A Review of Mammarenaviruses and Rodent Reservoirs in the Americas

EcoHealth - Tập 19 - Trang 22-39 - 2022
Gloria Tapia-Ramírez1, Consuelo Lorenzo1, Darío Navarrete2, Arturo Carrillo-Reyes3, Óscar Retana4, Rocío Carrasco-Hernández5
1Departamento de Conservación de la Biodiversidad, El Colegio de la Frontera Sur, San Cristóbal de las Casas, Mexico
2Departamento de Observación de la Tierra, Atmósfera y Océano, El Colegio de La Frontera Sur, San Cristóbal de Las Casas, Mexico
3Facultad de Ingeniería, Universidad de Ciencias y Artes de Chiapas, Tuxtla Gutiérrez, Mexico
4Centro de Estudios en Desarrollo Sustentable, Universidad Autónoma de Campeche, San Francisco de Campeche, Mexico
5Centro de Investigación en Enfermedades Infecciosas, Instituto Nacional de Enfermedades Respiratorias Ismael Cosío Villegas, Ciudad de México, Mexico

Tóm tắt

In the Americas, infectious viral diseases caused by viruses of the genus Mammarenavirus have been reported since the 1960s. Such diseases have commonly been associated with land use changes, which favor abundance of generalist rodent species. In the Americas—where the rates of land use change are among the highest worldwide—at least 1326 of all 2277 known rodent species have been reported. We conducted a literature review of studies between 1960 and 2020, to establish the current and historical knowledge about genotypes of mammarenaviruses and their rodent reservoirs in the Americas. Our overall goal was to show the importance of focusing research efforts on the American continent, since the conditions exist for future viral hemorrhagic fever (VHF) outbreaks caused by rodent-borne viruses, in turn, carried by widely distributed rodents. We found 47 species identified down to the species level, and one species identified only down to the genus level (Oryzomys sp.), reported in the Americas as reservoirs of mammarenaviruses, most these are ecological generalists. These species associate with 29 genotypes of Mammarenavirus, seven of which have been linked to VHFs in humans. We also highlight the need to monitor these species, in order to prevent viral disease outbreaks in the region.

Tài liệu tham khảo

Albariño CG, Palacios G, Khristova ML et al (2010) High diversity and ancient common ancestry of Lymphocytic Choriomeningitis virus. Emerging Infectious Diseases Journal 16:1093–1100. https://doi.org/10.3201/eid1607.091902 Andreo V, Neteler M, Rocchini D et al (2014) Estimating hantavirus risk in Southern Argentina: A GIS-based approach combining human cases and host distribution. Viruses 6:201–222. https://doi.org/10.3390/v6010201 Arata AA, Gratz NG (1975) The structure of rodent faunas associated with arenaviral infections. Buletin of World Health Organization 52:621–627 Arribalzaga RA (1955) Una nueva enfermedad epidémica a germen desconocido: Hipertermia nefrotóxica, leucopénica y enantemática. Dia Médico 37:1204–1210 Barragán F, Retana OG, Naranjo EJ (2007) The rodent trade of tzeltal indians of Oxchuc, Chiapas, Mexico. Human Ecology 35:769–773. https://doi.org/10.1007/s10745-007-9116-7 Barry M, Bia F, Cullen M (1994) Dembry L (1994) Arenavirus Infection—Connecticut. Journal of American Medical Association 272(13):998–999 Bausch DG, Mills JN (2014) Arenaviruses: Lassa Fever, Lujo Hemorrhagic Fever, Lymphocytic Choriomeningitis, and the South American Hemorrhagic Fevers. In: Kaslow RA, Stanberry LR, LeDuc JW (eds) Viral Infections