• View in gallery
    Figure 1.

    General Carneiro municipality, State of Paraná, southern Brazil.

  • View in gallery
    Figure 2.

    Climatic diagram of the study area obtained from December 2009 to December 2011. Rainfall (mm) = dark bars; Average temperature (°C) = Dark line.

  • View in gallery
    Figure 3.

    Population sizes, proportion of reproducing females, and prevalence of hantavirus infection for: (A) Akodon serrensis, (B) Akodon montensis, (C) Akodon paranaensis, (D) Oligoryzomys nigripes, (E) Oxymycterus judex, and (F) Thaptomys nigrita, in General Carneiro, between December 2009 and December 2011. (Dark bars = proportion of reproducing females; Dotted line = hantavirus prevalence; Continuous line = population size).

  • View in gallery
    Figure 4.

    Age structure of (A) Akodon serrensis, (B) Akodon montensis, (C) Akodon paranaensis, (D) Oligoryzomys nigripes, (E) Oxymycterus judex, and (F) Thaptomys nigrita, in General Carneiro, between December 2009 and December 2011 (Black bar = class I; Dark Gray bar = class II; Light Gray bar = class III).

  • 1.

    Lednicky JA, 2003. Hantaviruses: a short review. Arch Pathol Lab Med 127: 3035.

  • 2.

    Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412441.

    • Search Google Scholar
    • Export Citation
  • 3.

    Brazilian Ministry of Health, 2013. Report on Hantavirus Pulmonary Syndrome until May, 2013. Available at: http://portalsaude.saude.gov.br/portalsaude/arquivos/pdf/2013/Jun/21/ANEXOHANTA(2).pdf. Accessed July 8, 2013.

    • Search Google Scholar
    • Export Citation
  • 4.

    Raboni SM, Probst CM, Bordignon J, Zeferino A, Duarte dos Santos CN, 2005. Hantaviruses in Central South America: phylogenetic analysis of the S segment from HPS cases in Paraná, Brazil. J Med Virol 76: 553562.

    • Search Google Scholar
    • Export Citation
  • 5.

    Raboni SM, Hoffmann FG, Oliveira RC, Teixeira BR, Bonvicino CR, Stella V, Carstensen S, Bordignon J, D'Andrea PS, Lemos ER, Duarte dos Santos CN, 2009. Phylogenetic characterization of hantaviruses from wild rodents and hantavirus pulmonary syndrome cases in the State of Parana (Southern Brazil). J Gen Virol 90: 21662171.

    • Search Google Scholar
    • Export Citation
  • 6.

    Raboni SM, Delfraro A, de Borba L, Teixeira BR, Stella V, Araujo MR, Carstensen S, Rubio G, Maron A, Lemos ER, D'Andrea PS, Duarte dos Santos CN, 2012. Hantavirus infection prevalence in wild rodents and human anti-hantavirus serological profiles from different geographic areas of South Brazil. Am J Trop Med Hyg 87: 371378.

    • Search Google Scholar
    • Export Citation
  • 7.

    Suzuki A, Bisordi I, Levis S, Garcia J, Pereira LE, Souza RP, Sugahara TK, Pini N, Enria D, Souza LT, 2004. Identifying rodent hantavirus reservoirs, Brazil. Emerg Infect Dis 10: 21272134.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oliveira RC, Teixeira BR, Mello FC, Pereira AP, Duarte AS, Bonaldo MC, Bonvicino CR, D'Andrea PS, Lemos ER, 2009. Genetic characterization of a Juquitiba-like viral lineage in Oligoryzomys nigripes in Rio de Janeiro, Brazil. Acta Trop 112: 212218.

    • Search Google Scholar
    • Export Citation
  • 9.

    Oliveira RC, Padula PJ, Gomes R, Martinez VP, Bellomo C, Bonvicino CR, Freire e Lima DI, Bragagnolo C, Caldas AC, D'Andrea PS, Lemos ER, 2011. Genetic characterization of hantaviruses associated with sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in Southern Brazil. Vector Borne Zoonotic Dis 11: 301314.

    • Search Google Scholar
    • Export Citation
  • 10.

    Pereira LE, Suzuki A, Bisord I, Souza RP, Souza LT, Oshiro FM, Cerroni MP, Neto RS, Pinho JR, 2007. Estudo longitudinal da prevalência dos Vírus Juquitiba e Araraquara em roedores das regiões da Mata Atlântica e do Cerrado do Brasil. Bol Epidemiol Paul 4: 213.

    • Search Google Scholar
    • Export Citation
  • 11.

    Figueiredo GG, Borges AA, Campos GM, Machado AM, Saggioro FP, Sabino GS Jr, Badra SJ, Ortiz AA, Figueiredo LT, 2010. Diagnosis of hantavirus infection in humans and rodents in Ribeirão Preto, State of São Paulo, Brazil. Rev Soc Bras Med Trop 43: 348354.

    • Search Google Scholar
    • Export Citation
  • 12.

    Limongi JE, Moreira FG, Peres JB, Suzuki A, Ferreira IB, Souza RP, Pinto RM, Pereira LE, 2013. Serological survey of hantavirus in rodents in Uberlândia, Minas Gerais, Brazil. Rev Inst Med Trop Sao Paulo 55: 155158.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rosa ES, Medeiros DB, Nunes MR, Simith DB, Pereira AD, Elkhoury MR, Santos ED, Lavocat M, Marques AA, Via AV, Kohl VA, Terças AC, D'Andrea PS, Bonvicino CR, 2012. Molecular epidemiology of Laguna Negra virus, Mato Grosso State, Brazil. Emerg Infect Dis 18: 982985.

    • Search Google Scholar
    • Export Citation
  • 14.

    Raboni SM, de Borba L, Hoffmann FG, Noronha L, Azevedo ML, Carstensen S, Mazzarotto GA, Bordignon J, Duarte dos Santos CN, 2009. Evidence of circulation of Laguna Negra-like hantavirus in the Central West of Brazil: case report. J Clin Virol 45: 153156.

    • Search Google Scholar
    • Export Citation
  • 15.

    Johnson AM, Souza LT, Ferreira IB, Pereira LE, Ksiazek TG, Rollin PE, Peters CJ, Nichol ST, 1999. Genetic investigation of novel hantaviruses causing fatal HPS in Brazil. J Med Virol 59: 527535.

    • Search Google Scholar
    • Export Citation
  • 16.

    Rosa ES, Medeiros DB, Nunes MR, Simith DB, Pereira AS, Elkhoury MR, Lavocat M, Marques AA, Via AV, D'Andrea PS, Bonvicino CR, Lemos ER, Vasconcelos PF, 2011. Pygmy rice rat as potential host of Castelo dos Sonhos Hantavirus. Emerg Infect Dis 17: 15271530.

