Snakebite Envenomation in Rwanda: Patient Demographics, Medical Care, and Antivenom Availability in the Formal Healthcare Sector

INTRODUCTION

Snakebite envenomation (SBE) is a life-threatening condition that predominantly affects subsistence farmers and children in rural areas of sub-Saharan Africa and Asia, and especially those living in poverty. ^1–3 Each year, between 1.8 and 2.7 million people are envenomed by snakes, resulting in 81,000–138,000 deaths and 400,000 permanent disabilities (e.g., amputations and blindness). ^4,5 Snake venoms contain variable mixtures of precoagulants, cytolytic and hemolytic toxins, neurotoxins, hemorrhagins, and biogenic amines that cause effects ranging from pain and swelling to tissue necrosis, uncontrolled bleeding, descending paralysis, renal failure, and sometimes death. ⁶ Once bitten, those at highest risk of mortality are children (because of their small body mass), the elderly (because of lower fitness and general health condition), and those in rural/remote areas (because of delays in receiving medical care). ^1,7 Delays in accessing formal care are often attributed to remoteness, lack of transportation, antivenom shortages, preferential use of traditional healers, inability to pay for treatment, and poor knowledge among healthcare providers. Prognosis also depends on the snake species and venom dose.

In addition to causing acute and chronic physical trauma, SBE can be psychologically and economically devastating. ^5,8,9 In sub-Saharan Africa, SBE inflicts an estimated burden of 1.03 million disability-adjusted life years (95% CI: 0.8–1.28 million) among affected communities annually. ¹⁰ This does not include suffering incurred because of envenomation of household pets or domestic livestock. Limited information is available regarding SBE morbidity and mortality in domestic animals in Africa, but the global case-fatality rate recently estimated at 47% suggests that SBE of domestic animals causes significant losses for their human owners. ¹¹

In 2017, the WHO reclassified SBE as a category A neglected tropical disease, and in 2019, it released a strategic road map focused on halving disability and mortality by 2030. ^3,12 Noteworthy challenges to achieving this goal include the lack of epidemiological data in many affected countries and shortages of safe and effective antivenom worldwide. ⁴ Rwanda is a low-income, agrarian country that is home to 13 venomous snakes of public health concern. ^13–15 Those who earn income by working in close contact with rural and wild habitats and wildlife are most likely to suffer the effects of human–snake conflict, making this both a One Health issue and an occupational health issue. Estimates of SBE-related morbidity and mortality in people and livestock are scarce in Rwanda. Therefore, our goals were to 1) describe the demographics of people seeking hospital care for SBE, 2) audit physician compliance to national patient management recommendations, and 3) assess availability of snake antivenom at district and provincial hospitals in Rwanda during 2017 and 2018.

MATERIALS AND METHODS

Study setting.

Rwanda is a low-income country located in Africa. It has one of the highest population densities in sub-Saharan Africa (441 people/km²) and is home to approximately 12.2 million residents, with most employed in subsistence agriculture (72%). ^13,15 The seasons are split into four broad intervals: 1) the long rainy season (March–May), 2) the long dry season (June–September), 3) the short rainy season (October–November), and 4) the short dry season (December–February).

Thirteen medically important snakes are known to reside in Rwanda. ¹⁴ Three species are classified as category one snakes (i.e., those of highest medical importance): puff adders (Bitis arietans), Jameson’s mambas (Dendroaspis jamesoni), and black-necked spitting cobras (Naja nigricollis). Ten species are classified as category two snakes (i.e., those of secondary medical importance): Bibron’s burrowing asp (Atractaspis bibronii), variable burrowing asp (Atractaspis irregularis), East African Gaboon viper (Bitis gabonica), rhinoceros viper (Bitis nasicornis), black mamba (Dendroaspis polylepis), forest vine snake (Thelotornis kirtlandii), boomslang (Dispholidus typus), banded water cobra (Naja annulata), forest cobra (Naja melanoleuca), and Gold’s tree cobra (Pseudohaje goldii). ¹⁴ Medical services are controlled centrally and organized from village to national levels (i.e., health posts [N = 476], health centers [N = 499], district hospitals [DHs; N = 36], provincial hospitals [PHs; N = 4], and referral/teaching hospitals [N = 8]; Figure 1). ¹⁶ Individuals bitten by snakes usually seek care at a health center or a DH first and may be transferred to a higher facility (PH or referral hospital) as needed. Animal bites are reportable at hospitals but not by health posts or centers. The national integrated health management information system (HMIS) aggregates data so that bites from specific animals, such as snakes, cannot be accessed through the electronic system.

