Abstract
Hantavirus pulmonary syndrome (HPS) is a severe emerging endemic disease of the Americas. Because hantavirus reservoirs are sylvatic rodents, HPS risk has been associated with occupational and recreational activities in natural and rural environments. The aim of this study was to analyze the risk of HPS in an endemic province of Argentina. For this, we explored the relationship between HPS cases occurring in Entre Ríos province between 2004 and 2015 and climate, vegetation, landscape, reservoir population, and rodent community characteristics by means of generalized linear models. We modeled HPS occurrence at each site, and both the incidence and number of cases grouped by department. The resulting best model of each analysis was applied in a GIS to build HPS risk maps. Risk of occurrence of HPS increased with tree cover and decreased with distance to rivers. We identified the south of Entre Ríos as the area with higher HPS risk, and therefore, where HPS prevention measures should be more urgently applied. Risk maps based on data available in the public domain are a useful tool that should be used by decision makers to concentrate surveillance and control efforts in those areas with highest HPS risk.
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References
Adams MJ, Lefkowitz EJ, King AM, Harrach B, Harrison RL, Knowles NJ, et al. (2017) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2017). Archives of Virology 162:2505-2538
Amaral CD, Costa GB, de Souza WM, Alves PA, Borges IA, Tolardo AL, et al. (2018) Silent Orthohantavirus circulation among humans and small mammals from Central Minas Gerais, Brazil. EcoHealth 15:577-589
Andreo V, Neteler M, Rocchini D, Provensal C, Levis S, Porcasi X, et al. (2014) Estimating hantavirus risk in Southern Argentina: a GIS-based approach combining human cases and host distribution. Viruses 6:201-222
Avenant N (2005) Barn owl pellets: a useful tool for monitoring small mammal communities. Belgian Journal of Zoology 135:39-43
Bonvicino CR, Bezerra AMR (2003) Use of regurgitated pellets of barn owl (Tyto alba) for inventorying small mammals in the Cerrado of Central Brazil. Studies on Neotropical Fauna and Environment 38:1-5
Boone JD, Otteson EW, McGwire KC, Villard P, Rowe JE, St Jeor S (1998). Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. The American Journal of Tropical Medicine and Hygiene 59:445-451
Brown JH, Ernest SM (2002) Rain and rodents: complex dynamics of desert consumers. Bioscience 52:979–987
Brown AD, Pacheco S (2006) Propuesta de actualización del mapa ecorregional de la Argentina. Pages 587 In: Brown A, Martinez Ortíz U, Acerbi M, Corcuera J (editors), La situación ambiental argentina, Buenos Aires: Fundación Vida Silvestre Argentina
Busch M, Kravetz FO (1992) Competitive interactions among rodents (Akodon azarae, Calomys laucha, C. musculinus and Oligoryzomys flavescens) in a two-habitat system. I. Spatial and numerical relationships. Mammalia 56:45-56
Busch M, Alvarez MR, Cittadino EA, Kravetz FO (1997) Habitat selection and interspecific competition in rodents in pampean agroecosystems. Mammalia 1:167-184
Busch M, Cavia R, Carbajo A, Bellomo C, Gonzalez Capria S, Padula P (2004) Spatial and temporal analysis of the distribution of Hantavirus Pulmonary Syndrome (HPS) in Buenos Aires Province, and its relation to rodent distribution, agricultural and demographic variables. Tropical Medicine & International Health 9:508-519
Calisher CH, Root JJ, Mills JN, Beaty BJ (2002) Assessment of ecologic and biologic factors leading to hantavirus pulmonary syndrome, Colorado, USA. Croatian Medical Journal 43:330-337
Carver S, Mills JN, Parmenter CA, Parmenter RR, Richardson KS, Harris RL, et al. (2015). Toward a Mechanistic Understanding of Environmentally Forced Zoonotic Disease Emergence: Sin Nombre Hantavirus. Bioscience 65:651-666
Carvalho de Oliveira R, Guterres A, Fernandes J, D’Andrea PS, Bonvicino CR, de Lemos ERS (2014a). Hantavirus reservoirs: current status with an emphasis on data from Brazil. Viruses 6:1929-1973