    • Search Google Scholar
    • Export Citation
  • 17.

    Agrellos R, Bonvicino CR, Rosa ES, Marques AA, D'Andrea PS, Weksler M, 2012. The taxonomic status of the Castelo dos Sonhos Hantavirus reservoir. Zootaxa 3220: 128.

    • Search Google Scholar
    • Export Citation
  • 18.

    Rosa ES, Mills JN, Padula PJ, Elkhoury MR, Ksiazek TG, Mendes WS, Santos ED, Araújo GC, Martinez VP, Rosa JF, Edelstein A, Vasconcelos PF, 2005. Newly recognized hantaviruses associated with hantavirus pulmonary syndrome in northern Brazil: partial genetic characterization of viruses and serologic implication of likely reservoirs. Vector Borne Zoonotic Dis 5: 1119.

    • Search Google Scholar
    • Export Citation
  • 19.

    Leduc JW, Smith GA, Pinheiro FP, Vasconcelos PF, Rosa ES, Maiztegui JI, 1985. Isolation of a Hantaan-related virus from Brazilian rats and serologic evidence of its widespread distribution in South America. Am J Trop Med Hyg 34: 810815.

    • Search Google Scholar
    • Export Citation
  • 20.

    Xiao S, Chu Y, Knauert FK, Lofts R, Dalrymple JM, Leduc JW, 1992. Comparison of hantavirus isolates using a genus-reactive primer pair polymerase chain reaction. J Gen Virol 73: 567573.

    • Search Google Scholar
    • Export Citation
  • 21.

    Firth C, Tokarz R, Simith DB, Nunes MR, Bhat M, Rosa ES, Medeiros DB, Palacios G, Vasconcelos PF, Lipkin WI, 2012. Diversity and distribution of hantaviruses in South America. J Virol 86: 1375613766.

    • Search Google Scholar
    • Export Citation
  • 22.

    Chan YC, Wong TW, Yap EH, 1987. Hemorrhagic fever with renal syndrome: clinical, virological and epidemiological perspectives. Ann Acad Med Singapore 16: 696701.

    • Search Google Scholar
    • Export Citation
  • 23.

    Casapia M, Mamani E, Garcia MP, Miraval ML, Valencia P, Quino AH, Álvarez C, Donaires LF, 2012. Síndrome pulmonar por hantavirus (Virus Río Mamoré) en la Amazonía Peruana. Rev Peru Med Exp Salud Publica 29: 390395.

    • Search Google Scholar
    • Export Citation
  • 24.

    Chu YK, Goodin D, Owen RD, Koch D, Jonsson CB, 2009. Sympatry of 2 hantavirus strains, Paraguay, 2003–2007. Emerg Infect Dis 15: 20072010.

  • 25.

    Padula P, Martinez VP, Bellomo C, Maidana S, Juan JS, Tagliaferri P, Bargardi S, Vazquez C, Colucci N, Estévez J, Almirón M, 2007. Pathogenic hantaviruses, northeastern Argentina and eastern Paraguay. Emerg Infect Dis 13: 12111214.

    • Search Google Scholar
    • Export Citation
  • 26.

    Delfraro A, Tomé L, D’Elía G, Clara M, Achával F, Russi JC, Rodonz JR, 2008. Juquitiba-like hantavirus from 2 nonrelated rodent species, Uruguay. Emerg Infect Dis 14: 14471451.

    • Search Google Scholar
    • Export Citation
  • 27.

    Johnson AM, Bowen MD, Ksiazek TG, Williams RJ, Bryan RT, Mills JN, Peters CJ, Nichol ST, 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115127.

    • Search Google Scholar
    • Export Citation
  • 28.

    Carroll DS, Mills JN, Montgomery JM, Bausch DG, Blair PJ, Burans JP, Felices V, Gianella A, Iihoshi N, Nichol ST, Olson JG, Rogers DS, Salazar M, Ksiazek TG, 2005. Hantavirus pulmonary syndrome in Central Bolivia: relationships between reservoir hosts, habitats, and viral genotypes. Am J Trop Med Hyg 72: 4246.

    • Search Google Scholar
    • Export Citation
  • 29.

    Levis S, Garcia J, Pini N, Calderón G, Ramírez J, Bravo D, St Jeor S, Ripoll C, Bego M, Lozano E, Barquez R, Ksiazek TG, Enria D, 2004. Hantavirus pulmonary syndrome in northwestern Argentina: circulation of Laguna Negra virus associated with Calomys callosus. Am J Trop Med Hyg 71: 658663.

    • Search Google Scholar
    • Export Citation
  • 30.

    Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, De Velasquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG, 1997. An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57: 274282.

    • Search Google Scholar
    • Export Citation
  • 31.

    Hjelle BL, Torrez-Martinez N, Koster FT, 1996. Hantavirus pulmonary syndrome-related virus from Bolivia. Lancet 347: 57.

  • 32.

    Bharadwaj M, Boten J, Torrez-Martinez N, Hjelle BL, 1997. Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the Pygmy Rice rat, Oligoryzomys microtis, from Bolivia. Am J Trop Med Hyg 57: 368374.

    • Search Google Scholar
    • Export Citation
  • 33.

    Richter MH, Hanson JD, Cajimat MN, Milazzo ML, Fulhorst CF, 2010. Geographical range of Rio Mamoré virus (family Bunyaviridae, genus Hantavirus) in association with the small-eared pygmy rice rat (Oligoryzomys microtis). Vector Borne Zoonotic Dis 10: 613.

    • Search Google Scholar
    • Export Citation
  • 34.

    Hjelle B, Torres-Pérez F, 2010. Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2: 25592586.

  • 35.

    Chu Y-K, Owen RD, Jonsson CB, 2011. Phylogenetic exploration of hantaviruses in Paraguay reveals reassortment and host switching in South America. Virol J 8: 399.

    • Search Google Scholar
    • Export Citation
  • 36.

    Figueiredo LT, Moreli ML, de Sousa RL, Borges AA, Figueiredo GG, Machado AM, Bisordi I, Nagasse-Sugahara TK, Suzuki A, Pereira LE, Souza RP, Souza LT, Braconi CT, Harsi CM, Zanotto PM, 2009. Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg Infect Dis 15: 561567.

    • Search Google Scholar
    • Export Citation
  • 37.

    Araujo J, Pereira A, Nardi MS, Henriques DA, Lautenschalager DA, Dutra LM, Ometto TL, Hurtado RF, Maués F, Nava A, Morais FA, Aires CC, Favorito S, Durigon EL, 2011. Detection of hantaviruses in Brazilian rodents by SYBR-Green-based real-time RT-PCR. Arch Virol 156: 12691274.

