 1.1 (0.3–2.7) | ||
Areas where interaction with wildlife is more common | Forest edge | 75 | 41.9 (3.5–49.3) | 104 | 58.1 (50.7–65.1) | 179 | 48.5 (44.3–53.7) | |
Forest interior | 65 | 61.3 (51.7–70.1) | 41 | 38.7 (29.9–48.2) | 106 | 28.7 (24.2–33.6) | ||
Surrounding bush around household | 37 | 50.0 (38.8–61.2) | 37 | 50 (38.8–61.2) | 74 | 20.1 (16.1–24.5) | ||
Not recorded | 2 | 20.0 (5.0–54.2) | 8 | 80 (45.8–95.0) | 10 | 2.7 (1.3–4.9) | ||
Human grown food shared with wild animals | Maize | 147 | 49.8 (44.1–55.5) | 148 | 50.2 (44.5–55.9) | 80 | 80.0 (75.5–83.9) | |
Sugarcane | 12 | 70.6 (45.7–87.2) | 5 | 29.4 (12.8–54.3) | 4.6 | 4.6 (2.7–7.3) | ||
Cassava | 8 | 33.3 (17.6–53.9) | 16 | 66.7 (46.0–82.4) | 6.5 | 6.5 (4.2–9.5) | ||
Others | 7 | 29.2 (14.5–49.9) | 17 | 70.8 (50.1–85.5) | 6.5 | 6.5 (4.2–9.5) | ||
None | 5 | 55.6 (25.0–82.4) | 4 | 44.4 (17.6–74.9) | 2.5 | 2.4 (1.1–4.6) | ||
How are left over from wild animals treated | Chopped and buried | 5 | 17.2 (7.3–35.40) | 24 | 82.7 (64.6–92.7) | 37 | 10.0 (7.2–13.6) | |
Sort and use as food | 82 | 50.6 (42.9–58.3) | 80 | 49.4 (41.7–57.1) | 162 | 43.9 (38.8–49.1) | ||
Leave them to rot in the garden | 80 | 55.6 (47.3–63.5) | 64 | 44.4 (36.5–52.7) | 144 | 39.0 (34.0–44.2) | ||
Others | 9 | 34.6 (19.5–54.3) | 17 | 65.4 (45.6–80.9) | 26 | 7.0 (4.6–10.2) | ||
Not recorded | 3 | 37.5 (12.5–71.6) | 6 | 62.5 (28.4–87.5) | 9 | 2.4 (1.1–4.6) | ||
Has any member of family ever been attacked by wild animals | Yes | 27 | 48.9 (43.3–54.5) | 29 | 51.1 (45.5–56.7) | 56 | 15.1 (11.6–19.2) | 1.13(0.57) |
No | 150 | 48.2 (35.5–61.20 | 157 | 51.8 (38.8–64.5) | 307 | 83.0 (78.8–86.7) | ||
Non response | 2 | 28.6 (7.2–67.5) | 5 | 71.4 (32.5–92.8) | 7 | 1.9 (0.8–3.9) | ||
Is hunted meat shared in the community | Yes | 125 | 53.0 (46.6–59.3) | 111 | 47.0 (40.7–53.4) | 236 | 64.7 (59.6–69.6) | 5.61(0.061) |
No | 53 | 41.1 (32.9–49.8) | 76 | 58.9 (50.2–67.1) | 129 | 35.0 (30.1–40.1) | ||
Non response | 1 | 25.0 (3.3–76.4) | 3 | 75.0 (23.6–96.7) | 4 | 1.1 (0.3–2.7) | ||
Most frequently hunted animals | Non-human primates | 48 | 44.9 (35.7–54.4) | 59 | 55.1 (45.6–64.3) | 107 | 29.0 (24.4–33.9) | 9.09(0.059) |
Edible rodents | 80 | 47.3 (39.9–54.9) | 89 | 52.7 (45.1–60.1) | 169 | 45.8 (40.6–51.0) | ||
Wild ruminants | 33 | 67.3 (53.1–78.9) | 16 | 32.6 (21.0–46.9) | 49 | 13.3 (10.0–17.2) | ||
Others | 1 | 25 (3.3–76.3) | 3 | 75.0 (23.6–96.7) | 4 | 1.1 (0.3–2.7) | ||
None response | 17 | 42.5 (28.3–58.1) | 23 | 57.5 (41.9–71.7) | 40 | 10.8 (7.8–14.5) | ||
Reason for hunting | Cultural/Medical purpose | 47 | 55.9 (45.2–66.2) | 37 | 44.0 (33.8–54.8) | 84 | 22.7 (18.6–27.4) | |
Protein source | 106 | 51.9 (45.1–58.7) | 98 | 48.1 (41.2–54.9) | 204 | 55.3 (50.1–60.4) | ||
Others | 6 | 17.1 (7.9–33.3) | 29 | 82.9 (66.7–92.1) | 35 | 9.5 (6.7–12.9) | ||
Non response | 20 | 43.5 (30.0–58.0) | 26 | 56.5 (42.0–70.0) | 46 | 12.5 (9.3–16.3) | ||
Number of people involved in preparation of hunted animals | 1–3 People | 83 | 63.8 (55.2–71.7) | 47 | 36.2 (28.3–44.8) | 130 | 35.2 (30.4–40.3) | |
4–7 People | 37 | 44.0 (33.8–54.8) | 47 | 56.0 (45.2–66.2) | 84 | 22.8 (18.6–27.4) | ||
Above 7 people | 33 | 37.5 (28.0–48.1) | 55 | 62.5 (51.9–72.0) | 88 | 23.8 (19.6–28.5) | ||
Non response | 26 | 38.8 (29.7–50.9) | 41 | 61.2 (49.1–72.1) | 67 | 18.2 (14.3–22.5) |
The factors associated with falling sick after eating Bushmeat among communities around forests fragments of Hoima were analyzed using binary logistic regression model both at bivariate and multivariable levels. Bivariate results in