Carvalho de Oliveira R, Gentile R, Guterres A, Fernandes J, Teixeira BR, Vaz V, et al. (2014) Ecological study of hantavirus infection in wild rodents in an endemic area in Brazil. Acta Tropica 131:1-10
Cavia R, Cueto GR, Suárez OV (2009) Changes in rodent communities according to the landscape structure in an urban ecosystem. Landscape and Urban Planning 90:11-19
Crawley MJ (2012) The R book, West Sussex: John Wiley & Sons
Colombo VC, Brignone J, Sen C, Previtali MA, Martin ML, Levis S, et al. (2018) Orthohantavirus genotype Lechiguanas in Oligoryzomys nigripes (Rodentia: Cricetidae): new evidence of host-switching. Acta Tropica 191:133-138
de Oliveira SV, Fonseca LX, de Araújo Vilges KM, Maniglia FV, Pereira SV, de Caldas EP, et al. (2015) Vulnerability of Brazilian municipalities to hantavirus infections based on multi-criteria decision analysis. Emerging Themes in Epidemiology 12:1-8. https://doi.org/10.1186/s12982-015-0036-5
Donalisio MR, Peterson AT (2011) Environmental factors affecting transmission risk for hantaviruses in forested portions of southern Brazil. Acta Tropica 119:125-130
Eisen L, Eisen RJ (2007) Need for improved methods to collect and present spatial epidemiologic data for vectorborne diseases. Emerging Infectious Diseases 13:1816-1820
Engler P, Rodríguez M, Cancio R, Handloser M, Vera L (2008) Zonas Agro Económicas Homogéneas: Entre Ríos. Estudios socioeconómicos de la sustentabilidad de los sistemas de producción y recursos. Instituto Nacional de Tecnología Agropecuaria, Buenos Aires Available: https://inta.gob.ar/sites/default/files/script-tmp-inta_zonas_agroeconmicas_homogneas__entre_rios.pdf [accessed December 12, 2016]
Estrada-Peña A, Ostfeld RS, Peterson AT, Poulin R, de la Fuente J (2014) Effects of environmental change on zoonotic disease risk: an ecological primer. Trends in Parasitology 30:205-214
Forbes KM, Sironen T,Plyusnin A (2018). Hantavirus maintenance and transmission in reservoir host populations. Current opinion in virology 28:1-6
Glass GE, Cheek JE, Patz JA, Shields TM, Doyle TJ, Thoroughman DA, et al. (2000) Using remotely sensed data to identify areas at risk for hantavirus pulmonary syndrome. Emerging Infectious Diseases 6:238-247
Glass GE, Shields T, Cai B, Yates TL, Parmenter R (2007). Persistently highest risk areas for hantavirus pulmonary syndrome: potential sites for refugia. Ecological Applications 17:129-139
Gómez Villafañe IE, Miñarro F, Valenzuela L, Bilenca D (2009) Experimental assessment of rodent control on two poultry farms of central Argentina. Journal of Applied Poultry Research 18:622-629
Gómez Villafañe IE, Expósito Y, San Martín Á, Picca P, Busch M (2012) Rodent diversity and habitat use in a protected area of Buenos Aires province, Argentina. Revista Mexicana de Biodiversidad 83:762-771
Gorosito IL, Douglass RJ (2017) A damped precipitation‐driven, bottom‐up model for deer mouse population abundance in the northwestern United States. Ecology and Evolution 7:11113-11123
Happold D, Happold M (1986) Small mammals of Zomba Plateau, Malawi, as assessed by their presence in pellets of the grass owl, Tyto capensis, and by live‐trapping. African Journal of Ecology 24:77-87
Heisler LM, Somers CM, Poulin RG (2016) Owl pellets: a more effective alternative to conventional trapping for broad‐scale studies of small mammal communities. Methods in Ecology and Evolution 7:96-103
Hijmans RJ, Cameron S, Parra J, Jones P, Jarvis A, Richardson K (2005) WorldClim version 1. Available:http://www.worldclim.org/version1 [accessed December 1, 2016]
IGN (2013) GIS layers. Available: http://ign.gob.ar/NuestrasActividades//InformacionGeoespacial/CapasSIG [accessed March 2, 2015]
INDEC (Argentina´s National Institute of Statistics and Censuses; 2010) National Census of population, homes and dwellings 2010. Available: http://www.indec.gov.ar [accessed June 6, 2016]