of Humans. Springer, New York, US, pp 147–191 Bennett SG, Milazzo ML, Webb J, Fulhorst CF (2000) Arenavirus antibody in rodents indigenous to coastal southern California. American Journal of Tropical Medicine and Hygiene 62:626–630. https://doi.org/10.4269/ajtmh.2000.62.626 Bisordi I, Levis S, Maeda AY, Suzuki A, Nagasse-Sugahara TK, De Souza RP, Pereira LE, García JB, Cerroni MP, e Silva FDA, dos Santos CLS, da Fonseca BAL (2015) Pinhal virus, a new Arenavirus isolated from Calomys tener in Brazil. Vector-Borne and Zoonotic Disease 15:694–700 Bowen MD, Clarence JP, Mills JN, Nichol ST (1996) Oliveros virus: a novel Arenavirus from Argentina. Virology 217:362–366 Brehm MA, Pinto AK, Daniels KA et al (2002) T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nature Immunology 3:627–634. https://doi.org/10.1038/ni806 Byrd RG, Cone LA, Commess BC, Williams-Herman D, Rowland JM, Lee B, Fitzgibbons MW, Glaser CA, Jay MT, Fritz C, Ascher MS, Cheung M, Kramer VL, Reilly K, Vugia DJ, Fulhorst CF, Milazzo ML, Charrel RN (2000) Fatal illnesses associated with a New World Arenavirus, California, 1999–2000. Journal of American Medical Association 284:1237–1238. https://doi.org/10.1001/jama.284.10.1237 Cajimat MNB, Milazzo ML, Bradley RD, Fulhorst CF (2007) Catarina virus, an arenaviral species principally associated with Neotoma micropus (Southern plains woodrat) in Texas. American Journal of Tropical Medicine and Hygiene 77:732–736. https://doi.org/10.4269/ajtmh.2007.77.732 Cajimat MNB, Milazzo ML, Borchert JN, Abbott KD, Bradley RD, Fulhorst CF (2008) Diversity among Tacaribe serocomplex viruses (Family Arenaviridae) naturally associated with the Mexican woodrat (Neotoma mexicana). Virus Research 133:211–217 Cajimat MNB, Milazzo ML, Bradley RD, Fulhorst CF (2012) Ocozocoautla de Espinosa virus and Hemorrhagic Fever, Mexico. Emerging Infectious Diseases Journal 18:401–405 Calisher CH, Tzianabo T, Lord RD, Coleman PH (1970) Tamiami virus, a new member of Tacaribe group. American Journal of Tropical Medicine and Hygiene 19:520–526 Carballal G, Videla CM, Merani MS (1988) Epidemiology of Argentine Hemorrhagic Fever. European Journal of Epidemiology 4:259–274 Carlson CJ, Zipfel CM, Garnier R, Bansal S (2019) Global estimates of mammalian viral diversity accounting for host sharing. Nature Ecology & Evolution 3:1070–1075. https://doi.org/10.1038/s41559-019-0910-6 Carrasco-Hernandez R, Jácome R, López Vidal Y, Ponce de León S (2017) Are RNA viruses candidate agents for the next global pandemic? A Review. Institute for Laboratory Animal Research Journal 58(3):343–358. https://doi.org/10.1093/ilar/ilx026 Carver S, Mills JN, Parmenter CA et al (2015) Toward a mechanistic understanding of environmentally forced zoonotic disease emergence: Sin Nombre Hantavirus. Bioscience 65:651–666. https://doi.org/10.1093/biosci/biv047 Castellar A, Guevara M, Rodas JD, Lodoño AF, Arroyave E, Díaz FJ, Levis S, Blanco PJ (2017) Primera evidencia de infección por el virus de la Coriomeningitis Linfocítica (Arenavirus) en roedores Mus musculus capturados en la zona urbana del municipio de Sincelejo, Sucre. Colombia. Biomédica 37:75–85 CDC (2013) Old World/New World Arenaviruses. Viral Hemorrhagic Fevers (VHFs). Available:https://www.cdc.gov/vhf/virus-families/arenaviruses.html [accessed July 2, 2020] Charrel RN, De Lamballerie X, Fulhorst CF (2001) The Whitewater Arroyo virus: Natural evidence for genetic