Characteristic(s) | Crude analysis | Adjusted analysis | |||||
---|---|---|---|---|---|---|---|
Categories | cOR | 95% CI | P-value | aOR | 95% CI | P-value | |
Sex | Female | 1 | |||||
Male | 1.3 | 0.6–2.9 | 0.49 | ||||
Age Groups | <25 years | 1 | 1 | ||||
25–35 years | 1.9 | 0.4–9.4 | 0.419 | 2.1 | 0.4–11.0 | 0.377 | |
36+ years | 2.7 | 0.6–11.8 | 0.197 | 3 | 0.6–14.2 | 0.171 | |
Household Size | 1–3 | 1 | 1 | ||||
4–7 | 0.5 | 0.2–1.3 | 0.156 | 0.5 | 0.2–1.2 | 0.124 | |
8+ | 0.7 | 0.2–2.1 | 0.525 | 0.6 | 0.2–1.9 | 0.359 | |
Know of any diseases transmitted by wild animals to human | Yes | 1 | |||||
No | 0.6 | 0.3–1.3 | 0.222 | ||||
Non-response | 1 | ||||||
Ever heard of Ebola or Marburg | Yes | 1 | |||||
No | 0.6 | 0.1–2.7 | 0.532 | ||||
Mostly frequently hunted animals | Non-human primates | 1 | 1 | ||||
Edible rodents | 0.4 | 0.1–0.9 | 0.029 | 0.5 | 0.2–1.4 | 0.183 | |
Wild ruminants | 0.7 | 0.2–2.1 | 0.474 | 1.1 | 0.3–4.4 | 0.92 | |
Others | 3.6 | 0.3–42.3 | 0.312 | 3.1 | 0.2–44.6 | 0.406 | |
Non-response | 0.6 | 0.2–2.4 | 0.493 | 0.5 | 0.1–3.0 | 0.475 | |
Number of people involved in preparation of hunted animals | 1–3 People | 1 | |||||
4–7 People | 0.8 | 0.2–3.2 | 0.729 | 0.7 | 0.2–3.3 | 0.697 | |
Above 7 People | 3.6 | 1.3–9.7 | 0.014 | 2.9 | 0.8–9.7 | 0.091 |
cOR = Crude Odds Ratio; aOR = Adjusted Odds Ratio, CI = Confidence interval (at 95%)
However, none of the factors was independently associated with falling sick after consumption of bushmeat in the multivariate analysis after adjusting for confounding. This underscores the role of multiple factors leading to human illness after consumption of bushmeat and a summary of potential factors has been provided in
This study focused on understanding and describing the nature of interaction between humans and wildlife around the forest fragments of Hoima and its potential for zoonotic disease spillover to humans. Additionally, the study also explored whether humans understand the health risk associated with this constant interaction with wildlife. Results from this study reveal increased community sharing of resources (crops, fruits and water) with wildlife driven by survival needs of the people and wildlife alike as their habitats range continue to shrink due to human encroachment. Studies have highlighted that as the forest fragments become farmland, there has been a dietary change of wildlife to agriculture crops further increasing conflict between human and wildlife [
Respondents talked about persistent behaviors like hunting, bushmeat consumption and the use of wild animals’ parts as long time practices. These practices have been adopted in part to cope with challenges in life but there is also a strong sense of pride, cultural and community attachment to these practices despite the associated health risks. Studies have also shown that poor rural communities have been forced into circumstances of high human-wildlife contact due to poverty and a struggle to survive, exposing them to diseases [
Important to note is that there is a higher likelihood of acquiring wildlife related diseases when seven or more people are involved as compared to less people probably because of the time spend on the carcass. Studies have shown exposure to blood or other secretions during hunting and butchering of bushmeat or through bites and scratches from wild animals are considered a primary risk factor for a broad spectrum of other zoonotic disease transmission to humans [
