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Background: Hantavirus disease in humans is rare but frequently lethal in the Neotropics. Several abundant and widely distributed Sigmodontinae rodents are the primary hosts of Orthohantavirus and, in combination with other factors, these rodents can shape hantavirus disease. Here, we assessed the influence of host diversity, climate, social vulnerability and land use change on the risk of hantavirus disease in Brazil over 24 years., Methods: Landscape variables (native forest, forestry, sugarcane, maize and pasture), climate (temperature and precipitation), and host biodiversity (derived through niche models) were used in spatiotemporal models, using the 5570 Brazilian municipalities as units of analysis., Results: Amounts of native forest and sugarcane, combined with temperature, were the most important factors influencing the increase of disease risk. Population at risk (rural workers) and rodent host diversity also had a positive effect on disease risk., Conclusions: Land use change-especially the conversion of native areas to sugarcane fields-can have a significant impact on hantavirus disease risk, likely by promoting the interaction between the people and the infected rodents. Our results demonstrate the importance of understanding the interactions between landscape change, rodent diversity, and hantavirus disease incidence, and suggest that land use policy should consider disease risk. Meanwhile, our risk map can be used to help allocate preventive measures to avoid disease.

Several viruses from the genus Orthohantavirus are known to cause lethal disease in humans. Sigmodontinae rodents are the main hosts responsible for hantavirus transmission in the tropical forests, savannas, and wetlands of South America. These rodents can shed different hantaviruses, such as the lethal and emerging Araraquara orthohantavirus. Factors that drive variation in host populations may influence hantavirus transmission dynamics within and between populations. Landscape structure, and particularly areas with a predominance of agricultural land and forest remnants, is expected to influence the proportion of hantavirus rodent hosts in the Atlantic Forest rodent community. Here, we tested this using 283 Atlantic Forest rodent capture records and geographically weighted models that allow us to test if predictors vary spatially. We also assessed the correspondence between proportions of hantavirus hosts in rodent communities and a human vulnerability to hantavirus infection index across the entire Atlantic Forest biome. We found that hantavirus host proportions were more positively influenced by landscape diversity than by a particular habitat or agricultural matrix type. Local small mammal diversity also positively influenced known pathogenic hantavirus host proportions, indicating that a plasticity to habitat quality may be more important for these hosts than competition with native forest dwelling species. We found a consistent positive effect of sugarcane and tree plantation on the proportion of rodent hosts, whereas defaunation intensity did not correlate with the proportion of hosts of potentially pathogenic hantavirus genotypes in the community, indicating that non-defaunated areas can also be hotspots for hantavirus disease outbreaks. The spatial match between host hotspots and human disease vulnerability was 17%, while coldspots matched 20%. Overall, we discovered strong spatial and land use change influences on hantavirus hosts at the landscape level across the Atlantic Forest. Our findings suggest disease surveillance must be reinforced in the southern and southeastern regions of the biome where the highest predicted hantavirus host proportion and levels of vulnerability spatially match. Importantly, our analyses suggest there may be more complex rodent community dynamics and interactions with human disease than currently hypothesized., Competing Interests: The authors have declared that no competing interests exist.

We performed a literature review in order to improve our understanding of how landscape and climate drivers affect HCPS outbreaks. Anthropogenic landscape changes such as forest loss, fragmentation and agricultural land uses are related with a boost in hantavirus reservoir species abundance and hantavirus prevalence in tropical areas, increasing HCPS risk. Additionally, higher precipitation, especially in arid regions, favors an increase in vegetational biomass, which augments the resources for reservoir rodents, also increasing HCPS risk. Although these relationships were observed, few studies described it so far, and the ones that did it are concentrated in few places. To guide future research on this issue, we build a conceptual model relating landscape and climate variables with HCPS outbreaks and identified research opportunities. We point out the need for studies addressing the effects of landscape configuration, temperature and the interaction between climate and landscape variables. Critical landscape thresholds are also highly relevant, once HCPS risk transmission can increase rapidly above a certain degree of landscape degradation. These studies could be relevant to implement preventive measures, creating landscapes that can mitigate disease spread risk.

Hantavirus Cardiopulmonary Syndrome (HCPS) is a disease caused by Hantavirus, which is highly virulent for humans. High temperatures and conversion of native vegetation to agriculture, particularly sugarcane cultivation can alter abundance of rodent generalist species that serve as the principal reservoir host for HCPS, but our understanding of the compound effects of land use and climate on HCPS incidence remains limited, particularly in tropical regions. Here we rely on a Bayesian model to fill this research gap and to predict the effects of sugarcane expansion and expected changes in temperature on Hantavirus infection risk in the state of São Paulo, Brazil. The sugarcane expansion scenario was based on historical data between 2000 and 2010 combined with an agro-environment zoning guideline for the sugar and ethanol industry. Future evolution of temperature anomalies was derived using 32 general circulation models from scenarios RCP4.5 and RCP8.5 (Representative greenhouse gases Concentration Pathways adopted by IPCC). Currently, the state of São Paulo has an average Hantavirus risk of 1.3%, with 6% of the 645 municipalities of the state being classified as high risk (HCPS risk ≥ 5%). Our results indicate that sugarcane expansion alone will increase average HCPS risk to 1.5%, placing 20% more people at HCPS risk. Temperature anomalies alone increase HCPS risk even more (1.6% for RCP4.5 and 1.7%, for RCP8.5), and place 31% and 34% more people at risk. Combined sugarcane and temperature increases led to the same predictions as scenarios that only included temperature. Our results demonstrate that climate change effects are likely to be more severe than those from sugarcane expansion. Forecasting disease is critical for the timely and efficient planning of operational control programs that can address the expected effects of sugarcane expansion and climate change on HCPS infection risk. The predicted spatial location of HCPS infection risks obtained here can be used to prioritize management actions and develop educational campaigns.

Hantavirus Pulmonary Syndrome (HPS) is a disease caused by Hantavirus, which are negative-sense RNA viruses in the family Bunyaviridae that are highly virulent to humans. Numerous factors modify risk of Hantavirus transmission and consequent HPS risk. Human-driven landscape change can foster transmission risk by increasing numbers of habitat generalist rodent species that serve as the principal reservoir host. Climate can also affect rodent population dynamics and Hantavirus survival, and a number of social factors can influence probability of HPS transmission to humans. Evaluating contributions of these factors to HPS risk may enable predictions of future outbreaks, and is critical to development of effective public health strategies. Here we rely on a Bayesian model to quantify associations between annual HPS incidence across the state of São Paulo, Brazil (1993-2012) and climate variables (annual precipitation, annual mean temperature), landscape structure metrics (proportion of native habitat cover, number of forest fragments, proportion of area planted with sugarcane), and social factors (number of men older than 14 years and Human Development Index). We built separate models for the main two biomes of the state (cerrado and Atlantic forest). In both biomes Hantavirus risk increased with proportion of land cultivated for sugarcane and HDI, but proportion of forest cover, annual mean temperature, and population at risk also showed positive relationships in the Atlantic forest. Our analysis provides the first evidence that social, landscape, and climate factors are associated with HPS incidence in the Neotropics. Our risk map can be used to support the adoption of preventive measures and optimize the allocation of resources to avoid disease propagation, especially in municipalities that show medium to high HPS risk (> 5% of risk), and aimed at sugarcane workers, minimizing the risk of future HPS outbreaks., Competing Interests: The authors have declared that no competing interests exist.