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Locations of district and provincial hospitals and antivenom supply in Rwanda (between 2017 and 2018). .

Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0976

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RESULTS

DISCUSSION

In this first evaluation of SBE in Rwanda, snakes were identified as the second leading cause of animal bites among those seeking hospital care in 2017 and 2018. Our study identified major gaps in health surveillance and patient management, including discrepancies between HMIS data and hospital registers, lack of animal-specific case reporting, low compliance to national guidelines for patient care, and lack of antivenom appropriate for African venomous snakes. Rwanda has ambitious objectives for improving the health and prosperity of its citizens, including achieving middle income status by 2020. ¹⁸ Moreover, the agricultural sector contributes 33% of the national gross domestic product. ¹⁵ Snakebite envenomation is overrepresented among farmers, children, and economically productive age-groups. Therefore, it is a barrier to the country’s goals on poverty alleviation, and deserves increased attention in the medical, veterinary, agriculture, and tourism sectors. Improved surveillance of SBE among people and animals, including assessments of behavioral, occupational, economic, and environmental risk factors, are crucial to better understanding the burden of disease in Rwanda and to implementing evidence-based solutions.

Our study identified 363 cases of SBE treated at DHs and PHs over a 2-year period. These observations are far lower than the mean morbidity (4,171, 95% CI: 3,454–4,885) and mortality (196, 95% CI: 136–391) estimated to occur annually by Halilu et al. ¹⁰ The discrepancy is partly explained by the data management issues we encountered while obtaining data from HMIS, hospital registers, and patient files, such as missing patient registers and files. Furthermore, we were unable to estimate a case-fatality rate as hospital records in Rwanda do not report patient outcomes following discharge or transfer. Therefore, our case numbers should be interpreted as a minimum estimate of hospital-treated SBE cases. The difference in animal bites reported in HMIS (N = 3,607) versus DH/PH hospital registers (N = 2,600) demonstrates that this issue does not just apply to SBE patients. However, a far larger issue in Rwanda is the frequent and sometimes preferential use of traditional healers who use remedies not recommended by the WHO, including “black stone” treatment, oral venom extraction, and herbal extracts/ointments. ^1,19 Patients using such services, and those who self-treat at the pharmacy, are not recorded by the formal medical system, and, as a result, estimates of SBE incidence are based on East African data rather than empirical evidence generated in Rwanda.

Our survey suggested that more women sought medical care for SBE than men and that significant differences occurred between age-groups. It is unclear whether the gender difference was explained by a higher level of bites among women (because of increased exposure or decreased access to protection such as shoes) or because gender differences exist in health-seeking behavior. Men and women in Rwanda both participate in high-risk activities such as cultivating land, herding livestock, gathering firewood, and sleeping on the ground. Retrospective case audits in other sub-Saharan African countries such as Tanzania, Benin, Chad, and Ghana showed a different effect, with more men obtaining medical care for envenomation than women. ^20–23 With respect to age, the highest number of cases occurred in children (< 18 years) and young adults (18–30 years), whereas the highest numbers per capita occurred in older adults (> 60 years). This difference between case counts and population proportions is explained by the large population of children relative to adults in Rwanda, resulting from past civil war, political unrest, and infectious disease epidemics. ¹³ The heightened risk among economically productive age-groups was also reported in Tanzania, Ghana, Benin, and Kenya and is one reason why SBE is linked to the poverty cycle. ^{2,9,20–22,24} Low-income rural workers lacking personal protective equipment (e.g., shoes and torches) and safe sleeping areas are disproportionally exposed to high-risk rural environments through their work (e.g., farming, forestry, and mining) and also experience the greatest delays in accessing medical care. Rural children are similarly exposed but are more vulnerable because of their small body mass. ¹ Envenomed children and workers are not only burdened by physical and psychological trauma but also by financial costs. These take the form of direct medical costs (e.g., treatment and transportation to hospital) and indirect costs (e.g., lost work days and reduced productivity), ultimately impacting not only individuals but also their families and broader communities. ⁹

Available information on time of envenomation indicated that half of the bites occurred after dark. This supports the need for increased awareness on how to deter snakes from entering living quarters (e.g., bed nets, sleeping off the ground, removing rodent attractants, building houses away from grain storage areas, and blocking gaps). ⁶ Two-thirds of day-time bites occurred in the morning, and this is likely because people often engage in high-risk activities (e.g., cultivating, livestock herding, and firewood collection) in the morning. Our finding that SBE patients were predominantly bitten on their legs or feet (81%) is supported by other sub-Saharan African studies, suggesting many people are bitten after accidentally stepping on a snake. ^20,24 Wearing boots can protect against such bites but could be economically prohibitive or impractical for some environments (e.g., rice paddies).