Respondents from studied communities had limited understanding of the risk of zoonotic disease transmission from wildlife to humans. For example, 63% of respondents did not understand that Ebola or Marburg is associated with people coming into close contact with wildlife like Chimpanzees. Additionally, 43.8% of respondents reported regular consumption of leftovers from wildlife crop raids as food. Communities reported adapting to eating other wild animals (bushmeat) that they never used to eat before like squirrels because of the profound belief that bushmeat is medicinal. Interaction with rodents, bats and other wildlife are a long-standing feature of life in these landscapes and rodents are routinely hunted and consumed but also found in gardens of most respondents. An earlier study done in Hoima, recommends alternative viable livelihood and educational outreaches as means to promote co-existence between human and wildlife [
Communities acknowledge that clinical care and even diagnostic investigations are poor and most cases of ill health will resolve on their own. Research has shown that most zoonotic diseases remain neglected because of the lack of adequate diagnostic laboratory services and the fragmented collection of data that cannot be used to inform any recommendations [
Overall, findings suggest that knowledge about zoonoses is not adequately filtering down to the communities to impact human behaviors regarding wildlife interaction, despite awareness about the existence of specific zoonoses like Ebola. This is a reflection of the international and national focus and investment in certain diseases of public health concern and the neglect of endemic zoonotic diseases that significantly contribute to the disease burden in these communities. This also has implications for zoonotic disease spread and highlights the extent to which education and dissemination of information can mitigate future outbreaks of such zoonotic diseases [
The results from this study suggest that there is interaction between humans and wildlife among communities at the human wildlife interface in Hoima. This interaction is largely driven by human needs and creates a potential threat for disease spillover to humans due to persistent hunting-bushmeat activities. This is further complicated by communities’ lack of awareness of the health risk associated with close wildlife interaction and inadequate health care services. This therefore calls for concerted efforts among government agencies and partners to work with the communities and create adequate awareness about zoonotic diseases of wildlife origin. These findings will be shared with the local government of Hoima and at different scientific meetings to highlight some of the key cultural issues defining the risk of disease transmission along the human-wildlife interface in an area of high biodiversity and potential strategies to address this risk.
We are grateful to Conservation and Ecosystem Health Alliance and Hoima district local government for their support towards field work.
Dear Dr. Namusisi:
Thank you very much for submitting your manuscript "Zoonotic disease risk in South-Western Uganda: characterizing the human-wildlife interface in a biodiversity hot spot" (#PNTD-D-19-01184) for review by PLOS Neglected Tropical Diseases. Your manuscript was fully evaluated at the editorial level and by independent peer reviewers. The reviewers appreciated the attention to an important problem, but raised some substantial concerns about the manuscript as it currently stands. These issues must be addressed before we would be willing to consider a revised version of your study. We cannot, of course, promise publication at that time.