recombination among Tacaribe serocomplex viruses (family Arenaviridae). Virology 283:161–166. https://doi.org/10.1006/viro.2001.0874 Charrel RN, Feldmann H, Fulhorst CF, Khelifa R, de Chesse R, de Lamballerie X (2002) Phylogeny of New World arenaviruses based on the complete coding sequences of the small genomic segment identified an evolutionary lineage produced by intrasegmental recombination. Biochemical and Biophysical Research Communications 296:1118–1124 Charrel RN, de Lamberrie X (2010) Zoonotic aspects of Arenavirus infections. Veterinary Microbiology 140:213–220 Chiappero MB, Piacenza MF, Provensal MC, Calderón GE, Gardenal CN, Polop JJ (2018) Effective population size differences in Calomys musculinus, the host of Junín virus: their relationship with the epidemiological history of Argentine Hemorrhagic Fever. American Journal of Tropical Medicine and Hygiene 99:445–450. https://doi.org/10.4269/ajtmh.17-0838 Childs JE, Glass GE, Korch GW, Ksiazek TG, Leduc JW (1992) Lymphocytic Choriomeningitis virus infection and house mouse (Mus musculus) distribution in urban Baltimore. American Journal of Tropical Medicine and Hygiene 47:27–34 Coimbra TLM, Nassa ES, Burattini MN, Madia de Souza LT, Ferreira IB, Rocco IM, Travassos da Rosa APA, Vasconcelos PFC, Pinheiro FP, LeDuc JW, Rico-Hesse R, Gonzalez JP, Jahrling P, Tesh RB (1994) New arenaviruses isolated in Brazil. Lancet 343:391–392 Crespo JA (1966) Ecología de una comunidad de roedores silvestres en el Partido de Rojas, Provincia de Buenos Aires. Buenos Aires: Comisión Nacional Coordinadora para Estudio y Lucha contra la Fiebre Hemorrágica Argentina. Secretaría de Estado de Salud Pública Cuthill JH, Charleston MA (2013) A simple model explains the dynamics of preferential host switching among mammal rna viruses. Evolution 67:980–990. https://doi.org/10.1111/evo.12064 de Mello Malta F, Amgarten D, de Seixas Santos Nastri AC, Ho YL, Casadio LVB, Basqueira M, Selegatto G, Cervato MC, Duarte-Neto AN, Higashino HR, Medeiros FAF, Gendler JLPL, Levin AS, Pinho JRR (2020) Sabiá virus-like Mammarenavirus in patient with fatal hemorrhagic fever, Brazil, 2020. Emerging Infectious Diseases Journal 26:1332–1334. https://doi.org/10.3201/EID2606.200099 de Villafañe G, Bonaventura SM, Bellocq MI, Percich RE (1988) Habitat selection, social structure, density and predation in populations of Cricetine rodents in the Pampa region of Argentina and the effects of agricultural practices on them. Mammalia 52:339–360. https://doi.org/10.1515/mamm-1988-0305 de Villafañe G, Bonaventura SM (1987) Ecological studies in crop fields of the endemic area of Argentine Hemorrhagic fever. Calomys musculinus movements in relation to habitat and abundance. Mammalia 51:233–248 de Villafañe G, Kravetz FO, Donald O, Percich R, Knecher L, Torres MP, Fernández N (1977) Dinámica de las comunidades de roedores en agroecosistemas Pampásicos. Revista Medicina 37:128–140 Delgado S, Erickson BR, Agudo R, Blair PJ, Vallejo E, Albariño CG, Vargas J, Comer JA, Rollin PE, Ksiazek TG, Olson JG, Nichol ST (2008) Chapare virus, a newly discovered Arenavirus isolated from a fatal hemorrhagic fever case in Bolivia. PLoS Pathogens 4:1–6. https://doi.org/10.1371/journal.ppat.1000047 Downs WG, Anderson CR, Spence L, Aitken THG, Greenhall AH (1963) Tacaribe virus, a new agent isolated from Artibeus bats and mosquitos in Trinidad, West Indies. American Journal of Tropical