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Which Animals Are At The Greatest Risk For Anthrax?

  • Journal List
  • Emerg Infect Dis
  • v.23(9); 2017 Sep
  • PMC5572886

Emerg Infect Dis. 2017 Sep; 23(9): 1471–1477.

Role of Food Insecurity in Outbreak of Anthrax Infections amid Humans and Hippopotamuses Living in a Game Reserve Expanse, Rural Republic of zambia

Supplementary Materials

Technical Appendix English version of an investigation form used to interview persons potentially exposed to anthrax during in outbreak in northeastern Zambia, 2011.

GUID: D63EE531-D059-4D27-AFA6-3C40BBA139F0

Abstruse

In September 2011, a full of 511 human cases of anthrax (Bacillus anthracis) infection and 5 deaths were reported in a game management surface area in the district of Chama, Zambia, well-nigh where 85 hippopotamuses (Hippopotamus amphibious) had recently died of suspected anthrax. The human infections generally responded to antibiotics. To clarify transmission, we conducted a cantankerous-exclusive, interviewer-administered household survey in villages where homo anthrax cases and hippopotamus deaths were reported. Amongst 284 respondents, 84% ate hippopotamus meat before the outbreak. Eating, carrying, and preparing meat were associated with anthrax infection. Despite the adventure, 23% of respondents reported they would eat meat from hippopotamuses institute dead again because of nutrient shortage (73%), lack of meat (12%), hunger (vii%), and protein shortage (5%). Chronic nutrient insecurity tin can lead to consumption of dangerous foods, leaving communities susceptible to zoonotic infection. Interagency cooperation is necessary to prevent outbreaks by addressing the root crusade of exposure, such every bit food insecurity.

Keywords: anthrax, Bacillus anthracis, 1 health, hippopotamus, food prophylactic, food insecurity, zoonoses, Chama, Republic of zambia, bacteria

During August–September 2011, a total of 85 hippopotamuses (Hippopotamus amphibious) died of suspected anthrax (Bacillus anthracis) infection in a game management surface area forth the Due south Luangwa River almost the district of Chama in northeastern Zambia (Effigy 1) (one). At least 521 suspected human anthrax cases and 5 deaths were reported near this expanse during this menstruation. Residents of the expanse almost the river had reportedly found expressionless hippopotamuses and afterward butchered, cooked, and consumed meat from the dead animals, which was thought to be the cause of the homo outbreak. As previously reported, most human cases of anthrax infection were cutaneous infections, with most patients initially having papular lesions (95%) and the rest having lymphadenopathy and gastrointestinal symptoms (1). Near cases resolved later the patient received a course of oral ciprofloxacin. Some boosted animate being species were reported by local wild animals staff to have been affected, but no empiric data were establish to approve those reports.

An external file that holds a picture, illustration, etc.  Object name is 16-1597-F1.jpg

Location of an anthrax outbreak that originated in a game management expanse along the Due south Luangwa River in the Chama Commune of northeastern Zambia, 2011. Inset map shows location of Zambia in Africa.

Anthrax outbreaks associated with animals are common and reported worldwide. Herbivores are thought to take onset of disease later on ingesting spores in soil, water, or on vegetation. Reports of anthrax outbreaks occurring in wild and domestic animals in Africa have usually been associated with the dry out flavor and have stopped with the onset of the rainy season (2,three). Outbreaks can brainstorm with wild fauna, expand into domestic livestock, and ultimately affect humans (4,v). When anthrax outbreaks occur in national parks in Africa and are limited to the wildlife, the outbreak is usually immune to run its natural grade without any man intervention. Multiple challenges make it impractical to vaccinate free-ranging wildlife populations; sometimes vaccine programs are initiated simply usually only to protect endangered species or populations at loftier take chances (68).

Anthrax outbreaks associated with hippopotamuses have been reported previously in Republic of zambia, Uganda, Zimbabwe, and S Africa (three,911). Homo cases associated with wildlife outbreaks in Africa are mostly not well-documented simply are known to occur (5).