We therefore ask you to modify the manuscript according to the review recommendations before we can consider your manuscript for acceptance. Your revisions should address the specific points made by each reviewer.
When you are ready to resubmit, please be prepared to upload the following:
(1) A letter containing a detailed list of your responses to the review comments and a description of the changes you have made in the manuscript.
(2) Two versions of the manuscript: one with either highlights or tracked changes denoting where the text has been changed (uploaded as a "Revised Article with Changes Highlighted" file); the other a clean version (uploaded as the article file).
(3) If available, a striking still image (a new image if one is available or an existing one from within your manuscript). If your manuscript is accepted for publication, this image may be featured on our website. Images should ideally be high resolution, eye-catching, single panel images; where one is available, please use 'add file' at the time of resubmission and select 'striking image' as the file type.
Please provide a short caption, including credits, uploaded as a separate "Other" file. If your image is from someone other than yourself, please ensure that the artist has read and agreed to the terms and conditions of the Creative Commons Attribution License at
(4) If applicable, we encourage you to add a list of accession numbers/ID numbers for genes and proteins mentioned in the text (these should be listed as a paragraph at the end of the manuscript). You can supply accession numbers for any database, so long as the database is publicly accessible and stable. Examples include LocusLink and SwissProt.
(5) To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see
Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.
While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool,
We hope to receive your revised manuscript by Dec 06 2019 11:59PM. If you anticipate any delay in its return, we ask that you let us know the expected resubmission date by replying to this email.
To submit a revision, go to
Sincerely,
Charles Apperson
Guest Editor
PLOS Neglected Tropical Diseases
Bruce Lee
Deputy Editor
PLOS Neglected Tropical Diseases
***********************
Reviewer's Responses to Questions
As you describe the new analyses required for acceptance, please consider the following:
-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?
-Is the study design appropriate to address the stated objectives?
-Is the population clearly described and appropriate for the hypothesis being tested?
-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?
-Were correct statistical analysis used to support conclusions?
-Are there concerns about ethical or regulatory requirements being met?
Reviewer #1: See comments above on summary section. The choice of qualitative and quantitative seems appropriate for the objective of the study, but overall methods are insufficiently explained.
Reviewer #2: (No Response)
Reviewer #3: Field methods may be appropriate. See additional comments below.
Study design is fine for what they wish to report.
Characterizing the actual disease risk w/o a known response (specific disease) that can be attributable to zoonoses is not possible in this study. There is no pathogen or serological testing and reported disease is limited. Recommend revising title.
--------------------
-Does the analysis presented match the analysis plan?
-Are the results clearly and completely presented?
-Are the figures (Tables, Images) of sufficient quality for clarity?
Reviewer #1: See comments on summary section. Some analysis are mentioned but not reported in results.
Reviewer #2: (No Response)
Reviewer #3: See additional notes re: interpreting 95% CI for ORs
Tables will need editorial assistance.
Need 95% CI for proportions where applicable.
--------------------
-Are the conclusions supported by the data presented?
-Are the limitations of analysis clearly described?
-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?
-Is public health relevance addressed?
Reviewer #1: Adequate
Reviewer #2: (No Response)
Reviewer #3: See additional notes re: interpreting 95% CI for ORs
--------------------
Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.
Reviewer #1: (No Response)
Reviewer #2: (No Response)
Reviewer #3: See summary and general comments
--------------------
Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.
Reviewer #1: The paper provides an overview of the nature of interaction between humans and wildlife around the forest fragments of Hoima in Uganda, as well as the level of knowledge of the community regarding the risk associated with wildlife interactions. Although the study is not particularly novel or unique, it provides an interesting summary of the challenges and types of interactions in the human-wildlife interface. Some sections of the papers need to be heavily edited and clarified. For example, the introduction needs to be written. It was numerous sentences that are unclear or repetitive. Similarly, the section on quantitative analysis is insufficient to understand what was done. It seems like the models were univariate, but multivariate methods are mentioned on results, but not described.
Specific comments:
L69-71: The sentence is unclear, are 60 % of the infectious diseases zoonotic in origin?