Medicine and Hygiene 12:640–646 Alliance E (2019) Infectious disease emergence and economics of altered landscapes (IDEEAL). New York: EcoHealth Alliance/USAID/RDMA Ellis BA, Mills JN, Childs JE, Muzzini MC, McKee KT, Enria DA, Glass GE (1997) Structure and floristics of habitats associated with five rodent species in an agroecosystem in Central Argentina. Journal of Zoology 243:437–460. https://doi.org/10.1111/j.1469-7998.1997.tb02794.x Enserink M (2000) New Arenavirus blamed for recent deaths in California. Science 289:842–843. https://doi.org/10.1126/science.289.5481.842 Escalera-Antezana JP, Rodriguez-Villena OJ, Arancibia-Alba AW, Alvarado-Arnez LE, Bonilla-Aldana DK, Rodríguez-Morales AJ (2020) Clinical features of fatal cases of Chapare virus hemorrhagic fever originating from rural La Paz, Bolivia, 2019: A cluster analysis. Travel Medicine and Infectious Disease 33:1–6. https://doi.org/10.1016/j.tmaid.2020.101589 Everard M, Johnston P, Santillo D, Staddon C (2020) The role of ecosystems in mitigation and management of Covid-19 and other zoonoses. Environmental Science and Policy 111:7–17. https://doi.org/10.1016/j.envsci.2020.05.017 Fernandes J, de Oliveira RC, Guterres A, de Carvalho Serra F, Bonvicino CR, D’Andrea PS, Cunha RV, Levis S, de Lemos ERS (2015) Co-circulation of Clade C New World Arenaviruses: New geographic distribution and host species. Infection, Genetics and Evolution 33:242–245. https://doi.org/10.1016/j.meegid.2015.05.010 Fernandes J, de Oliveira RC, Guterres A, Barreto-Vieira DF, Terças ACP, Teixeira BR, da Silva MAN, Caldas GC, de Oliveira Coelho JMC, Barth OM, D’Andrea PS, Bonvicino CR, de Lemos ERS (2018) Detection of Latino virus (Arenaviridae: Mammarenavirus) naturally infecting Calomys callidus. Acta Tropica 179:17–24. https://doi.org/10.1016/j.actatropica.2017.12.003 Fernandes J, Guterres A, de Oliveira RC, Jardim R, Dávila AMR, Hewson R, De Lemos ERS (2019) Aporé virus, a novel Mammarenavirus (Bunyavirales: Arenaviridae) related to highly pathogenic virus from South America. Memorias Do Instituto Oswaldo Cruz 114:1–3. https://doi.org/10.1590/0074-02760180586 Foster ES, Signs KA, Marks DR et al (2006) Lymphocytic choriomeningitis in Michigan. Emerging Infectious Diseases Journal 12:851–853. https://doi.org/10.3201/eid1205.050794 Fulhorst CF, Bowen MD, Ksiazek TG, Rollin PE, Nichol ST, Kosoy MY, Peters CJ (1996) Isolation and characterization of Whitewater Arroyo virus, a novel North American Arenavirus. Virology 224:114–120. https://doi.org/10.1006/viro.1996.0512 Fulhorst CF, Bowen MD, Salas RA, de Manzione N, Duno G, Utrera A, Ksiazek TG, Peters CJ, Nichol ST, de Miller E, Tovar D, Ramos B, Vasquez C, Tesh RB (1997) Isolation and characterization of Pirital virus, a newly discovered South American Arenavirus. American Journal of Tropical Medicine and Hygiene 56:548–553 Fulhorst CF, Bennett SG, Milazzo ML, Murray HL, Webb JP, Cajimat NB, Bradley RD (2002) Bear Canyon virus: an Arenavirus naturally associated with the California mouse (Peromyscus californicus). Emerging Infectious Diseases Journal 8:717–721 García-Peña GE, Rubio AV, Mendoza H, Fernández M, Milholland MT, Aguirre AA, Suzán G, Zambrana-Torrelio C (2021) Land-use change and rodent-borne diseases: Hazards on the shared socioeconomic pathways. Philosophical Transactions of the Royal Society B Biological Sciences 376:1–11. https://doi.org/10.1098/rstb.2020.0362 Geoghegan