Estimating and predicting snakebite risk in the Terai region of Nepal through a high-resolution geospatial and One Health approach
Our results showed that covariates at different geographical scales (national and local) may have important effects on the risk of snakebite, both for humans and animals. The results indicate that the risk of snakebite in the Terai varies at national scale between clusters and at local scale between households. The evaluation of the final models without spatial random components and the worsening of the models’ goodness of fit as a result highlighted how snakebite risk and its determining factors are indeed spatially structured.A strong association between high snakebite incidence and mortality, and poverty was established from the analysis of 138 countries affected by the disease32. In this study, we identified the PPI, an indicator for poverty, as a highly influential risk-increasing factor for humans. This not only confirms the critical role of poverty as a driver for this Neglected Tropical Disease, but also offers the possibility to use a standardized index at individual household scale for similar studies. Chaves et al.33 used the Poverty Gap, which is a simpler index expressing how far a person is from the average national poverty line, but to our knowledge, no study has used PPI for snakebite in any way. Applying PPI as a snakebite risk predictor also addresses previous expert calls for an Ecohealth approach to consider the relationship between the structural characteristics of houses, poverty, and snakebite34.Three of the survey covariates had significant effects on the odds of snakebite. Food storage and straw storage increased them, while sleeping on the floor reduce them. The effect of the first two covariates is likely to be related to prey availability, represented by rodents, which are attracted by food and shelter sources. Both food and straw are very often stored near dwellings, which in the end multiply the number of possible encounters between humans, domestic animals, and the hunting snakes20. The expected snakebite risk reduction effect by sleeping on the floor is more complex though. Previously, a higher snakebite incidence was reported among rural Hindus in Maharashtra, India, due to their custom of sleeping on the floor35,36, while in Nepal, Chappuis et al. did not find any protective effect or significant difference in snakebite cases between sleeping on a cot or on the floor37. This result, nevertheless, might be influenced again by regional customs that make sleeping on the floor more common in eastern Terai (71.1% of all affirmative answers to this question), and second, by the commonly acknowledged prevalence of kraits (Bungarus spp.) in western Terai, which are the species most commonly linked to bites to people sleeping on the floor while hunting at night inside houses22,38. This geographic separation, between the human behaviour and the distribution of the species considered to cause most bites linked to it, could explain the observed shift in the odds towards a reduction effect. This effect should be further explored in localized studies designed to capture behavioural differences in humans and snakes.For both the general human risk model and its equivalent prediction model, the covariate Distance to water had a significant risk-increasing effect. For each additional km in distance from permanent water sources, the odds of snakebite increased by 1.38 and 1.51 times, respectively. From a human perspective and in this socio-economic framework, it would be important to consider not only the distance to water, but also the path taken to get the water (or any other resource). If this path would lead a person through grasslands and open fields, this could imply an increased risk of snakebite. From an ecological perspective, there are two important aspects to consider in relation to water sources. One is, as in this study, the distance from large, constant water sources, which usually represent stable environments subject to less hydric stress. The second (not considered here) are the human-made water sources, such as ponds, reservoirs, and paddy fields that change often, are usually closer to human dwellings, and are known to attract some medically important venomous snakes (MIVS)5. Studies on snake migration and home range use have concluded that depending on species and ecological conditions, snakes can move between a few tens of meters per day and more than 10 km between seasons, while searching for water and prey resources38,39,40,41. In sub-tropical regions like the Terai, snakes living closer to continuous sources of water and vegetation should have easier access to a wider variety of prey. On the contrary, those living in agricultural areas might need to scout farther in the search for resources, encountering human-made waterbodies and prey, such as rodents42 and amphibians, abundant in this region10. Further studies considering all sources of water, and species ecology, biology and richness would be necessary to completely understand the effect of this and similar eco-physiological covariates.Another important factor was the NDVI, which is a commonly used value to express photosynthetic activity, leaf production and in summary the ‘greenness’ of the environment43. As is the case for other covariates, its interpretation depends on the study circumstances. In Iran, it was considered an indicator of prey availability for snakes and linked to snake habitat suitability14. Elevated NDVI values have been associated with higher number of hospitalizations in Nigeria and northern Ghana, in particular during the periods of high agricultural activity, which is also related to higher snake-human contact and higher