Jahangir E, Irazola V, Rubinstein A (2012) Need, enabling, predisposing, and behavioral determinants of access to preventative care in Argentina: analysis of the national survey of risk factors. PloS One 7:1-6. https://doi.org/10.1371/journal.pone.0045053
Jonsson CB, Figueiredo LTM, Vapalahti O (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical Microbiology Reviews 23:412-441
Kallio E, Klingstrom J, Gustafsson E, Manni T, Vaheri A, Henttonen H, et al. (2006) Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. Journal of General Virology 87:2127–2134
Kruger DH, Figueiredo LTM, Song J-W, Klempa B (2015) Hantaviruses—Globally emerging pathogens. Journal of Clinical Virology 64:128-136
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159-174
Lovera R, Fernandez SM, Cavia R (2015) Wild small mammals in intensive milk cattle and swine production systems. Agriculture, Ecosystems & Environment 202:251-259
Luis AD, Douglass RJ, Mills JN, Bjørnstad ON (2010). The effect of seasonality, density and climate on the population dynamics of Montana deer mice, important reservoir hosts for Sin Nombre hantavirus. Journal of Animal Ecology 79:462-470
Maroli M, Vadell MV, Iglesias A, Padula PJ, Gómez Villafañe IE (2015) Daily movements and microhabitat selection of hantavirus reservoirs and other sigmodontinae rodent species that inhabit a protected natural area of Argentina. EcoHealth 12:421–431
Maroli M, Vadell MV, Padula P, Gómez Villafañe IE (2018) Rodent Abundance and Hantavirus Infection in Protected Area, East-Central Argentina. Emerging Infectious Diseases 24:131-134
Martinez VP, Bellomo C, San Juan J, Pinna D, Forlenza R, Elder M, Padula PJ (2005) Person-to-person transmission of Andes virus. Emerging infectious diseases 11:1848-1853
Martinez VP, Bellomo CM, Cacace ML, Suárez P, Bogni L, Padula PJ (2010) Hantavirus pulmonary syndrome in Argentina, 1995–2008. Emerging Infectious Diseases 16: 1853–1860
Massa C, Teta P, Cueto GR (2013) Effects of regional context and landscape composition on diversity and composition of small rodent assemblages in Argentinian temperate grasslands and wetlands. Mammalia 78:371-382
Massa C, Gabelli FM, Cueto GR (2015) Using GPS tracking to determine movement patterns and foraging habitat selection of the common barn-owl (Tyto alba). El hornero 30:7-12
Maurice AdS, Ervin E, Schumacher M, Yaglom H, VinHatton E, Melman S, et al. (2017) Exposure characteristics of hantavirus pulmonary syndrome patients, United States, 1993–2015. Emerging Infectious Diseases 23:733-739
Mills JN, Ellis BA, McKee KT, Maiztegui JI, Childs JE (1991) Habitat associations and relative densities of rodent populations in cultivated areas of central Argentina. Journal of Mammalogy 72: 470-479
Mills JN, Amman BR, Glass GE (2010). Ecology of hantaviruses and their hosts in North America. Vector-Borne and Zoonotic Diseases 10:563-574
Moons KG, Kengne AP, Woodward M, Royston P, Vergouwe Y, Altman DG, et al. (2012) Risk prediction models: I. Development, internal validation, and assessing the incremental value of a new (bio) marker. Heart 98:683-690INDEC (National Institute of Statistics and Censuses) 2010)National Census of population, homes and dwellings 2010. Available: http://www.indec.gov.ar [accessed June 6, 2016]
Núñez JJ, Fritz CL, Knust B, Buttke D, Enge B, Novak MG, et al. (2014) Hantavirus infections among overnight visitors to Yosemite National Park, California, USA, 2012. Emerging Infectious Diseases 20:386-393
Nsoesie EO, Mekaru SR, Ramakrishnan N, Marathe MV, Brownstein JS (2014) Modeling to predict cases of hantavirus pulmonary syndrome in Chile. PLoS Neglected Tropical Diseases 8:1-10. 10.1371/journal.pntd.0002779
O´Donnell O (2007) Access to health care in developing countries: breaking down demand side barriers. Cadernos Saúde Pública 23:2820-2834
Padula P J, Edelstein A, Miguel SDL, Lopez N M, Rossi CM, Rabinovich RD (1998) Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241: 323-330
Parmenter RR, Brunt JW, Moore DI, Ernest S (1993) The hantavirus epidemic in the southwest: rodent population dynamics and the implications for transmission of hantavirus-associated adult respiratory distress syndrome (HARDS) in the four corners region. Sevilleta LTER report #41 for the Federal Centers for Disease Control and Prevention 1-10