    • Search Google Scholar
    • Export Citation
  • 38.

    Araujo J, Thomazelli LM, Henriques DA, Lautenschalager D, Ometto T, Dutra LM, Aires CC, Favorito S, Durigon EL, 2012. Detection of hantavirus in bats from remaining rain forest in São Paulo, Brazil. BMC Res Notes 5: 690.

    • Search Google Scholar
    • Export Citation
  • 39.

    Oliveira RC, Guterres A, Schrago CG, Fernandes J, Teixeira BR, Zeccer S, Bonvicino CR, D'Andrea PS, Lemos ER, 2012. Detection of the first incidence of Akodon paranaensis naturally infected with the Jabora Virus strain (Hantavirus) in Brazil. Mem Inst Oswaldo Cruz 107: 424428.

    • Search Google Scholar
    • Export Citation
  • 40.

    Cerqueira R, Gentile R, Fernandez FA, D'Andrea PS, 1993. A five-year population study of an assemblage of small mammals in southeastern Brazil. Mammalia 57: 507517.

    • Search Google Scholar
    • Export Citation
  • 41.

    D'Andrea PS, Gentile R, Cerqueira R, Grelle CE, Horta C, Rey L, 1999. Ecology of small mammals in a Brazilian rural area. Rev Bras Zool 16: 611620.

  • 42.

    D'Andrea PS, Gentile R, Maroja LS, Fernandes FA, Coura R, Cerqueira R, 2007. Small mammal populations of an agroecosystem in the Atlantic Forest domain, southeastern Brazil. Braz J Biol 67: 179186.

    • Search Google Scholar
    • Export Citation
  • 43.

    Gentile R, D'Andrea PS, Cerqueira R, Maroja LS, 2000. Population dynamics and reproduction of marsupials and rodents in a Brazilian rural area: a five-year study. Stud Neotrop Fauna Environ 9: 19.

    • Search Google Scholar
    • Export Citation
  • 44.

    Feliciano BR, Fernandez FA, Freitas D, Figueiredo MS, 2002. Population dynamics of small rodents in a grassland between fragments of Atlantic Forest in southeastern Brazil. Mamm Biol 67: 304314.

    • Search Google Scholar
    • Export Citation
  • 45.

    Cademartori CV, Fabián ME, Menegheti JO, 2004. Variações na abundância de roedores (Rodentia, Sigmodontinae) em duas áreas de Floresta Ombrófila Mista, Rio Grande do Sul, Brasil. Rev Bras Zoociências 6: 147167.

    • Search Google Scholar
    • Export Citation
  • 46.

    Cademartori CV, Fabián ME, Menegheti JO, 2005. Biologia reprodutiva de Delomys dorsalis (Hensel, 1872) - Rodentia, Sigmodontinae - em área de floresta ombrófila mista, Rio Grande do Sul, Brasil. Mastozool Neotrop 12: 133144.

    • Search Google Scholar
    • Export Citation
  • 47.

    Bonecker ST, Portugal LG, Costa-Neto SF, Gentile R, 2009. A long term study of small mammal populations in a Brazilian agricultural landscape. Mamm Biol 74: 467477.

    • Search Google Scholar
    • Export Citation
  • 48.

    Antunes PC, Campos MA, Oliveira-Santos LG, Graipel ME, 2010. Population dynamics of Akodon montensis (Rodentia, Cricetidae) in the Atlantic forest of Southern Brazil, 2010. Mamm Biol 75: 186190.

    • Search Google Scholar
    • Export Citation
  • 49.

    Galiano D, Kubiak BB, Marinho JR, Freitas TR, 2013. Population dynamics of Akodon montensis and Oligoryzomys nigripes in an Araucaria forest of Southern Brazil. Mammalia 77: 173179.

    • Search Google Scholar
    • Export Citation
  • 50.

    Bonvicino CR, Oliveira JA, D'Andrea PS, 2008. Guia dos roedores do Brasil, com chaves para gêneros baseadas em caracteres externos. Rio de Janeiro: Centro Pan-Americano de Febre Aftosa - OPAS/OMS.

    • Search Google Scholar
    • Export Citation
  • 51.

    Oliveira JA, Bonvicino CR, 2011. Ordem Rodentia. Reis NR, Peracchi AL, Pedro WA, Lima IP, eds. Mamíferos do Brasil. Second edition. Londrina, PR: Universidade Estadual de Londrina, 358414.

    • Search Google Scholar
    • Export Citation
  • 52.

    Boone JD, Otteson EW, McGwire KC, Villard P, Rowe JE, St Jeor SC, 1998. Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. Am J Trop Med Hyg 59: 445451.

    • Search Google Scholar
    • Export Citation
  • 53.

    Mills JN, Ksiazek TG, Peters CJ, Childs JE, 1999. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg Infect Dis 5: 135142.

    • Search Google Scholar
    • Export Citation
  • 54.

    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 Zoonotic Dis 7: 229240.

    • Search Google Scholar
    • Export Citation
  • 55.

    Suárez OV, Cueto GR, Cavia R, Villafañe IE, Bilenca DN, Edelstein A, Martínez P, Miguel S, Bellomo C, Hodara K, Padula PJ, Busch M, 2003. Prevalence of infection with hantavirus in rodent populations of central Argentina. Mem Inst Oswaldo Cruz 98: 727732.

    • Search Google Scholar
    • Export Citation
  • 56.

    Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN, 2001. Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65: 768776.

    • Search Google Scholar
    • Export Citation
  • 57.

    Owen RD, Goodin DG, Koch DE, Chu Y-K, Jonsson CB, 2010. Spatiotemporal variation in Akodon montensis (Cricetidae: Sigmodontinae) and hantaviral seroprevalence in a subtropical forest ecosystem. J Mammal 91: 467481.

    • Search Google Scholar
    • Export Citation
  • 58.

    Piudo L, Monteverde MJ, Walker RS, Douglass RJ, 2011. Rodent community structure and Andes virus infection in sylvan and peridomestic habitats in northwestern Patagonia, Argentina. Vector Borne Zoonotic Dis 11: 315324.

    • Search Google Scholar
    • Export Citation
  • 59.

    Vadell MV, Bellomo C, San Martín A, Padula P, Villafañe IG, 2011. Hantavirus ecology in rodent populations in three protected areas of Argentina. Trop Med Int Health 16: 13421352.

    • Search Google Scholar
    • Export Citation
  • 60.

    Palma RE, Polop JJ, Owen RD, Mills JN, 2012. Ecology of rodent-associated hantaviruses in the Southern Cone of South America: Argentina, Chile, Paraguay, and Uruguay. J Wildl Dis 48: 267281.