snakebite incidence43. In our study, its ‘protective’ effect can indeed be the consequence of better access to prey associated with healthier ecosystems, explained in the Terai by the higher NDVI values of the multiple dense forests distributed along the region. In addition, the averaged NDVI values for agricultural areas should be lower than those for perennial forests, because they include the highs and lows of production and harvest.Environmental drivers like temperature and precipitation are common factors in geospatial analyses of snakebite13,14,17,44. They are found in many cases to be the main factors modulating the incidence or risk of snakebite, while varying in importance according to study conditions. For example, in Iran, precipitation seasonality was the most prevalent climatic covariate determining the habitat suitability leading to snakebite risk14, while in Mozambique, temperature seasonality was the predominant covariate13. Despite the Terai’s sub-tropical climate, the range of the average minimum temperature of the coldest month (BIO6) was 1.8–10.9 °C. For our snakebite risk analysis in animals, an increase of 10 °C of BIO6 between any two points represented an increase in the odds of snakebite of 23.41 times. For snakes, this range could be the difference between total lethargy and partial activity45, which could lead to increased numbers of snakebites. In addition, and according to the production and holding practices of domestic animals in the Terai, this temperature range can also represent the difference between animals (mainly ruminants) being kept in sheds when at the lower range limits, or being let out of them at the upper limits, which would again increase the chances of encounters with snakes.Similarly, for the animal model, pig density and sheep density, significantly influenced the variation in the risk of snakebite for animals in the Terai. This could be due to the conditions in which the animals and their feed are kept, favouring environments that are beneficial for either snakes or their prey. At more local scales, rather than the distribution, the presence of other animal species could instead be the factor associated with higher snakebite rates12. However, since the available data on domestic animal density was produced more than 10 years ago, and the animal population has grown substantially in the last years in Nepal, this outcome should be interpreted with caution.For the animal risk, the possession of an animal shed also significantly increased the odds of snakebite. Similar to straw storage, animal sheds and similar constructions offer some shelter and at the same time attract small (prey) animals, both of which are likely to attract snakes, increasing snakebite risk for the animals using the shed. If in addition, the sheds function as poultry coops, the snake hunting behaviour might be instead targeted towards chicks and chickens12. Mitigation measures such as raising the coop’s floor or securing openings with fine metal mesh have been suggested to reduce this risk12.The human modification of terrestrial systems was the only non-significant covariate in the animal risk model. However, as its strong, risk-reducing effect still seems to explain a lot of the response variation, it was retained. Its change in one unit, i.e., going from a pristine to fully modified environment, decreased the odds of snakebite by 0.13 (equivalent to 7.69 times), which agrees with previous national survey results from Sri Lanka21.For our human risk prediction model, four covariates were either significant or helped to explain the changes in the response. Distance to water and NDVI were clearly significant, and precipitation of the driest quarter (BIO17) and the mean annual temperature (BIO1) helped to explain some of the response variation with convincing, unambiguous effects. For BIO17, an increase of 100 mm of rain during the driest months of the year represented an odds-reduction effect equivalent to 8.33 times. This agrees with the results of distance to water, suggesting that the additional availability of resources during water shortage periods, i.e., almost four times more rain (BIO17 range: 18–71 mm), could locally improve ecological conditions for snakes also leading to less scouting and fewer human encounters. Previous studies have analysed the multilevel ecological effects of droughts, e.g., reducing snake prey and leading snakes to engage in riskier behaviours46,47. For BIO1, the protective effect was weaker. An increase of 10 °C represented a reduction of the odds of snakebite equivalent to 3.57 times. Average temperatures for specific locations are difficult to interpret, since they might depend on mild highs and lows, strong highs and lows, or relative combinations of both. Thus, despite having a relatively important effect on the response, this effect still might be the consequence of confounding and unknown interactions.Several other evaluated covariates, for both humans and animals, showed a negligible effect on describing the response, were not significant while having very large uncertainties, or both. Consequently, they were discarded as predicting factors. For the list of baseline covariates evaluated, see supplementary Table S1. For a complete list of available survey covariates, see Alcoba et al.27.Some of our discarded covariates have been important in other studies, for example, to quantify snakebite risk based on reclassification methods of covariates such as habitat suitability, species presence, or envenoming severity13,14,17,44,48. These methods are especially relevant when one species (or very few) is the cause of most snakebite cases, and has differentiated optimal and sub-optimal habitats. In Nepal, and particularly in