JL, Duchene S, Holmes EC (2017) Comparative analysis estimates the relative frequence of co-divergence and cross-species transmission within viral families. PLoS Pathogens 13:1–11 Geoghegan JL, Senior AM, Di Giallonardo F, Holmes EC (2016) Virological factors that increase the transmissibility of emerging human viruses. Proceedings of the National Academy of Sciences 113:4170–4175. https://doi.org/10.1073/pnas.1521582113 Goldsmith RS, Shields KP (1971) Epidemic in Southern Mexico of disease resembling virus haemorrhagic fevers. Lancet 298(7716):151–154. https://doi.org/10.1016/s0140-6736(71)92320-8 González J, Emonet S, de Lamballerie X, Charrel RN (2007) Arenaviruses. Current Topics in Microbiology and Inmunology 315:253–288 Greer A, Ng V, Fisman D (2008) Climate change and infectious diseases in North America: the road ahead. Canadian Medical Association Journal 178:715–722 Gubler DJ, Reiter P, Ebi KL, Yap W, Nasci R, Patz JA (2001) Climate variability and change in the United States: potential impacts on vector-and rodent-borne diseases. Environmental Health Perspectives 109:223–233 Han BA, Schmidt JP, Bowden SE, Drake JM (2015) Rodent reservoirs of future zoonotic diseases. Proceeding of National Academy of Sciences 112:7039–7044 Inizan CC, Cajimat MNB, Milazzo ML, Barragán-Gomez A, Bradley RD, Fulhorst CF (2010) Genetic evidence for a Tacaribe serocomplex virus, Mexico. Emerging Infectious Diseases Journal 16:1007–1010. https://doi.org/10.3201/eid1606.091648 Irwin NR, Bayerlová M, Missa O, MartÍnková N (2012) Complex patterns of host switching in New World arenaviruses. Molecular Ecology 21:4137–4150. https://doi.org/10.1111/j.1365-294X.2012.05663.x IUCN (2020) The IUCN Red List of Threatened Species. Version 2020–1. Available:https://www.iucnredlist.org/ [accessed Jun 10, 2020] Johnson KM, Weibenga NH, Mackensie RB, Kuns ML, Tauraso NM, Shelokov A, Webb PA, Justines G, Beye HK (1963) Virus isolations from human cases of hemorrhagic fever in Bolivia. Proceedings of the Society for Experimental Biology and Medicine 118:113–118 Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993. https://doi.org/10.1038/nature06536 Kravetz FE, Percich RE, Zuleta G, Calello MA, Weisembacher MC (1986) Distribution of Junin virus and its reservoirs. A tool for Argentine Hemorrhagic Fever risk evaluation in non-endemic areas. Interciencia 11:185–188 Laenen L, Vergote V, Calisher CH, Klempa B, Klingström J, Kuhn JH, Maes P (2019) Hantaviridae: Current classification and future perspectives. Viruses 11:1–17. https://doi.org/10.3390/v11090788 Lavergne A, de Thoisy B, Tirera S, Donato D, Bouchier C, Catzeflis F, Lacoste V (2016) Identification of Lymphocytic Choriomeningitis mammarenavirus in house mouse (Mus musculus, Rodentia) in French Guiana. Infection, Genetics and Evolution 37:225–230 Lavergne A, de Thoisy B, Donato D, Guidez A, Matheus S, Catzeflis F, Lacoste V (2015) Patawa virus, a new Arenavirus hosted by forest rodents in French Guiana. Ecohealth 12:339–346 Luis AD, O’Shea TJ, Hayman DTS, Wood JLN, Cunningham AA, Gilbert AT, Mills JN, Webb CT (2015) Network analysis of host-virus communities in bats and rodents reveals determinants of cross-species transmission. Ecology Letters 18:1153–1162. https://doi.org/10.1111/ele.12491 Mackenzie RB, Beye HK, Valverde L, Garrón H (1964) Epidemic Hemorrhagic Fever in Bolivia I. A Preliminary report of the epidemiologic and clinical