    • Search Google Scholar
    • Export Citation
  • 61.

    Balbinot R, Valério ÁF, Sanquetta CR, Caldeira MV, Silvestre R, 2008. Estoque de carbono em plantações de Pinus spp. em diferentes idades no Sul do Estado do Paraná. Floresta 38: 317324.

    • Search Google Scholar
    • Export Citation
  • 62.

    Mills JN, Childs JE, Ksiazek TG, Peters CJ, 1995. Methods for Trapping and Sampling Small Mammals for Virologic Testing. Atlanta, GA: Center for Disease Control and Prevention.

    • Search Google Scholar
    • Export Citation
  • 63.

    Bonvicino C, Oliveira JA, Gentile R, 2010. A new species of Calomys (Rodentia: Sigmodontinae) from Eastern Brazil. Zootaxa 2336: 1925.

  • 64.

    Bonvicino CR, 2011. Diversidade cariotípica em roedores Akodontini do Brasil. Bol Soc Bras Mastozoologia 62: 711.

  • 65.

    Figueiredo LT, Moreli ML, Borges AA, Figueiredo GG, Badra SJ, Bisordi I, Suzuki A, Capria S, Padula P, 2009. Evaluation of an enzyme-linked immunosorbent assay based on Araraquara virus recombinant nucleocapsid protein. Am J Trop Med Hyg 81: 273276.

    • Search Google Scholar
    • Export Citation
  • 66.

    Mazzarotto GA, Raboni SM, Stella V, Carstensen S, Noronha L, Levis S, Zanluca C, Zanetti CR, Bordignon J, Santos CN, 2009. Production and characterization of monoclonal antibodies against the recombinant nucleoprotein of Araucaria hantavirus. J Virol Methods 162: 96100.

    • Search Google Scholar
    • Export Citation
  • 67.

    Guterres A, Oliveira RC, Fernandes J, D'Andrea PS, Bonvicino CR, Bragagnolo C, Guimarães GD, Almada GL, Machado RR, Lavocat M, Elkhoury MD, Schrago CG, Lemos ER, 2013. Phylogenetic analysis of the S segment from Juquitiba hantavirus: Identification of two distinct lineages in Oligoryzomys nigripes. Infect Genet Evol 18: 262268.

    • Search Google Scholar
    • Export Citation
  • 68.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403410.

  • 69.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 27312739.

    • Search Google Scholar
    • Export Citation
  • 70.

    Glass GE, Childs JE, Korch GW, Leduc JW, 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101: 459472.

    • Search Google Scholar
    • Export Citation
  • 71.

    Paise G, Vieira EM, 2005. Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma Floresta Ombrófila Mista no Rio Grande do Sul, Brasil. Rev Bras Bot 28: 615625.

    • Search Google Scholar
    • Export Citation
  • 72.

    Iob G, Vieira EM, 2008. Seed predation of Araucaria angustifolia (Araucariaceae) in the Brazilian Araucaria Forest: influence of deposition site and comparative role of small and “large” mammals. Plant Ecol 198: 185196.

    • Search Google Scholar
    • Export Citation
  • 73.

    Vieira EM, Ribeiro JF, Iob G, 2011. Seed predation of Araucaria angustifolia (Araucariaceae) by small rodents in two areas with contrasting seed densities in the Brazilian Araucaria Forest. J Nat Hist 45: 843854.

    • Search Google Scholar
    • Export Citation
  • 74.

    Fonseca GA, Kierulff MC, 1989. Biology and natural history of Brazilian Atlantic forest small mammals. Bull Fla State Mus Biol Sci 34: 99152.

    • Search Google Scholar
    • Export Citation
  • 75.

    Graipel ME, Cherem JJ, Monteiro-Filho EL, Glock L, 2006. Dinâmica populacional de marsupiais e roedores no Parque Municipal da Lagoa do Peri, Ilha de Santa Catarina, sul do Brasil. Mastozoología Neotrop 13: 3149.

    • Search Google Scholar
    • Export Citation
  • 76.

    Hardestam J, Karlsson M, Falk KI, Olsson G, Klingström J, Lundkvist A, 2008. Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg Infect Dis 14: 12091215.

    • Search Google Scholar
    • Export Citation
  • 77.

    Calisher CH, Sweeney W, Mills JN, Beaty BJ, 1999. Natural history of Sin Nombre virus in western Colorado. Emerg Infect Dis 5: 126134.

  • 78.

    Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL, 2004. Wounding: the primary mode of Seoul virus transmission among male Norway Rats. Am J Trop Med Hyg 70: 310317.

    • Search Google Scholar
    • Export Citation
  • 79.

    Escutenaire S, Chalon P, De Jaegere F, Karelle-bui L, Mees G, Brochier B, Rozenfeld F, Pastoret P, 2002. Behavioral, physiologic, and habitat influences on the dynamics of Puumala Virus infection in Bank Voles (Clethrionomys glareolus). Emerg Infect Dis 8: 930936.

    • Search Google Scholar
    • Export Citation
  • 80.

    Vieira EM, Paise G, Machado PH, 2006. Feeding of small rodents on seeds and fruits: a comparative analysis of three species of rodents of the Araucaria Forest, southern Brazil. Acta Theriol (Warsz) 51: 311318.

    • Search Google Scholar
    • Export Citation
  • 81.

    Bohlman MC, Morzunov SP, Meissner J, Taylor MB, Ishibashi K, Rowe J, Levis S, Enria D, Jeor SC, 2002. Analysis of hantavirus genetic diversity in Argentina: S segment-derived phylogeny. J Virol 76: 37653773.

    • Search Google Scholar
    • Export Citation
  • 82.

    Salazar-Bravo J, Armién B, Suzán G, Armién A, Ruedas LA, Avila M, Zaldívar Y, Pascale JM, Gracia F, Yates TL, 2004. Serosurvey of wild rodents for hantaviruses in Panama, 2000–2002. J Wildl Dis 40: 103109.

    • Search Google Scholar
    • Export Citation
  • 83.

    Raboni SM, Rubio G, de Borba L, Zeferino A, Skraba I, Goldenberg S, Dos Santos CN, 2005. Clinical survey of hantavirus in southern Brazil and the development of specific molecular diagnosis tools. Am J Trop Med Hyg 72: 800804.

    • Search Google Scholar
    • Export Citation
  • 84.

    Monroe MC, Morzunov SP, Johnson AM, Bowen MD, Artsob H, Yates T, Peters CJ, Rollin PE, Ksiazek TG, Nichol ST, 1999. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg Infect Dis 5: 7586.

    • Search Google Scholar
    • Export Citation
  • 85.