Eastern Province hospitals treated more SBE patients than hospitals in any other administrative district. This province is an intense area for livestock and cash crop production, and has a hotter and drier climate relative to the other provinces. ²⁵ Eastern Province also contains Akagera National Park, a protected wildlife area home to a variety of venomous snakes and surrounded by farmed land. However, the proportion of cases per capita was highest in Kigali city. Although the country capital has a large urban population base, it also includes many peri-urban and suburban areas with intense agricultural activities. Other explanations for the large proportion of cases observed in this urban center is that some patients might have traveled from other provinces to Kigali city DHs and PHs, believing that they were superior, or that Kigali city residents with their higher literacy and proximity to hospitals were more likely to seek health services.

The WHO states that antivenom is the only safe and effective treatment to neutralize snake venom. ¹ Our study demonstrated low availability of antivenom at hospital pharmacies (only three of 40 were in stock), availability only of Crotalidae polyvalent antivenom labeled for use against Asian snakes, and infrequent prescription of antivenom (13%). Some patients were prescribed antivenom at hospitals when it was not available at the pharmacy, whereas other patients were not prescribed antivenom even though it was available. On the global average, approximately 50% of bites from venomous snakes result in envenomation, depending on the species and situation. ²⁶ Altogether, this suggests that antivenom is under-prescribed and underused in Rwanda, possibly because of poor knowledge among health authorities and medical staff, lack of access, lack of information about snake species (no snakes were fully identified in the patient files), low severity of cases, or fear of anaphylactic reaction. No information is available on SBE severity, highlighting a major knowledge gap in understanding current antivenom needs in Rwanda. In many countries, the cost of antivenom is economically devastating to a typical low-income patient; however, 90% of this expense is covered for Rwandese with CBHI. Increased access to African-specific polyvalent antivenom is clearly needed at DHs and PHs, especially for those in higher risk locations such as Kigali city and Eastern Province. This could be achieved by capitalizing on an existing contract between the Rwandan Ministry of Health and Zipline (https://flyzipline.com/), a company currently using drones to transport blood products from a central warehouse to government hospitals. Drones could be particularly valuable in the context of antivenom as SBE patients require rapid treatment, antivenom is in short supply, and quality products can be costly (especially if unused and allowed to expire).

The cytotoxic and neurotoxic proteins contained in venom require specific treatment and careful management. Overall, compliance to SBE patient management guidelines was low, suggesting that physicians are not aware of proper protocols or that limitations in resources influenced management behaviors. Of the 15 checklist items, lowest compliance was observed for prescription of vitamin K (promotes blood clotting), antivenom, and tetanus toxoid. Highest compliance was observed for nonspecific procedures such as taking vital signs, avoiding tourniquets, and avoiding administration of aspirin. Many medical records had incomplete clinical descriptions, and none reported the grade of envenomation. ¹⁷ Our team was unable to directly observe physician practices; however, instructions for patient management are communicated through patient records, making this an acceptable proxy for assessing patient care. We recommend that any intervention to improve physician practices should also encourage improvements to detailed record keeping and strict adherence to protocols.

Snakebite envenomation is both a One Health issue and an occupational health issue. Those who earn income by cultivating land, herding livestock, collecting firewood, and extracting natural resources (e.g., mineral mining) are highly affected. Environmental conditions in built and natural environments, including housing construction, climate (e.g., rainfall), and land use changes, greatly influence human and livestock risk to SBE. ²⁰ Moreover, snakes play important roles in ecosystem health (including rodent control) and cannot simply be eliminated. Our results also highlight gaps in SBE reporting, patient management, and antivenom use/availability in Rwandan hospitals. Therefore, comprehensive and multidisciplinary strategies are needed that engage high-risk communities (e.g., farmers) in prevention, strengthen health systems (e.g., improved SBE reporting and patient management), build global partnerships, and improve the affordability and accessibility to safe and effective treatment (i.e., antivenom). ⁴ These pillars are the basis of the WHO road map for SBE prevention and control, and are promoted to ensure that SBE strategies are both equitable and impactful for those who are most vulnerable. Future research prospects may include SBE patient follow-up to identify One Health risk factors and economic burden, mapping snakebite sites, an epidemiological assessment of SBE victims not seeking hospital care, an evaluation of care provided by traditional healers, and engagement with policy-makers to improve physician training and availability of antivenom appropriate against local snake species.