findings in a new epidemic area in South America. American Journal of Tropical Medicine and Hygiene 13:620–625 Maroli M, Vadell MV, Padula P, Gómez Villafañe IE (2018) Rodent abundance and Hantavirus infection in protected area, east-central Argentina. Emerging Infectious Diseases Journal 24(1):131–134 Mattar S, Guzmán C, Arrazola J, Soto E, Barrios J, Pini N, Levis S, Salazar-Bravo J, Mills JN (2011) Antibody to arenaviruses in rodents Caribbean Colombia. Emerging Infectious Diseases Journal 17:1315–1317 Mendoza H, Rubio AV, García-Peña GE, Suzán G, Simonetti JA (2020) Does land-use change increase the abundance of zoonotic reservoirs? Rodents say yes. European Journal of Wildlife Research 66:1–6. https://doi.org/10.1007/s10344-019-1344-9 Milazzo ML, Cajimat MNB, Haynie ML, Abbott KD, Bradley RD, Fulhorst CF (2008) Diversity among Tacaribe serocomplex viruses (Family Arenaviridae) naturally associated with the white-throated woodrat (Neotoma albigula) in the southwestern United States. Vector-Borne and Zoonotic Diseases 8:523–540 Milazzo ML, Barragán-Gomez A, Hanson JD, Estrada-Franco JG, Arellano E, González-Cózatl FX, Fernández-Salas I, Ramirez-Aguilar F, Rogers DS, Bradley RD, Fulhorst CF (2010) Antibodies to Tacaribe serocomplex viruses (Family Arenaviridae, Genus Arenavirus) in Cricetid rodents from New Mexico, Texas, and Mexico. Vector-Borne and Zoonotic Diseases 10:629–637 Milholland MT, Castro-Arellano I, Suzan G, Garcia-Pena GE, Lee TE Jr, Rohde RE, Alonso Aguirre A, Mills JN (2018) Global diversity and distribution of Hantaviruses and their hosts. Ecohealth 15:163–208 Mills JN (2005) Regulation of rodent-borne in the natural host: implications for human disease. In: Peters CJ, Calisher CH (eds) Infectious diseases from nature: mechanisms of viral emergence and persistence, Springer, Viena, pp 45–57. https://doi.org/10.1007/3-211-29981-5_5 Mills JN, Schmidt K, Ellis BA, Calderón G, Enría DA, Ksiazek TG (2007) A longitudinal study of Hantavirus infection in three sympatric reservoir species in agroecosystems on the Argentine Pampa. Vector-Borne and Zoonotic Diseases 7:229–240 Mills JN, Childs JE (1998) Ecologic studies of rodent reservoirs: Their relevance for human health. Emerging Infectious Diseases 4:529–537 Mills JN, Ellis BA, Ksiazek TG, McKee KT, Maiztegui JI, Childs JE, Peters CJ, Mills JN, Nelson GO, Calderon GE (1992) A longitudinal study of Junin virus activity in the rodent reservoir of Argentine Hemorrhagic Fever. American Journal of Tropical Medicine and Hygiene 47:749–763 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. https://doi.org/10.2307/1382129 Moncayo AC, Hice CL, Watts DM, Travassos De Rosa APA, Guzmán H, Russell KL, Calampa C, Gozalo A, Popov VL, Weaver SC, Tesh RB (2001) Allpahuayo virus: a newly recognized Arenavirus (Arenaviridae) from arboreal rice rats (Oecomys bicolor and Oecomys paricola) in northeastern Peru. Virology 284:277–286 Murphy GEP, Romanuk TN (2014) A meta-analysis of declines in local species richness from human disturbances. Ecology and Evolution 4:91–103. https://doi.org/10.1002/ece3.909 PAHO (2021) Fiebres Hemorrágicas. Viral Diseases Available:https://www3.paho.org/hq/index.php?option=com_content&view=article&id=8304:2013-fiebre-hemorragica-boliviana&Itemid=39844&lang=en [accessed Aug 2, 2021] Pardiñas UFJ, Myers P, León-Paniagua L. Ordóñez, Garza N, Cook JA, Kryštufek B, Haslauer R, Bradley RD, Shenbrot