    Santos ED, Coelho GE, Silva LR, Camargo NJ, Rúbio GG, Correa DS, Stremel N, Elkhoury MR, Oliveira RC, Martins EC, Ferreira IB, Pereira LE, Hatch DL, 2002. Fatores de risco para infecção por hantavirus entre trabalhadores florestais no Paraná, agosto a novembro de 2000. Boletim eletrônico epidemiológico - Ministério da Saúde, Brasil Ano 2: 89. Available at: http://portal.saude.gov.br/portal/arquivos/pdf/ano02_n01_fatores_risco_hantavirus_pr.pdf. Accessed July 8, 2013.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 423 151 34
PDF Downloads 152 55 8
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Population Ecology of Hantavirus Rodent Hosts in Southern Brazil

Bernardo R. TeixeiraLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Bernardo R. Teixeira in
Current site
Google Scholar
PubMed
Close
,
Nathalie LoureiroLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Nathalie Loureiro in
Current site
Google Scholar
PubMed
Close
,
Liana StrechtLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Liana Strecht in
Current site
Google Scholar
PubMed
Close
,
Rosana GentileLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Rosana Gentile in
Current site
Google Scholar
PubMed
Close
,
Renata C. OliveiraLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Renata C. Oliveira in
Current site
Google Scholar
PubMed
Close
,
Alexandro GuterresLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Alexandro Guterres in
Current site
Google Scholar
PubMed
Close
,
Jorlan FernandesLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Jorlan Fernandes in
Current site
Google Scholar
PubMed
Close
,
Luciana H. B. V. MattosLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Luciana H. B. V. Mattos in
Current site
Google Scholar
PubMed
Close
,
Sonia M. RaboniLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Sonia M. Raboni in
Current site
Google Scholar
PubMed
Close
,
Giselia RubioLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Giselia Rubio in
Current site
Google Scholar
PubMed
Close
,
Cibele R. BonvicinoLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Cibele R. Bonvicino in
Current site
Google Scholar
PubMed
Close
,
Claudia N. Duarte dos SantosLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Claudia N. Duarte dos Santos in
Current site
Google Scholar
PubMed
Close
,
Elba R. S. LemosLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Elba R. S. Lemos in
Current site
Google Scholar
PubMed
Close
, and
Paulo S. D'AndreaLaboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Programa de Pós-Graduação em Biologia Parasitária, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Laboratório de Hantaviroses e Rickettsioses, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil; Instituto Carlos Chagas, FIOCRUZ, Paraná, Brazil; Secretaria de Saúde do Estado do Paraná, Paraná, Brazil; Divisão de Genética, Instituto Nacional de Câncer, Rio de Janeiro, Brazil

Search for other papers by Paulo S. D'Andrea in
Current site
Google Scholar
PubMed
Close

In this study we analyze population dynamics of hantavirus rodent hosts and prevalence of infection over a 2-year period in Southern Brazil, a region with a high incidence of hantavirus pulmonary syndrome. The 14 small mammal species captured were composed of 10 rodents and four marsupials, the six most abundant species being Akodon serrensis, Oxymycterus judex, Akodon montensis, Akodon paranaensis, Oligoryzomys nigripes, and Thaptomys nigrita. These species displayed a similar pattern with increasing population sizes in fall/winter caused by recruitment and both, increase in reproductive activity and higher hantavirus prevalence in spring/summer. Specific associations between A. montensis/Jaborá Virus (JABV) and O. nigripes/Juquitiba-like Virus (JUQV-like) and spillover infections between A. paranaensis/JABV, A. serrensis/JABV, and A. paranaensis/JUQV-like were observed. Spillover infection in secondary hosts seems to play an important role in maintaining JABV and JUQV-like in the hantavirus sylvatic cycle mainly during periods of low prevalence in primary hosts.

Introduction

Hantavirus pulmonary syndrome (HPS) in Brazil is a zoonosis usually associated with rural activities in disturbed environments or in sylvatic interface areas.1,2 Since the first HPS case in 1993, more than 1,600 cases have been confirmed in Brazil, distributed among all regions, mainly in the southern states of Paraná, Santa Catarina, and Rio Grande do Sul.3 The State of Paraná is the fourth in HPS occurrence with two hantavirus genotypes described, Araucaria Virus (ARAUV) and Jaborá Virus (JABV).46 Because Araucaria Virus is recognized as a Juquitiba-like Virus (JUQV-like), we adopt this nomenclature herein to report this hantavirus genotype.

So far, five hantavirus genotypes associated with HPS cases have been described in rodent hosts and humans in many Brazilian regions: 1) Juquitiba Virus (JUQV) distributed in the Atlantic Forest in the South and Southeastern regions, the host being Oligoryzomys nigripes,4,7 with seroprevalence of 2.5–18.3%69; 2) Araraquara Virus (ARAV) with a wide distribution in the Cerrado Biome (Central plateau and Southeastern), transmitted by Necromys lasiurus,7 with seroprevalence of 1.2–11%7,1012; 3) Laguna Negra-like Virus (LNV) from a transition area of Cerrado and Amazon, restricted until now to Mato Grosso State in Northwestern Brazil, associated with Calomys callidus,13,14 with a seroprevalence of 17.4%13; 4) Castelo dos Sonhos Virus (CASV) from North and Northwestern Brazil in the Amazonian State of Pará, and in a transition area with Cerrado in the State of Mato Grosso, harbored by Oligoryzomys utiaritensis,1517 with seroprevalence of 4.5%16; and 5) Anajatuba Virus (ANAJV) from lowland areas of the Amazon Forest Biome in the northeastern state of Maranhão, transmitted by Oligoryzomys fornesi with seroprevalence of 41.7%.18 Another four genotypes were described only in rodents without any human infection reported: 1) Seoul Virus (SEOV) associated with the sinanthropic species Rattus norvegicus19,20 in the Amazonian State of Pará in Northern Brazil; 2) Rio Mearim Virus (RIMEV) from the lowlands of the Amazon Forest, sympatric to ANAJV in Northeastern Brazil, whose host is Holochilus sciureus, with seroprevalence of 29.4%18; 3) Rio Mamore Virus (RMV) from North Brazil in the Amazon Forest, whose host is Oligoryzomys microtis21; and 4) Jaborá Virus (JABV) distributed in the Atlantic Forest from the Southern region harbored by Akodon montensis with seroprevalence of 14.5%.9 However, SEOV and RMV have also been associated with human infection in other countries.22,23

Five of these nine genotypes are also present in rodent hosts from other South American regions: 1) JUQV in Paraguay,24 Argentina,25 and Uruguay26 with seroprevalence of 3.2–11.9% in O. nigripes25,26 and 6% in Oxymycterus sp.26; 2) LNV in Paraguay,24,27 Bolivia,28 and Argentina,29 with seroprevalence of 5.1–8.1% in C. callosus28,29 and 23% in C. laucha30; 3) RMV in Bolivia28,31,32 and Peru33 with seroprevalence of 7.7% in O. microtis28; 4) JABV in Paraguay24; and 5) SEOV distributed worldwide.

