An investigation of an anthrax outbreak in Makoni District Ward 22 and 23 in Zimbabwe

Background : The first official clinical case of human anthrax case was made at Makoni District Medical Office on the 19 th of December 2013. This followed cattle deaths which were confirmed in the laboratory to be due to anthrax. We report the clinical characteristics, distribution of anthrax cases (place and time), risk factors for contracting the disease, environmental assessment, district preparedness and response and outbreak prevention and control measures. Methods: We conducted an outbreak investigation with the design of a 1:1 unmatched case-control study. Data were collected using a structured questionnaire. Environmental assessment, district preparedness and response and outbreak prevention and control measures were assessed using checklists through observations and key informant interviews. Data were analyzed using Stata-16. Bivariate analysis was performed to identify risk factors for contracting anthrax. Results: Thirty-seven cases (37) and 37 controls were interviewed. All the cases had cutaneous anthrax with commonest site of eschar being the hand (43%). Most of the cases (89%) were managed according to national guidelines. Eating meat from a from a cattle slaughtered due unknown illness or died alone [OR = 7.00 , 95%CI(2.06-23.82], skinning [OR = 5.04, 95%CI(1.77-14.36)], cutting meat [OR = 5.32, 95%CI(1.91-14.77)], cooking meat [OR = 3.42, 95%CI(1.32-8.91.)], source of from other villagers [vs butchery, OR = 14.85, 95%CI(2.79-79.06)], cuts during cutting meat or skinning cattle [OR = 3.50, 95% CI(1.18-10.51)], belonging to a religion which permits eating meat from a from a cattle slaughtered due unknown illness or died alone [OR = 6.29, 95%CI(1.85-21.39)] were associated with contracting anthrax. Having heard of anthrax before was protective against contracting anthrax [OR = 0.35, 95%CI (0.13-0.93)]. The district was ill-equipped and delay to respond to the outbreak.


Introduction
Anthrax is a bacterial infection caused by the spore forming Bacillus anthracis, a Gram positive, rod shaped bacterium [1]. Globally, approximately 2 000-20 000 human cases of anthrax occur each year [2]. Anthrax in humans is often a result of consumption of infected meat from livestock and wildlife [1]. The most common cases of anthrax in humans are cutaneous while inhalation and gastrointestinal are less frequent [1]. During the past three decades, there has been a progressive global reduction in the number of reported cases of anthrax in livestock and this might be attributed to response by to national programs [2]. Anthrax is still endemic in most African countries and the majority experience at least one outbreak per year. In South Africa, the annual number of outbreaks is less than 5 and occasionally zero, despite the continued occurrence of the disease in wildlife in the various parks [3]. Good control programs have been established in Botswana, Zimbabwe and Zambia, but the disease remains well known in the latter two countries at least [3].
In Zimbabwe anthrax is still a disease of public health importance because annually sporadic outbreaks are reported in many parts of the country [4,5]. The disease was first diagnosed in 1898 in the Matabeleland Region with the largest recorded outbreak in humans and possibly the largest among animals having occurred in 1978-1980 during the peak of the Liberation War. The disease spread over time from area to area, until six of the eight provinces were affected and over 10,000 human cases and 182 human deaths were documented. Human cases were secondary to an unprecedented outbreak in cattle. The outbreak in the cattle was due to cessation of cattle vaccination which was caused by the war. The number of cases of anthrax recorded during this period was far high than the previous years which usually records a dozen or less cases annually [6][7][8][9][10].
Since then sporadic outbreaks have been reported in many parts of the country. Over the years, compulsory dipping of cattle in the rural (communal) areas led to the decrease in the number recorded of outbreaks. However, with the current deterioration of the economic environment which has led to poor prevention and control measures regular outbreaks are being reported.
In Manicaland Province of Zimbabwe anthrax is endemic and annually cases in cattle and humans are reported. In 2011 and 2012, 37 and 49 cases were recorded respectively. In 2012 the cases were reported from Buhera, Chipinge, Mutare and Mutasa Districts in the province [11]

Study design
We conducted an outbreak investigation using an unmatched 1:1 case-control study. The study population were residents of Makoni District Ward 22 and 23. A case was defined as any person in Makoni District Ward 22 and 23 who developed a disease which manifested by itching of the affected area, followed by a painful lesion which became papular, then vesiculated and eventually developed into a depressed black eschar between 19 June 2013 and 29 January 2014. A control was defined as any person in Makoni District Ward 22 and 23 who never developed a disease which is manifested by itching of the affected area, followed by a painful lesion which became papular, then vesiculated and eventually developed into a depressed black eschar between 19 June 2013 and 29 January 2014.
Cases were identified from the line lists that was available at Makoni Rural Hospital which services the two wards and through active case findings in the community. Controls were selected from the neighborhood of cases in same villages. Any person who was diagnosed with chickenpox, skin drug reaction, acute skin disease or other disease which mimics anthrax were excluded from the study.

Data collection
Data were collected using an interviewer administered questionnaire. Review of medical records was done to assess how cases were managed. An Integrated Disease Surveillance Response (IDSR) checklist was used to assess the emergency preparedness response of the district [12]. An Environmental health assessment was done to assess how carcasses were buried, availability of dip tanks and adequacy of grazing land. Key informant interviews were conducted with the District Medical Officer, District Veterinary Officer, District Environmental Health Office and the Environmental Health Technicians (EHTs) at Makoni Rural Hospital.