GI, Patton JL (2017) Family Cricetidae (true hamsters, voles, lemmings and New World rats and mice). In: Wilson DE, Lacher TE, Mittermeier RA (eds) Handbook of the Mammals of the World Barcelona: Lynx Edicions, pp 204–279 Parodi AS, Greenway DJ, Rugiero HR, Frigerio M, De La Barrera JM, Mettler N, Garzon F, Boxaca M, Guerrero L, Nota N (1958) Concerning the epidemic outbreak in Junín. Dia Médico 30:2300–2301 Pinheiro FP, Wooddall JP, Travasos da Rosa APA, Travasos da Rosa JF (1977) Studies in arenaviruses in Brazil. Medicina 37:175–181 Polop F, Provensal C, Scavuzzo M, Lamfri M, Calderón G, Polop J (2008) On the relationship between the environmental history and the epidemiological situation of Argentine Hemorrhagic Fever. Ecological Research 23:217–225. https://doi.org/10.1007/s11284-007-0371-2 Polop J, Calderón G, Feuillade MR, García J, Enria D, Sabattini M (2007) Spatial variation in abundance of the Junin virus hosts in endemic and nonendemic Argentine Haemorrhagic Fever zones. Austral Ecology 32:245–253. https://doi.org/10.1111/j.1442-9993.2007.01679.x Prist PR, Prado A, Tambosi LR et al (2021) Moving to healthier landscapes: Forest restoration decreases the abundance of Hantavirus reservoir rodents in tropical forests. Science of the Total Environment 752:141967. https://doi.org/10.1016/j.scitotenv.2020.141967 Prist PR, Uriarte M, Tambosi RL, Prado A, Pardini R, D’Andrea PS, 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 QGIS Development Team (2020) QGIS Geographic Information System. Open Source Geospatial Foundation Project Queen K, Shi M, Anderson LJ, Tong S (2015) Other bat-borne viruses. In: Wang L, Cowled C (eds) Bats and viruses: a new frontier of emerging infectious diseases New Jersey: John Wiley and Sons, pp 217–247 Radoshitzky SR, Bào Y, Buchmeier MJ, Charrel RN, Clawson AN, Clegg CS, DeRisi JL, Emonet S, Gonzalez JP, Kuhn JH, Lukashevich IS, Peters CJ, Romanowski V, Salvato MS, Stenglein MD, de la Torre JC (2015) Past, present, and future of Arenavirus taxonomy. Archives of Virology 160:1851–1874 Radoshitzky SR, Buchmeier MJ, Charrel RN, Clegg CS, González JP, Gunther S, Hepooki J, Kuhn JH, Lukash IS, Romanowski V, Salvato MS, Sironi M, Stenglein MD, de la Torre J C., ICTV RC (2019) ICTV Virus Taxonomy Profile: Arenaviridae. In: Journal of General Virology. Available: https://talk.ictvonline.org/ictv-reports/ictv_online_report/negative-sense-rna-viruses/bunyavirales/w/arenaviridae#Citation [accessed Jun 23 2020] Riera L, Castillo E, Saavedra MC, Priotto J, Sottosanti J, Polop J, Ambrosio AM (2005) Serological study of the Lymphochoriomeningitis virus (LCMV) in an Inner City of Argentina. Journal of Medical Virology 76:285–289 Rubio AV, Ávila-Flores R, Suzán G (2014) Responses of small mammals to habitat fragmentation: Epidemiological considerations for rodent-borne Hantaviruses in the Americas. Ecohealth 11:526–533. https://doi.org/10.1007/s10393-014-0944-9 Sabattini MS, González de Rios LE, Díaz G, Vega VR (1977) Infección natural y experimental de roedores con virus Junin. Medicina (buenos Aires) 37:149–161 Salas R, de Manzione N, Tesh RB, Rico-Hesse R, Shope RE, Betancourt A, Godoy O, Bruzual R, Pacheco ME, Ramos B, Taibo ME, Tamayo JG, Jaimes E, Vasquez C, Araoz F, Querales J (1991) Venezuelan Haemorrhagic Fever. Lancet 338:1033–1036 Sarute N, Ross SR (2017) New World Arenavirus Biology. Annual Review of Virology 