Republic of zambia's Chama District (population 103,894) borders Malawi, in what is currently known as Muchinga Province (Effigy 1) (12). Nearly 93% of the district's residents alive in rural areas, and overall population density is 5.nine persons/km2 (12). The rural population resides in minor villages largely accessible simply by all-terrain vehicles. Communication in many parts of the district is only possible through 2-way radios. Chama is within a game management area that includes the South Luangwa River and contains rich flora and fauna, including hippopotamuses but likewise other foragers and predators. Considering of Chama'southward status every bit a game management expanse, residents are not permitted to protect crops from foragers or hunt on area grounds, which are overseen past the Republic of zambia Wildlife Authority (ZAWA). Nutrient and water are scarce for animals and humans during Zambia's dry flavour, more often than not May–Nov. A filibuster in the annual rainy flavor, usually December–March, can put farmers at risk for low crop production, as was the case in 2011 (13). During this period, animals forage deep into riverbeds in search of h2o and nutrient, earthworks up and activating fallow anthrax spores. Residents, for whom nutrient can also be deficient under these conditions, have been known to consume animals they find dead in their area (Effigy two).

An external file that holds a picture, illustration, etc.  Object name is 16-1597-F2.jpg

A family searching for water by digging deep into a dried riverbed during the dry flavor in northeastern Republic of zambia.

In September 2011, a few months later the offset human anthrax cases were reported in the district, a team of epidemiologists, wellness officers, and ecology wellness technicians from the Zambia Central Ministry building of Health, the Eastern Provincial Health Office, and Chama Commune Health Office conducted a preliminary investigation of the possible outbreak under their jurisdiction. Shortly thereafter, upon formal request, epidemiologists from the US Centers for Disease Control and Prevention joined the Zambia team to conduct this outbreak investigation in an effort to further inform prevention activities.

Specifically, we aimed to shorten the outbreak by identifying and eliminating any remaining exposures and by recommending mitigation and prevention strategies for this and future outbreaks. We also wanted to make up one's mind the riskiest exposures then that educational messages could exist properly tailored. Here we report the results of a household survey used to place the most common exposures associated with human being anthrax and to determine how food insecurity contributed to consumption of the anthrax-contaminated meat and anthrax infection among residents of this game management expanse.

Methods

Nosotros conducted a cross-exclusive, 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 aggrandize on the data initially collected in the commune by local public health officials. Information technology 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 institute dead. Those who responded that they would consume animals they institute dead were asked an open-concluded question to elucidate their reasons for doing and 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 skillful administering the survey on one another before interviewing community participants.

Three teams administered the questionnaire, each team made upwardly of a trained District Health Office staff supervisor and 6 trained volunteer interviewers. Each team was assigned to 1 of the iii communities. Interviewers selected every fifth household they encountered in each hamlet 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 information technology was voluntary and could be stopped at whatever time past request. The Zambia Ministry of Health accounted this outbreak investigation to be exempt from Research Ideals Commission 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 adamant to exist nonresearch under 45 CFR 46 §102(d) and therefore did non require Institutional Review Board review.

Data from completed questionnaires were entered into an Access database (Microsoft, Redmond, WA, United states) 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 past example status by using χ2 and t tests. Associations were quantified with elementary and multivariable logistic regression.

The second function of the investigation involved going into the field to view 3 of the areas where most of the infected hippopotamuses were plant. The site visits occurred within about a month later on the outbreak and were conducted to ameliorate empathize the topography and the range of the animals and to place any additional animal species affected by anthrax. All sites were areas frequented past the exposed human populations and were <i km from residents' homes. The site surveys were not exhaustive; they focused on areas with known man-brute interaction (Figure 3) and recently discovered expressionless hippopotamuses (Effigy 4). N95 masks, Tyvek suits, and condom 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 command future spread of the infection to humans, animals, and the environment.

An external file that holds a picture, illustration, etc.  Object name is 16-1597-F3.jpg

Hippopotamus basic and hides left behind after butchering of animals that were found expressionless on a river depository financial institution and afterward identified equally the source of anthrax causing an outbreak among humans in northeastern Zambia, 2011.

An external file that holds a picture, illustration, etc.  Object name is 16-1597-F4.jpg

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

Results

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 past a healthcare worker since July 2011; another 137 (48%) reported non having anthrax infection diagnosed, and 116 (41%) did not know whether they had anthrax infection diagnosed. Nosotros assumed that those who did not know did not accept anthrax infection diagnosed. Male respondents deemed for 48% (n = 136) of full participants but 68% (n = 21) of those reporting having anthrax infection diagnosed, compared with 36% of cases occurring amidst female respondents (p<0.001) (Table i). 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 non evaluated as a risk factor. The median historic period of persons having received an anthrax diagnosis since July 2011 was 33 years, like to the median age of all participants (32 years) (Table 1). The most mutual signs and symptoms reported by those reporting having been diagnosed with anthrax included myalgia, skin lesions, fatigue, diarrhea, and fever (Table 2).