Data analysis
The data were analyzed using Stata 16 [13]. Cases and controls baseline characteristics were compared using frequencies, proportions and Chi -square. To assess risk factors for contracting anthrax bivariate analysis was conducted using logistic regression at 95% confidence interval and significance level of 5% (p < 0.05).

Permissions and ethical considerations
The permission to carry out the study was sought from the Manicaland Provincial Medical Director, Makoni District Medical Officer, Local Headman and Councilor. The study was approved ethically by the Health Study Office within the Ministry of Health and Child Care which coordinate the Zimbabwe Field Epidemiology Training Programme. Written consent was obtained from every participant prior to entry into the study. For participants under 18 years consent was sought from parents or guardians.
No names were written on the data collection tools. Confidentiality was assured and maintained.

Baseline Characteristics of cases and controls
We interviewed 37 cases and 37 controls. The median age for cases and controls were 34 years (Q 1 : 22; Q 3 :42) and 28 years (Q 1 :25; Q 3 :46) respectively. Males constituted 73% (27) of cases and 70.3% (26) of controls. Most of both cases (67.6%) and controls (59.5%) had secondary education and above. Most of both cases and controls were also not employed (59.5%). Generally, the baseline characteristics for cases and controls were comparable (Table 1).   Figure 4 shows the epidemiological curve of the outbreak.

Risk factors for contracting anthrax
On bivariate analysis (   The department also stopped issuing of permits for cattle movement.

Discussion
This anthrax outbreak affected both humans and cattle. Cattle which were slaughtered or died due to unknown illnesses were the source of infection while meat was the vehicle of transmission. Most of the cases of human anthrax were cutaneous with the hands most affected. The case fatality rate was low. The following were found to be risk factor for contracting anthrax eating meat from cattle which were slaughtered or died alone due to unknown illnesses, source of meat from other villagers, skinning, cutting and cooking meat, cuts/ abrasions during skinning or cutting meat and belonging to religion which permits eating meat from cattle slaughtered or died alone due to unknown illnesses.
Having heard of anthrax before was protective of contracting the disease. The carcasses of the dead cattle were incorrectly buried, and disinfection of sites were the animals died was not done. The district was not prepared to handle the outbreak. The outbreak was prolonged, and it took time for the district to institute control measures.
The anthrax eschar was more common in hands. This was consistent with the findings from other studies [15,16]. This is because hands are used for handling meat and are at higher risk of developing abrasions, bruises and cuts which creates the route for entry of the anthrax spores. The case fatality rate for this outbreak was very low. The finding is consistent with other studies which have also recorded low fatality cases in anthrax outbreaks [17,18]. The low case fatality rate in anthrax outbreaks might be due to the fact that the commonest form anthrax i.e. cutaneous anthrax has the least mortality rate as compared to other form of anthrax [1]. In our study all the interviewed cases had cutaneous anthrax and the victim who died in this outbreak might have developed respiratory anthrax based on the described symptoms and signs. Respiratory anthrax has a higher mortality as compared to cutaneous anthrax [19,20].
The following were found to be risk factor for contracting anthrax eating meat from a dead animal, skinning, cutting and cooking meat, cuts/ abrasions during skinning or cutting meat and religion which permits eating meat of a dead animal. These finding are consistent with other studies done locally and might be due to similarity of practices [15,21,22]. The reason why having cuts or abrasions was associated with contracting anthrax is due to the fact that during the process of preparation of meat cuts and abrasions are likely to develop and these creates access routes for the spores to the subdermal tissue [1]. Belonging to a religion which permits eating meat from animals which died on their own was associated with contracting anthrax. These finding is however not consistent with other study done locally where one's religion belief on consumption of meat from a dead animal was a was not associated with contracting anthrax [15,21]. Having heard of anthrax before was protective against contracting anthrax in our study. This is because those who heard of anthrax will be aware of the modes of transmission, signs and symptoms and preventive measures so they will not put themselves at risk [23].
The environment assessment showed some factors which increased the risk of anthrax in the area.
There were inadequate grazing land and pastures in the affected areas. This outbreak started a few months before the rainy season, a period typically associated with lack of grazing grass. During this period the grass will be short which predisposes grazing cattle to ingestion of the anthrax bacilli due to overgrazing [24,25]. Anthrax spores can survive for a long period of time in conducive soil conditions [26]. The presence of an army base in one of the affected wards raises the possibility of anthrax having been introduced to the area as part of bioterrorism during the liberation struggle [27].
One of the wards also bordered a game reserve.

Conclusion
Eating meat from cattle that were slaughtered due unknown illness or died alone were the source of infection for the outbreak. All cases had cutaneous anthrax and the majority were managed according to national guidelines on anthrax. Eating meat from cattle slaughtered due unknown illness or that were dying alone, skinning, cutting and cooking meat, having cuts during skinning or cutting meat and belonging to a religion which permits eating meat from cattle slaughtered due unknown illness or that were dying alone were among factors associated with contracting anthrax. Having heard of anthrax before was protective against contracting anthrax. The district delayed and was not prepared for the outbreak. Zoonotic committees were not functional and there was weak coordination between the health and veterinary departments during the outbreak response.