Despite the general rule of specificity between hantavirus genotypes and rodent host species, an increasing number of studies have reported hantavirus spillover into secondary hosts.34 However, little information about natural history of spillover infection on the host population dynamics is available. South American hantavirus genotypes do not correspond with the same level of co-evolution in studies with hantaviruses in Europe and Asia, thus affording great potential for host switching and adaptation.35 In Brazil, spillover has been witnessed in many hantavirus genotypes and host species, like ARAV harbored by secondary hosts, such as A. montensis, O. nigripes, Thaptomys nigrita, and Juliomys sp.,36,37 and species of marsupials and bats.38 Furthermore, JUQV-like and JABV have been reported in secondary hosts in Southern Brazil, JUQV-like associated with Akodon paranaensis,6 A. montensis, and Oxymycterus judex,5 and JABV with Akodon serrensis6 and A. paranaensis.39

Studies of small mammals have clarified many aspects on population ecology of Brazilian rodents, mainly in the Atlantic Forest.4049 Notwithstanding the great diversity of rodents in Brazil (about 240 species),50,51 consequently providing a high potential for many new hantavirus hosts, no studies have considered the infection dynamics. Population ecology studies are crucial for understanding the temporal patterns of infection in host populations and furnishing data on epidemiology, outbreak prediction, and risk of human infection.5260

In this study, we analyze population dynamics of hantaviruses in wild rodent hosts and prevalence of infection over a 2-year period from December 2009 to December 2011 in General Carneiro municipality, State of Paraná, Southern Brazil. This municipality has a high incidence of HPS, mainly affecting rural workers of pine tree management. This region also is inhabited by infected rodents with spillover infection of JUQV-like and JABV genotypes.5,6

Materials and Methods

Field data: study area and small mammal sampling.

The fieldwork was conducted in General Carneiro municipality, State of Paraná, Southern Brazil (Figure 1), located in a Mixed Ombrophilous Forest region. We studied different vegetation types, including native forests of Araucaria angustifolia (Bertol.) Kuntze 1898, native forest with anthropic disturbance, and exotic pine tree reforestation areas (Pinus elliotti and Pinus taeda) for timber trade.

Figure 1.
Figure 1.

General Carneiro municipality, State of Paraná, southern Brazil.

Citation: The American Society of Tropical Medicine and Hygiene 91, 2; 10.4269/ajtmh.13-0465

The climate is humid subtropical (Cfa), according to the Köppen climate classification, with mild summers and cold winters, and without dry seasons.61 The Technological Institute SIMEPAR provided monthly data of average temperature and accumulated rainfall from December 2009 to December 2011 obtained from Palmas Station, Paraná (Figure 2), the closest and most representative weather station in proximity to General Carneiro municipality.

Figure 2.
Figure 2.

Climatic diagram of the study area obtained from December 2009 to December 2011. Rainfall (mm) = dark bars; Average temperature (°C) = Dark line.

Citation: The American Society of Tropical Medicine and Hygiene 91, 2; 10.4269/ajtmh.13-0465

Rodent sampling was conducted every 3 months from December 2009 to December 2011, during five consecutive nights for each of the nine capture sessions. All capture sessions took place at the end of each season as follows: December in late spring, March in late summer, June in late fall, and September in late winter. The capture effort was constant in all capture sessions. We established 12 transects with 20 capture stations setting Tomahawk (Tomahawk Live Trap, Hazelhurst, WI) (40.64 × 12.70 × 12.70 cm) and Sherman traps (HB Sherman Traps, Tallahassee, FL) (7.62 × 9.53 × 30.48 cm), 300 traps in each capture night, baited with a mixture of bacon, peanut butter, banana, and oatmeal.

Specimens were captured, anesthetized, and euthanized according to recommended safety procedures62 and under the Guidelines for the Care and Use of Laboratory Animals, Oswaldo Cruz Foundation, Brazil (FIOCRUZ, License number L-049/08). Animals were captured with authorization of the Chico Mendes Institute for Biodiversity Conservation (ICMBIO Authorization 13373). Specimens were then measured, weighted, sexed, and identified by both karyotyping63,64 and cranial morphology/morphometry. Hantavirus antibody-positive specimens were confirmed by molecular analysis (amplification of the cytochrome b gene).

Hantavirus infection analysis.

Serum and tissue samples were obtained from all small mammals captured and submitted to immunoglobulin G (IgG) enzyme-linked immunosorbent assay (ELISA) for detection of hantavirus antibodies with the N-Araraquara hantavirus recombinant nucleocapsid protein (USP, Ribeirão Preto, Brazil).65 Samples of December 2009 and March 2010 captures were also tested with the Hantec Kit (FIOCRUZ-ICC, Curitiba, Brazil).66 Total RNA was extracted from lung, liver, or kidney tissue samples of hantavirus antibody-positive rodent species with the PureLink Micro-to-Midi total RNA Purification Kit (Invitrogen, San Diego, CA). The rodent samples were analyzed using the polymerase chain reaction with reverse transcription (750 base pair [bp]) and nested reactions (478 bp) of the S segment, with primers AG04-25F (5′ TAGTAGACTCCTTGAKAAGCT 3′), AG733-752R (5′ GAYTGGATGGAAAGGATWGA 3′), and AG274-291F (5′ CCCTGTTGGATCAACTGG 3′).39,67 For purification we adopted WizardSV Gel and the PCR Clean-Up System kit (Promega, Corp., Madison, WI) and for sequencing the BiqDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, Grand Island, NY). Virus sequences were analyzed with MEGA5 software, and hantavirus genotypes were identified with BLAST (http://blast.ncbi.nlm.nih.gov) through comparison with other hantavirus sequences.68,69

Data analysis and seasonal patterns.

Population size, reproductive status of females, and age structure were analyzed by species and year/season. Population size was estimated as the absolute number of captured specimens over a constant trapping effort. Lactating and pregnant females were considered as reproductively active. Females were classified as mated or unmated by uterus analysis, thus females with tumescence and marks of previous pregnancy were classified as non-virgins. Frequency of reproductively active females of the total number of mated females in each capture session was calculated to determine the reproductive season. Total sex ratio of each species was tested in the expected 1:1, with a χ2 analysis. Age structures were based on body weight (grams), dividing individuals into three classes with approximately the same number of animals.54

We recorded the presence of wounds and scars on the tail or ear as indicative of antagonistic encounters, the main form of hantavirus transmission among rodents.70 Prevalence of infection was calculated for each species, regarding sex, age class, number of specimens, and capture season. The χ2 test with Yates correction was adopted to test the association with these data.