the Terai, there are at least two, and sometimes more than 10 MIVS with overlapping distributions49. Thus, it could be said that practically the whole region offers suitable habitat for multiple MIVS. In addition, the impossibility of reliably identifying the species having bitten the surveyed victims hindered the use of single species in the analysis. In our analysis, species richness was removed, as it showed almost no effect on the response. A recent meta-analysis reported an equivalent result at global scale, finding no significant difference between the number of venomous snake species in tropical and temperate locations, while the number of snakebites is clearly higher in tropical areas50. These results suggested that high incidence of snakebite is unrelated to species richness, but instead related to other factors like the number of people working in agricultural environments21,32,50. Another important driver of snakebite incidence has been population density50. In our study, however, any possible effect from population density on the risk was diminished by the random selection of households at specific numbers during study design. This was later confirmed by the minimal effect of population density as covariate in the human risk analysis.This study presents a few limitations. For instance, despite the capacity of the INLA method to borrow strength from neighbouring observations and areas, the selection of adequate covariates with enough explanatory power still depends greatly on the number of snakebite cases, which even for a national scale study like this remains small. Also, some of the covariates with the strongest explanatory power came from our household survey, which prevented their use for generalized spatial prediction models. Concerning the animal risk analysis, due to the small number of snakebite cases we opted to aggregate all animal species and consider a grouped response. Thus, for a spatial analysis of animal risk, it was not worth it to consider each species, since that would dilute further an already sparse dataset in individual models and selection processes. Moreover, the data gathered for animals was dependent on the random selection of (human) households and unrelated to the current distribution of animal populations. This, in addition to the possible number of dry bites that go unnoticed, might be responsible for the low number of animal victims recorded (even combined across all species), making a more detailed analysis unfeasible.Despite the large number of covariates examined during our analysis, very few were useful to predict snakebite risk along the Terai. It is possible that confounders or other difficult-to-measure covariates could better explain the complex relationship between the ecology and biology of MIVS, socio-economic factors, human behavioural traits, and the circumstances around domestic animal keeping. This needs to be further explored, following a recent call for an overarching One Health and Ecohealth approach to better understand the drivers for snakebite risk, incidence, and mortality under specific situations34.In conclusion, snakebite is a multi-factorial disease and there is no possible universal approach to model its risk. Each model should be individually designed for each set of socio-economical, geographic, ecological, cultural, and environmental circumstances19. To better understand and address the snakebite problem, it is necessary to approach it, whenever possible, with local data collected at a national scale, so that the conclusions drawn can fuel appropriate national public health policies and actions. As long as people work, live, and keep their domestic animals in close contact with natural environments with MIVS, the risk of snakebite will be present. However, better understanding of the factors influencing that risk at the most granular scale possible, and the estimation of the populations at risk, can help to better target prevention and mitigation measures. For humans, this evidence can channel efforts towards improved access to treatment through the optimized stockpiling of antivenom, and the improvement, relocation or new construction of treating facilities, but more importantly, towards community education and sensitization in preventive campaigns51. Part of that preventive and educative efforts can be done at household level, by promoting and facilitating the use of protective equipment such as rubber boots, or the guidance on how to improve and adapt their immediate surroundings to make them ecologically less attractive for snakes and their prey. For domestic animals, this information could help better target awareness-raising activities for animal owners and implement mitigation strategies. For animals at higher risk, tailored interventions such as the improvement of housing conditions, regular cleaning of sheds and surrounding areas (e.g., from food waste and surrounding vegetation), and using light when animals are walked out of the enclosure at night could be deployed specifically as snakebite prevention measures52. It is also important to highlight that many of the factors analysed in this study affect most directly the snakes themselves, not only as snakebite agents, but also as a diverse group of species, differently affected by ecological, climatic and environmental factors in a multiplicity of settings shared with humans and domestic animals. It is therefore necessary to further investigate how those factors influence the behavioural and ecological traits of MIVS in order to truly understand this disease from a One Health viewpoint. At stake is the reduction of snakebite envenoming incidence rates in humans and animals, and of its possible long-term sequelae on human populations. More