L78-89: Rephrase the sentence, e.g. “The burden of infectious diseases is particularly high in Sub-Saharan Africa. In addition, poor communities are disproportionally affected by climate and environmental changes that further drive the emergence of infectious diseases. “
L85: Spell out EBOV and DRC
L88: Missing reference
L88-L90: Rephrase: “forest fragments are inhabited by a mobile population of about 5000 chimpanzees that move within and between forest-farm habitats, causing increased conflict with human farming communities”
L92-L101: Sentences are duplicated.
L388: “Having more than seven people involved in preparation of hunted animals had a higher risk associated with sickness (cOR=3.6, 95% CI=1.3-9.7) compared to involving 1-3 people” this is the only significant cOR. It should be discussed.
L140-41: Are the number of villages and forest fragment equally represented, how are both related (1 to 1)?
L179: Were 10 FGD per village? That would give you 80m which then it should give you more than the 370 individuals indicated above.
L211-220: Description of the logistic models is inadequate.
L233: what kind of risks are perceived by the communities
Table 1 should also summarize the most frequent hunted animals and all uses.
Recall bias is going to play a role in this study
Where are the multivariate results?
Discussion is well-written but overall it provides little reference back to the results.
Reviewer #2: (No Response)
Reviewer #3: This study is a cross-sectional, mixed methods study based on a “face to face” administered (semi-structured) questionnaire about zoonotic disease and risk behaviors in Uganda. This study has some merit, but the manuscript needs additional editorial work and some major revisions by the authors.
Oxford comma, line 34 (After Minnesota)
Statements (Line 36-38) read as if they are presented as facts. They are participant impressions. There should be clear language stating such –or perhaps the judicious use of quotes.
In abstract, and throughout manuscript, please include confidence intervals for proportions/percentages so that the reader can infer certainty based on sample size.
Line 44: Sentence needs revision.
Line 46: “fora” changed to “for a”
Line 47: missing word (? campaigns) after education
Line 59: “less aware” suggests a comparison … consider other word choice
Line 63: “sensitized” should be defined here or consider other word choice
Line 64: Consider removing “Hoima” here and add “agencies” or “officials” after government
Line 78: Sentence needs revision (? Edit as “…is considered to have the highest burden…”)
Line 85: EBOV should be defined [Review author guidelines re: abbreviations]
Line 88: Missing reference
Line 140: Remove extra “.”
Line 157: How were household randomized?
Line 161: Change “10focus” to “10 focus”
Line 161: Add space after “(FGDs)”
Line 170: Consider “We used the services of a local…”
Line 184: add comma after “humans”
Line 185: Was consent obtained?
Line 195 and throughout: Does “Runyoro” need to be italicized
Line 200: Please expand on analysis methods for qualitative data analysis
Line 202: Consider “Validity” en lieu of “Trustworthiness”
Note: the manuscript needs editorial assistance. Missing articles and typographical errors abound in this draft. I am not making additional basic edits/suggestions beyond line 202.
Data analysis: An odds ratio is not the same as a relative risk. The statements that include “times at risk” need to be revised (or the data analysis should include relative risk). Furthermore, if the 95% CI contains 1, then it isn’t significant. Thus, most of the reported OR in lines 327-339 are NOT significant. Thus, inference should be limited as it isn’t supported by data.
Data tables and images are mixed within the manuscript text. Recommend that authors conform to standard author guidelines. Manuscript sections and headings are not standardized. Review guidelines.
Conclusions state that there is increasing interaction between humans and wildlife based on the study. No clear evidence was provided for this. The discussion and conclusions need significant editorial assistance.
References are not in standard format. Need to revise many to the standard format.
--------------------
PLOS authors have the option to publish the peer review history of their article (
If you choose “no”, your identity will remain anonymous but your review may still be made public.
Reviewer #1: No
Reviewer #2: No
Reviewer #3: No
Submitted filename:
Click here for additional data file.
Dear Dr. Namusisi: We have received your revised manuscript, including your responses to the reviewers' comments and concerns. The reviewers recommended that your manuscript required a major revision before it would be suitable for publication. They made numerous comments and provided extensive suggestions for improving your manuscript. We find that your response to these comments and concerns is not adequate. Accordingly, we are requesting that you address each review separately and provide a response to each point raised by each reviewer. Once we have received a more comprehensive response to the reviews, we will send your revised manuscript out for review.