Table 1

Demographic characteristics of respondents to a survey conducted subsequently an outbreak of anthrax infections among humans and hippopotamuses living in a game reserve area, by example status, Chama District, Zambia, September 2011*

Characteristic Persons with anthrax diagnosed since July 2011, n = 31 Persons without anthrax diagnosed since July 2011, north = 137
Median age (range), y
33 (xv–72)
34 (xv–83)
Sex, %
M 68 36
F 32 64

*116 (41%) of survey participants reported that they did not know whether they had had anthrax diagnosed since July 2011; of these, median age was xxx (range 15–77) years, and 52% were male.

Table 2

Signs and symptoms of respondents reporting having had anthrax in survey conducted after outbreak of anthrax infections amongst humans and hippopotamuses living in a game reserve expanse, Chama District, Zambia, September 2011*

Signs/symptoms No. (%) respondents
Myalgia 21 (67)
Pare lesion 18 (58)
Fatigue xviii (58)
Diarrhea 17 (54)
Fever 16 (52)

*Anthrax infection diagnosed since July 2011.

Near 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 than probable to report having had anthrax than those who did non eat the meat. Carrying hippopotamus meat (odds ratio 5.3, 95% CI 2.0–xv.4) and preparing it for cooking (odds ratio 3.iii, 95% CI 1.i–13.7) were also significantly associated with anthrax infection. Afterwards decision-making for having eaten the hippopotamus meat, 3 activities (skinning, conveying, and cut the meat) were all still significantly associated with reported anthrax infection (Table 3).

Table 3

Association of anthrax diagnosis with specific activities involving hippopotamus carcasses based on responses to a survey conducted after an outbreak of anthrax infections among humans and hippopotamuses living in a game reserve surface area, Chama District, Zambia, September 2011*

Activity No. (%) persons
OR (95% CI) aOR (95% CI)
With anthrax diagnosed since July 2011, n = 31 Without anthrax diagnosed, n = 137
Skinning 14 (45) eight (6) 13.3 (4.iv–41.5) 12.0 (4.3–36.5)
Cutting 28 (90) lxx (51) 8.9 (2.5–47.5) viii.one (2.2–29.two)
Eating xxx (97) 106 (77) 8.eight (i.3–369.3)
Carrying 24 (77) 54 (39) 5.three (ii.0–fifteen.4) 4.four (ane.seven–11.eight)
Preparing 27 (87) 92 (67) three.3 (1.1–13.7) two.1 (0.v–11.viii)
Cooking 27(87) 93(68) three.ii (1.0–13.2) 2.0 (0.5–one.1)
Drying 21(68) 64(47) 2.four (i.0–6.one) 1.7 (0.half-dozen–iv.5)

*aOR, adjusted odds ratio (adjusted for eating hippopotamus meat); OR, odds ratio.

Virtually people surveyed (216 [76%]) reported they would not eat meat from a dead hippopotamus knowing at present that it can cause anthrax infection, merely 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 noesis. Of the 65 participants saying they would eat the meat if given the risk again, reasons given were because they lacked other options for a side dish ("bask") to Nshima, the maize-based staple food (44 [73%]); lacked meat (xiv [22%]); suffered from hunger (4 [7%]); or lacked protein (iii [five%]), in addition to other less commonly reported reasons (Table iv).

Table 4

Reasons for intending to eat meat again from hippopotamuses suspected to have died from anthrax among 65 persons who reported consuming expressionless hippopotamus meat in a survey conducted after an outbreak of anthrax infections amidst humans and hippopotamuses living in a game reserve area, Chama District, Republic of zambia, September 2011

Reason No. (%) respondents*
Lack of side dish 44 (73)
Lack of meat 14 (22)
Hunger 4 (7)
Lack of poly peptide 3 (5)

*Respondents could provide >1 response.

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

Give-and-take

A big outbreak of cutaneous anthrax amongst humans in the Chama Commune 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 gene driving the local population to consume meat from expressionless animals.

