[Source: PLoS Neglected Tropical Diseases, full page: (LINK). Abstract, edited.]
OPEN ACCESS / PEER-REVIEWED / RESEARCH ARTICLE
Hantavirus host assemblages and human disease in the Atlantic Forest
Renata L. Muylaert , Ricardo Siqueira Bovendorp, Gilberto Sabino-Santos Jr, Paula R. Prist, Geruza Leal Melo, Camila de Fátima Priante, David A. Wilkinson, Milton Cezar Ribeiro, David T. S. Hayman
Published: August 12, 2019 / DOI: https://doi.org/10.1371/journal.pntd.0007655 / This is an uncorrected proof.
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.
Hantaviruses cause disease in people, mainly following transmission from wild rodents to people through contact with infected excreta. Wild rodents use different habitats, and many survive even in anthropogenically changed environments, but to an unknown extent. The objective of our study was to understand how these rodents respond to habitat change in the landscape, to biodiversity and to climate. We measured the proportion of pathogenic hantavirus hosts in the rodent community. We then investigated the spatial correspondence between this proportion and a vulnerability to pathogenic hantavirus infection index in humans within the Atlantic Forest. We found 12 well represented species of rodents that can carry at least one hantavirus genotype. Despite high variation in the host proportion data, the peaks of human vulnerability to disease occurs at higher levels of habitat diversity in the landscape, intermediate levels of rainfall, and areas with less than 15 species in the local small mammal community. Our results suggest hantavirus surveillance and prevention measures are needed in the south and south-east regions of Brazil where highest host proportions and levels of vulnerability spatially match.
Citation: Muylaert RL, Bovendorp RS, Sabino-Santos G Jr, Prist PR, Melo GL, Priante CdF, et al. (2019) Hantavirus host assemblages and human disease in the Atlantic Forest. PLoS Negl Trop Dis 13(8): e0007655. https://doi.org/10.1371/journal.pntd.0007655
Editor: Colleen B. Jonsson, University of Tennessee Health Science Center College of Medicine Memphis, UNITED STATES
Received: January 17, 2019; Accepted: July 24, 2019; Published: August 12, 2019
Copyright: © 2019 Muylaert et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: The input data is provided in S2 Table. All relevant data are within the manuscript, its Supporting Information files and in the ATLANTIC series files. The data underlying the results presented in the study is available at: https://github.com/LEEClab/Atlantic_series/tree/master/ATLANTIC_SMALL_MAMMALS. Atlantic Forest data is available at: https://github.com/LEEClab/ATLANTIC-limits.
Funding: This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo FAPESP to RLM (https://bv.fapesp.br/pt/pesquisador/176171/renata-de-lara-muylaert/) (2015/17739-4, 2017/21816-0), GSSJ (https://bv.fapesp.br/pt/pesquisador/79234/gilberto-sabino-dos-santos-junior/) (2017/21816-0), RSB (https://bv.fapesp.br/pt/pesquisador/76113/ricardo-siqueira-bovendorp/) (2013/25441-0), PRP (2017/11666-0), and MCR (https://bv.fapesp.br/pt/pesquisador/176172/milton-cezar-ribeiro/) (2013/50421-2); Royal Society Te Apārangi Rutherford Discovery Fellowship to DTSH (https://royalsociety.org.nz/what-we-do/funds-and-opportunities/rutherford-discovery-fellowships/rutherford-discovery-fellowship-recipients/david-hayman/) (RDF-MAU1701); Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPQ to MCR (425746/2016-0); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior CAPES to MCR (312045/2013-1; 312292/2016-3) and RLM (33004137); and New Zealand Food Safety Science and Research Centre (https://www.nzfssrc.org.nz/) to DW (2019). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Keywords: Orthohantavirus; Hantavirus; Rodents; Human; Brazil.