4:141–158. https://doi.org/10.1146/annurev-virology-101416-042001 Sayler KA, Barbet AF, Chamberlain C, Clapp WL, Alleman R, Loeb JC, Lednicky JA, Kuhn JH (2014) Isolation of Tacaribe virus, a Caribbean Arenavirus, from host-seeking Amblyomma americanum ticks in Florida. PLoS One 9:1–16. https://doi.org/10.1371/journal.pone.0115769 Shi M, Lin XD, Chen X, Tian JH, Chen LJ, Li K, Wang W, Eden JS, Shen JJ, Liu L, Holmes EC, Zhang YZ (2018) The evolutionary history of vertebrate RNA viruses. Nature 556:197–202. https://doi.org/10.1038/s41586-018-0012-7 Shipley R, Wright E, Selden D, Wu G, Aegerter J, Fooks AR, Banyard AC (2019) Bats and viruses: Emergence of novel Lyssaviruses and association of bats with viral zoonoses in the EU. Tropical Medicine and Infectious Disease 4:1–22. https://doi.org/10.3390/tropicalmed4010031 Suzán G, Marcé E, Giermakowski JT, Armién B, Pascale J, Mills J, Ceballos G, Gómez A, Aguirre AA, Salazar-Bravo J, Armién A, Parmenter R, Yates T (2008) The effect of habitat fragmentation and species diversity loss on Hantavirus prevalence in Panama. Annals of the New York Academy of Sciences 1149:80–83. https://doi.org/10.1196/annals.1428.063 Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease emergence. Philosophical Transactions of the Royal Society B Biological Sciences 356:983–989 Ter Meulen J, Lukashevich I, Sidibe K, Inapogui A, Marx M, Dorlemann A, Yansane ML, Koulemou K, Chang-Claude J, Schmitz H (1996) Hunting of peridomestic rodents and consumption of their meat as possible risk factors for rodent-to-human transmission of Lassa virus in the Republic of Guinea. American Journal of Tropical Medicine and Hygiene 55:661–666. https://doi.org/10.4269/ajtmh.1996.55.661 Tian H, Stenseth NC (2019) The ecological dynamics of Hantavirus diseases: from environmental variability to disease prevention largely based on data from China. PLoS Neglected Tropical Diseases 13:1–19. https://doi.org/10.1371/journal.pntd.0006901 Trapido H, Sanmartin C (1971) Pichindé virus, a new virus of the Tacaribe group from Colombia. American Journal of Tropical Medicine and Hygiene 20:631–641 Utrera A, Duno G (2007) Preferencias de hábitat de Sigmodon alstoni y Zygodontomys brevicauda (Rodentia, Cricetidae) en agroecosistemas de los Llanos de Venezuela. Interciencia 32:471–476 Vitullo AD, Merani MS (1988) Is vertical transmission sufficient to maintain Junin virus in nature? Journal of General Virology 69(Pt6):1437–1440. https://doi.org/10.1099/0022-1317-69-6-1437 Webb PA, Johnson KM, Hibbs JB, Kuns ML (1970) Parana, a new Tacaribe complex virus from Paraguay. Arch Gesamte Virusforsch 32:379–388 Webb PA, Johnson KM, Peters CJ, Justines G (1973) Behavior of Machupo and Latino viruses in Calomys callosus from two geographic areas of Bolivia. In: Lehmann-Grube F (ed) Lymphocytic Choriomeningitis virus and other Arenaviruses Berlin: Springer, pp 313–322. https://doi.org/10.1007/978-3-642-65681-1_27 Yates TL, Mills JN, Parmenter CA, Ksiazek TG, Parmenter RR, Vande Castle JR, Calisher CH, Nichol ST, Abbott KD, Young JC, Morrison ML, Beaty BJ, Dunnum JL, Baker RJ, Salazar-Bravo J, Peters CJ (2002) The ecology and evolutionary history of an emergent disease: hantavirus pulmonary syndrome. Bioscience. 52:989–998. https://doi.org/10.1641/0006-3568(2002)052[0989:teaeho]2.0.co;2 Zapata JC, Salvato MS (2013) Arenavirus variations due to host-specific adaptation. Viruses 5:241–278. https://doi.org/10.3390/v5010241