Influence of monthly rainfall, average monthly temperature, and reproducing females in population sizes was analyzed by multiple linear regression considering backward criterion for a 1-, 2-, and 3-month time lag. Population sizes were also included in this analysis to verify the influence of these variables on prevalence.

Results

Population analysis and seasonal patterns.

The 14 small mammal species consisted of 10 rodents (Rodentia, Sigmodontinae: Akodon serrensis [N = 401]; Oxymycterus judex [N = 294]; Akodon montensis [N = 253]; Akodon paranaensis [N = 87]; Oligoryzomys nigripes [N = 73]; Thaptomys nigrita [N = 70]; Sooretamys angouya [N = 13]; Delomys dorsalis [N = 2]; Nectomys squamipes [N = 2]; and Brucepattersonius iheringi [N = 2]); and four marsupials (Didelphimorphia, Didelphidae: Monodelphis dimidiata [N = 34]; Philander frenatus [N = 9]; Gracilinanus sp. [N = 5]; and Lutreolina crassicaudata [N = 1]).

Population dynamics and prevalence were analyzed for A. serrensis, O. judex, A. montensis, A. paranaensis, O. nigripes, and T. nigrita, the six most abundant species. All species displayed similar seasonal patterns of population sizes, with higher values during the cooler months (from June to September) (Figure 3). This pattern was emphasized by A. serrensis, A. montensis, O. nigripes, T. nigrita, and A. paranaensis, this latter species still maintaining higher population values until December 2010. Oxymycterus judex presented a quite different pattern, with more homogeneous population sizes and less marked peaks (Figure 3).

Figure 3.
Figure 3.

Population sizes, proportion of reproducing females, and prevalence of hantavirus infection for: (A) Akodon serrensis, (B) Akodon montensis, (C) Akodon paranaensis, (D) Oligoryzomys nigripes, (E) Oxymycterus judex, and (F) Thaptomys nigrita, in General Carneiro, between December 2009 and December 2011. (Dark bars = proportion of reproducing females; Dotted line = hantavirus prevalence; Continuous line = population size).

Citation: The American Society of Tropical Medicine and Hygiene 91, 2; 10.4269/ajtmh.13-0465

All six species exhibited a reproductive pattern with higher reproductive frequency during the warmer months (from December to March) (Figure 3). Akodon serrensis and A. montensis also reproduced in June and September, although at lower rates. Oxymycterus judex presented a reproduction activity with similar rates throughout the year in accordance with population size dynamics data.

Age classes were based on weight. Akodon serrensis males (♂) and females (♀) were divided into class I (11–22 g), class II (23–26 g), and class III (27–40 g for ♂ and 27–45 g for ♀), A. montensis class I (7–25 g ♂ and 8–21 g ♀), class II (26–31 g ♂ and 22–28 g ♀), and class III (32–49 g ♂ and 29–44 g ♀), A. paranaensis class I (14–31 g ♂ and 17–25 g ♀), class II (32–41 g ♂ and 26–34 g ♀), and class III (44–61 g ♂ and 35–48 g ♀), O. judex class I (22–82 g ♂ and 34–69 g ♀), class II (83–110 g ♂ and 70–87 g ♀), and class III (111–160 g ♂ and 88–140 g ♀), O. nigripes class I (10–20 g ♂ and 9–15 g ♀), class II (21–25 g ♂ and 16–19 g ♀), and class III (26–37 g ♂ and 20–31 g ♀), and T. nigrita class I (11–17 g ♂ and 11–15 g ♀), class II (18–20 g ♂ and 16–20 g ♀), and class III (21–27 g ♂ and 21–24 g ♀).

A high frequency of young individuals (class I and II) was observed during the cooler months (from June to September). This pattern was conspicuous mainly in A. serrensis and A. montensis (Figure 4). Adults (class III) presented a more homogeneous distribution throughout the year as expected because of population aging. However, peaks of higher adult abundance were evident during the breeding season (December to March).

Figure 4.
Figure 4.

Age structure of (A) Akodon serrensis, (B) Akodon montensis, (C) Akodon paranaensis, (D) Oligoryzomys nigripes, (E) Oxymycterus judex, and (F) Thaptomys nigrita, in General Carneiro, between December 2009 and December 2011 (Black bar = class I; Dark Gray bar = class II; Light Gray bar = class III).

Citation: The American Society of Tropical Medicine and Hygiene 91, 2; 10.4269/ajtmh.13-0465

Five of the six most abundant species presented male sex bias: A. serrensis2 = 4.611, degrees of freedom [df] = 1, P = 0.0360), A. montensis2 = 4.271, df = 1, P = 0.0451), A. paranaensis2 = 4.545, df = 1, P = 0.0428), O. judex2 = 9.918, df = 1, P = 0.002), and T. nigrita2 = 4.629, df = 1, P = 0.0422).

We observed an inverse relationship between temperature and population sizes in A. serrensis, A. montensis, O. nigripes, and O. judex with a 1-month time lag (R2 = 0.552, β = −0.743, P = 0.022; R2 = 0.580, β = −0.762, P = 0.017; R2 = 0.748, β = −0.865, P = 0.003; R2 = 0.532, β = −0.729, P = 0.026, respectively), in A. paranaensis with a 1- and 2-month time lag (R2 = 0.630, β = −0.793, P = 0.011; R2 = 0.708, β = −0.841, P = 0.004, respectively), and in T. nigrita with a 2- and 3-month time lag (R2 = 0.829, β = −0.910, P = 0.001; R2 = 0.874, β = −0.768, P = 0.002, respectively). There was also an inverse relationship between rainfall and T. nigrita population size with a 3-month time lag (R2 = 0.874, β = −0.378, P = 0.045). There was no significant influence of reproductive activity on population sizes whatsoever.

Hantavirus infection.

We screened 26 hantavirus-infected rodents (ELISA and PCR confirmed) (Table 1), proving statistically biased to males (χ2 = 7.3; gL = 1; P = 0.0121). Two hantavirus genotypes were confirmed, establishing between a 95% and 99% identity with deposited sequences: i) JABV in A. montensis, A. serrensis, and A. paranaensis and ii) JUQV-like in O. nigripes and A. paranaensis. The other species, O. judex, T. nigrita, S. angouya, D. dorsalis, N. squamipes, and B. iheringi were not diagnosed seropositive.