Thank you for your patience in the process and for your interest in publishing in PLoS Neglected Tropical Diseases.
Sincerely yours,
Charles S. Apperson
Guest Editor
We cannot make any decision about publication until we have seen the revised manuscript and your response to the reviewers' comments. Your revised manuscript is also likely to be sent to reviewers for further evaluation.
When you are ready to resubmit, please upload the following:
[1] A letter containing a detailed list of your responses to the review comments and a description of the changes you have made in the manuscript. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.
[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).
Important additional instructions are given below your reviewer comments.
Please prepare and submit your revised manuscript within 60 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email. Please note that revised manuscripts received after the 60-day due date may require evaluation and peer review similar to newly submitted manuscripts.
Thank you again for your submission. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.
Sincerely,
Charles Apperson
Guest Editor
PLOS Neglected Tropical Diseases
Bruce Lee
Deputy Editor
PLOS Neglected Tropical Diseases
***********************
Dear Dr. Namusisi: We have received your revised manuscript, including your responses to the reviewers' comments and concerns. The reviewers recommended that your manuscript required a major revision before it would be suitable for publication. They made numerous comments and provided extensive suggestions for improving your manuscript. We find that your response to these comments and concerns is not adequate. Accordingly, we are requesting that you address each review separately and provide a response to each point raised by each reviewer. Once we have received a more comprehensive response to the reviews, we will send your revised manuscript out for review.
Thank you for your patience in the process and for your interest in publishing in PLoS Neglected Tropical Diseases.
Sincerely yours,
Charles S. Apperson
Guest Editor
Figure Files:
While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool,
Data Requirements:
Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example see here:
Reproducibility:
To enhance the reproducibility of your results, PLOS recommends that you deposit laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see
Dear Dr. Namusisi,
Thank you very much for submitting your manuscript "A descriptive study of zoonotic disease risk at the human-wildlife interface in a biodiversity hot spot in South Western Uganda" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you modify the manuscript according to the review recommendations.
Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.
When you are ready to resubmit, please upload the following:
[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript.
Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out
[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).
Important additional instructions are given below your reviewer comments.
Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.
Sincerely,
Charles Apperson
Guest Editor
PLOS Neglected Tropical Diseases
Bruce Lee
Deputy Editor
PLOS Neglected Tropical Diseases
***********************
Reviewer's Responses to Questions
As you describe the new analyses required for acceptance, please consider the following:
-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?
-Is the study design appropriate to address the stated objectives?
-Is the population clearly described and appropriate for the hypothesis being tested?
-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?
-Were correct statistical analysis used to support conclusions?
-Are there concerns about ethical or regulatory requirements being met?
Reviewer #1: In general methods are appropriate and the population clearly defined.
Reviewer #2: (No Response)
Reviewer #3: Objectives are generally clearly described.
Recommend (line 230) additional description of what "data cleaned' means.
Sample sizes are impressive and likely provide sufficient power to address comparative questions.
I do have some concerns over the interpretations of the odds ratios. (see comments in results/conclusions critiques below)
--------------------
-Does the analysis presented match the analysis plan?
-Are the results clearly and completely presented?
-Are the figures (Tables, Images) of sufficient quality for clarity?
Reviewer #1: Yes, mostly negative results
Reviewer #2: (No Response)
Reviewer #3: Some formatting issues (likely PDF) for figure 2. Other figures/tables are clear. line 373 references table 4, but should be table 3 (no table 4 is provided)
The cORs are not appropriately interpreted with the given 95%CI. For example (Line 373) the authors stated that men are 1.3 times more likely to get sick: since this is an odds ratio, that is an incorrect interpretation -- ORs are not the same as risk ratios. In addition, in multiple places, OR data is presented with accompanying 95% CIs that have an interval that includes "1" -- thus the authors should not conclude there is a difference. These issues must be addressed before publication
--------------------
-Are the conclusions supported by the data presented?
-Are the limitations of analysis clearly described?
-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?
-Is public health relevance addressed?
Reviewer #1: Limited conclusions given the lack of conclusive results.