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

Our findings are subject to a few limitations. In the household surveys, we used cocky-study of anthrax diagnosis to define a example; nonetheless, 41% of participants indicated they did not know whether they had received an anthrax diagnosis. We assumed that these respondents might non have understood the question and had probably not had anthrax diagnosed. Although this supposition is a limitation, information technology would probably bias our associations toward the null. We also had to utilise self-report of diagnosis rather than laboratory confirmation. However, separately some hippopotamus and man samples were confirmed in the laboratory every bit positive for B. anthracis, which does strengthen the epidemiologic linkage (xiv). Finally, slight discrepancies can exist noted in the number of cases and hippopotamus deaths in this and the two 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 nosotros institute that the greatest run a risk for having anthrax diagnosed came from carrying, skinning, or butchering hippopotamuses. This finding is consequent 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 educational activity, enhanced surveillance in human and animal populations, and resolution of nutrient 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 existence butchered, nosotros call up the messages were received and understood past the communities affected. Because the handling of the carcasses proved to exist the near important risk gene for anthrax infection, futurity education campaigns should also focus on fugitive handling animals that accept died of unknown causes. In rural Zimbabwe communities where anthrax awareness was high (71.v%) 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 customs-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 place loftier-run a risk periods and locations for naturally occurring animal outbreaks through ecologic studies that identify weather condition favoring anthrax infection among fauna populations (18twenty). Wildlife and public wellness authorities should piece of work together to ensure that community-based campaigns proactively set up communities for possible outbreaks co-ordinate to their take chances profile (20). Community-based interventions should involve residents in addressing communitywide nutrient insecurity and in educating neighbors on the hazards of consuming meat from animals that die of unknown causes (16). These interventions should brainstorm before the dry flavour in outbreak-decumbent areas.

Questionnaire responses showed that nutrient insecurities appear to be the primary reason for treatment and consuming meat from animals found dead. Other countries in Africa have undertaken successful programs to distribute meat from bays animals to feed communities with express access to protein while also reducing poaching past 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; nevertheless, 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 boosted corn meal as a possible solution for the food shortage. However, populations at gamble for nutrient insecurity need improve access to balanced diets rather than more carbohydrates (22). Our survey respondents highlighted the want 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. Aid is needed to help the population better residue subsistence farming with cash crops on minor family unit farms to improve the overall diverseness of crops and ultimately mitigate the risk for food insecurity (22).

Our household survey aimed to determine the main risk factors for anthrax manual and the underlying factors driving those infected to adventure exposure. Our results suggest the need to accost long-standing political and economic issues related to food insecurity in protected areas, as well every bit an urgent need for better coordination between wild animals management and public health government. A more than proactive approach could help prevent time to come outbreaks.

Technical Appendix:

English version of an investigation form used to interview persons potentially exposed to anthrax during in outbreak in northeastern Zambia, 2011.

Acknowledgments

Nosotros would like to thank the following organizations for supporting this investigation: Epidemic Intelligence Service, Us Centers for Illness Control and Prevention, Atlanta, Georgia, United states of america; Center for Global Health, United states of america Centers for Affliction Control and Prevention; the Zambia Ministry of Health, Lusaka, Zambia; and local medical staff, participants, and interviewers from the Chama District of Zambia. Thanks as well to Michael Peters for his contributions to the mapping.

Biography

At the fourth dimension of this investigation, Dr. Lehman was an Epidemic Intelligence Officeholder assigned to the Bacterial Special Pathogens Branch, Sectionalisation of High-Consequence Pathogens and Pathology, National Centre for Emerging and Zoonotic Infectious Diseases, Centers for Illness Command and Prevention, Atlanta, Georgia, U.s.a.. He is currently a public wellness officeholder in the Usa Air Force, assigned to the US Air Force School of Aerospace Medicine, Wright-Patterson Air Forcefulness Base of operations, Ohio, Us. His primary research interests include food protection, nutrient security, and international public health.

Footnotes

Suggested citation for this article: Lehman MW, Craig Equally, Malama C, Kapina-Kany'anga M, Malenga P, Munsaka F, et al. Role of food insecurity in outbreak of anthrax infections among humans and hippopotamuses living in a game reserve area, rural Zambia. Emerg Infect Dis. 2017 Sep [date cited]. https://doi.org/x.3201/eid2309.161597

1Current amalgamation: U.s.a. Air Force School of Aerospace Medicine, Wright-Patterson AFB, Ohio, U.s.a..

iiCurrent affiliation: Centers for Illness Control and Prevention, Atlanta, Georgia, USA.

3Current amalgamation: Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland, United states

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5572886/

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