Peters CJ, Khan AS (2002) Hantavirus pulmonary syndrome: the new American hemorrhagic fever. Clinical Infectious Diseases 34:1224-1231
Peters DH, Garg A, Bloom G, Walker DG, Brieger WR, Rahman MH (2008) Poverty and access to health care in developing countries. Annals of the New York Academy of Sciences 1136:161-171
Prist PR, Uriarte M, Tambosi LR, Prado A, Pardini R, Metzger JP (2016) Landscape, environmental and social predictors of Hantavirus risk in São Paulo, Brazil. PLoS ONE 11:1-18. https://doi.org/10.1371/journal.pone.0163459
Prist PR, D’Andrea PS, Metzger JP (2017). Landscape, climate and hantavirus cardiopulmonary syndrome outbreaks. EcoHealth 14:614-629
R-Core-Team (2013) R: A Language and Environment for Statistical Computing. Vienna. Available at: http://www.r-project.org
Scheibler DR, Christoff AU (2007) Habitat associations of small mammals in southern Brazil and use of regurgitated pellets of birds of prey for inventorying a local fauna Brazilian Journal of Biology 67:619-625
Steyerberg EW, Harrell Jr FE, Borsboom GJ, Eijkemans M, Vergouwe Y, Habbema JDF (2001) Internal validation of predictive models: efficiency of some procedures for logistic regression analysis. Journal of Clinical Epidemiology 54:774-781
Townshend J, Hansen M, Carroll M, DiMiceli C, Sohlberg R, Huang C (2011) User Guide for the MODIS Vegetation Continuous Fields product Collection 5 Version 1. Available:http://glcf.umd.edu/library/guide/VCF_C5_UserGuide_Dec2011.pdf [accessed May 11, 2015]
Udrizar Sauthier WO, Abba AM, Udrizar Sauthier DE (2010) Nests of Oligoryzomys sp. and Holochilus brasiliensis (Rodentia, Cricetidae) in eastern Entre Ríos Province, Argentina. Mastozoología Neotropical 17:207-211
Vadell MV, Bellomo C, San Martín A, Padula P, Gómez Villafañe IE (2011). Hantavirus ecology in rodent populations in three protected areas of Argentina. Tropical Medicine & International Health 16:1342–1352
Vadell MV, García Erize F, Gómez Villafañe IE (2017) Evaluation of habitat requirements of small rodents and effectiveness of an ecologically-based management in a hantavirus-endemic natural protected area in Argentina. Integrative Zoology 12:77–94
Vadell MV, Gómez Villafañe IE (2016). Environmental Variables Associated with Hantavirus Reservoirs and Other Small Rodent Species in Two National Parks in the Paraná Delta, Argentina: Implications for Disease Prevention. EcoHealth 13: 248-260
Verner D (2006) Rural poor in rich rural areas: poverty in rural Argentina. World Bank. Available:http://econ.worldbank.org [accessed January 28, 2017]
Vial PA, Valdivieso F, Mertz G, Castillo C, Belmar E, Delgado I, et al. (2006) Incubation period of hantavirus cardiopulmonary syndrome. Emerging Infectious Diseases 12:1271-1273
Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, et al. (2002) The ecology and evolutionary history of an emergent disease: Hantavirus Pulmonary Syndrome. Bioscience 52: 989-998
Young JC, Hansen GR, Graves TK, Deasy MP, Humphreys JG, Fritz CL, et al. (2000) The incubation period of hantavirus pulmonary syndrome. The American Journal of Tropical Medicine and Hygiene 62:714-717
Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data, Nueva York: Springer
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1:3-14
Acknowledgements
We are thankful to the National Health Ministry of Argentina (Ministerio de Salud de la Nación) for providing the data on confirmed HPS cases and, to the anonymous reviewers for improving the manuscript with their comments and suggestions.
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Vadell, M.V., Carbajo, A.E., Massa, C. et al. Hantavirus Pulmonary Syndrome Risk in Entre Ríos, Argentina. EcoHealth 16, 558–569 (2019). https://doi.org/10.1007/s10393-019-01425-3
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DOI: https://doi.org/10.1007/s10393-019-01425-3