Reviewer #2: (No Response)
Reviewer #3: Recommend reviewing how to interpret ORs:
--------------------
Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.
Reviewer #1: L27: remove comma after district
L125: delete ‘of’ and replace ‘has’ for ‘have’
L127: Full stop after humans. Delete for example and edit the next sentence as follows: “Degradation results in higher contact within existing habitat and causes significant migration of wildlife out of the degraded environments into human settlements.”
L129: What activities? Please specify.
L132: Finish the list (a), b)…).
L215: Rephrase sentence: “The translator transcribed recordings to English.
L218: Delete that
L241: Do you mean p-value less than 0.05?
Table 2, provide label for the last CI
L440-L441: Unclear what the point of the sentence is.
Reviewer #2: (No Response)
Reviewer #3: Still some typos, but the manuscript is greatly improved. The cOR interpretation must be edited for clarity and statistical accuracy.
--------------------
Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.
Reviewer #1: The study is mostly descriptive in nature with negative results, but this version is improved and addresses most previous comments reviewer.
Reviewer #2: The authors provide a much-improved version of the manuscript. I appreciate the attention to my previous major comments, which I think have increased the clarity of the work. I do have three other additional major comments, as well as a series of minor/grammatical comments, which I think will help convey the message more clearly. In addition, I encourage the authors to correct punctuation issues such as inconsistent/multiple spacing and use/exclusion of commas, which I have not commented on specifically.
Reviewer #3: The authors have a solid study that is original and adds to the body of knowledge about spillover risk in Uganda based on cultural practices and place. The work is important and has relevance beyond an academic readership -- thus should be of interest to practitioners in multiple fields. Field methods appear sound although I seek clarity about what "data cleaning" actually means. Statistical methods are appropriate, but need some work with interpreting cORs.
--------------------
PLOS authors have the option to publish the peer review history of their article (
If you choose “no”, your identity will remain anonymous but your review may still be made public.
Reviewer #1: No
Reviewer #2: No
Reviewer #3: No
Figure Files:
While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool,
Data Requirements:
Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example see here:
Reproducibility:
To enhance the reproducibility of your results, PLOS recommends that you deposit laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. For instructions see
Submitted filename:
Click here for additional data file.
Submitted filename:
Click here for additional data file.
Dear Dr. Namusisi,
We are pleased to inform you that your manuscript 'A descriptive study of zoonotic disease risk at the human-wildlife interface in a biodiversity hot spot in South Western Uganda' has been provisionally accepted for publication in PLOS Neglected Tropical Diseases.
Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.
Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.
IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.
Should you, your institution's press office or the journal office choose to press release your paper, you will automatically be opted out of early publication. We ask that you notify us now if you or your institution is planning to press release the article. All press must be co-ordinated with PLOS.
Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.
Best regards,
Charles Apperson
Guest Editor
PLOS Neglected Tropical Diseases
Bruce Lee
Deputy Editor
PLOS Neglected Tropical Diseases
***********************************************************
Dear Dr. Namusisi,
We are delighted to inform you that your manuscript, "A descriptive study of zoonotic disease risk at the human-wildlife interface in a biodiversity hot spot in South Western Uganda," has been formally accepted for publication in PLOS Neglected Tropical Diseases.
We have now passed your article onto the PLOS Production Department who will complete the rest of the publication process. All authors will receive a confirmation email upon publication.
The corresponding author will soon be receiving a typeset proof for review, to ensure errors have not been introduced during production. Please review the PDF proof of your manuscript carefully, as this is the last chance to correct any scientific or type-setting errors. Please note that major changes, or those which affect the scientific understanding of the work, will likely cause delays to the publication date of your manuscript. Note: Proofs for Front Matter articles (Editorial, Viewpoint, Symposium, Review, etc...) are generated on a different schedule and may not be made available as quickly.
Soon after your final files are uploaded, the early version of your manuscript will be published online unless you opted out of this process. The date of the early version will be your article's publication date. The final article will be published to the same URL, and all versions of the paper will be accessible to readers.
Thank you again for supporting open-access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.
Best regards,
Shaden Kamhawi
co-Editor-in-Chief
PLOS Neglected Tropical Diseases
Paul Brindley
co-Editor-in-Chief
PLOS Neglected Tropical Diseases