Table 1

Species prevalence, sex, and hantavirus genotype of infected specimens (ELISA and PCR confirmed)*

Species No. of infected rodents/total of captured rodents Gender Hantavirus genotype
Akodon montensis 16/253 (5.91%) 16 M JABV
Akodon paranaensis 5/87 (5.68%) 2 M/2 F JABV
1 F JUQV-like
Akodon serrensis 2/401 (0.74%) 1 M/1 F JABV
Oligoryzomys nigripes 3/73 (4.17%) 3 M JUQV-like
TOTAL 26/814 (3.19%) 22 M JABV
4 F JUQV-like

PCR = polymerase chain reaction; M = males; F = females; JABV = Jaborá Virus; JUQV-like = Juquitiba-like Virus.

Infection by JABV was apparent throughout the year with peaks during the warmer months (December–March), especially in A. montensis, which rendered infected specimens in eight of the nine trap sessions. Only four animals presented JUQV-like infection (Table 1) in four different capture sessions; consequently, the prevalence of JUQV-like species corresponded always to only one infected animal in each capture session (Figure 3). Likewise, JUQV-like also had a similar pattern, with infection in warmer months (Figure 3E). Akodon paranaensis was the only species that harbored two hantavirus genotypes, JUQV-like (March 2010) and JABV (December 2010 and June 2011).

The majority of the infected animals belonged to class III (N = 23; χ2 = 32.462, degrees of freedom [df] = 2, P < 0.0001), two to class II (one A. montensis and one A. paranaensis), and only one to class I (one O. nigripes). The scar analysis revealed that 60% of all infected A. montensis had ear/tail scars, expressing a significant relationship between infection and scars (χ2 = 9.192; df = 1; P = 0.0063). No significant influence of temperature, precipitation, population size, and reproductive activity on prevalence of A. montensis (the only species with sufficient data for this analysis) was evident.

Discussion

The six most abundant species displayed similar patterns of population dynamics, with increasing population sizes in fall/winter (June to September) and increasing reproductive activity in spring/summer (December to March), although reproductive activity throughout the year was confirmed for A. serrensis, A. montensis, and O. judex. Climate analysis showed the influence of the low temperature periods on population sizes, with population increase in cooler months probably related to food availability, mainly seed production of the Brazilian Pine, A. angustifolia. Some authors reported the availability of mature seeds on the forest floor during fall and winter in other areas of Mixed Ombrophilous forest46 and also associated this high seed production to rodent population increases.45 Other studies have also reported A. angustifolia seeds as an important food source in the diet of these rodent species.7173 In fact, we found a great amount of A. angustifolia seeds on the forest floor of the studied areas during late fall, many with rodent gnaw marks.

During the spring/summer more individuals of age class III were apparent, which is in agreement with the reproductive results, because reproductive activity occurs mainly in this age class. Likewise, in the fall/winter, we observed a predominance of individuals of age class I, indicating that the population increase is a result of the younger individual recruitment. These population dynamics patterns agree with other studies on Sigmodontinae ecology in both Atlantic Forest landscape types, Mixed Ombrophilous Forest,45,48,49 and Dense Ombrophilous Forest.44,47,74,75

Hantavirus exhibited a seasonal pattern with higher prevalence in spring/summer, when population sizes were lower and both reproductive activity and numbers of adults were higher. This pattern was also witnessed for other hantavirus genotypes in North52,56 and South America.54,55,59

Hantavirus transmission among rodents is largely accepted as a consequence of bites and inoculation of the virus from the saliva, which contains higher levels of viral RNA than urine.76 This transmission occurs in antagonistic encounters and many authors have determined the presence of scars as indicative of this behavior.10,70,77,78 Aggressive encounters occur mainly in the breeding season79 and are more frequent in adult males.52,54,56,58,59 Our results corroborated these postulations, with a higher hantavirus prevalence found in spring/summer, seasons with higher reproductive activity, and a higher prevalence of infection in males of age class III (adults), with correlation between the presence of scars and hantavirus infection.

In addition to antagonistic encounters, inhalation of contaminated aerosols and ingestion of a contaminated shared food source might be important modes of transmission among hosts.76 Although A. paranaensis is not so dependent as O. nigripes on A. angustifolia seeds, this is an important alternative food source in cooler months, when others decrease. Both species also possessed a trophic niche overlap in the seasons without the A. angustifolia seeds (Perini AA, unpublished data). In addition to the common consumption of A. angustifolia seeds, other food sources such as fruits, seeds, and invertebrates are also shared by A. montensis and O. nigripes.80 Thus, the oral route by mutual food source intake may also be contributing to both intraspecific and spillover transmissions in the study area.

In addition to the already established host–parasite-specific interactions between A. montensis/JABV9 and O. nigripes/JUQV,7 we also observed spillover associations between A. paranaensis/JABV, A. serrensis/JABV, and A. paranaensis/JUQV-like. In previous studies in General Carneiro municipality, we first presented these two latter associations6 and spillover infections in A. montensis and O. judex, both infected by JUQV-like5; during this 2-year study, only one in five A. paranaensis was infected by JUQV-like. Furthermore, no spillover was observed in A. montensis and O. judex. Considering the low frequency, we cannot confirm the importance of spillover on JUQV-like maintenance in the wild. However, the occurrence of JUQV-like infection in three different genera of secondary hosts suggested the adaptation of this genotype to genetically distinct rodent species. This scenario could be a determinant to establish both hantavirus genetic diversity81 and the evolution of new hantavirus genotypes.2 Furthermore, in low prevalence times in the primary host, spillover infection can be very important in maintaining the virus in the wild until spillback infection,2 as was likely the case for JUQV-like spillover in A. paranaensis, which took place in a month without O. nigripes (primary host) infection.

We also attested to low relative abundance and disruptions in the population dynamics of O. nigripes, with the absence of animals on the December 2009 and December 2011 capture sessions, a pattern observed in other Atlantic Forest areas.47,75 This low abundance and instability on O. nigripes populations may be playing an important role to keep JUQV-like at low frequency.

Spillover infections of JABV seem to be restricted to the three Akodon species. We can speculate that JABV was harbored by the common ancestor of these species and remained associated with them, a fact also discussed for spillover infections between Calomys laucha and Calomys callosus, hosts of LNV in Paraguay.28 However, the geographic distribution of these Calomys species does not overlap, unlike A. montensis, A. serrensis, and A. paranaensis, which occurred in sympatry in our studied area, a pattern also reported for three Reithrodontomys species hosts of Rio Segundo Virus (RSV) in Panama.82 Thus, infection of A. serrensis and A. paranaensis by JABV may be related to overlap in habitat and food sharing.

Despite the low frequency of spillover infection in A. serrensis, there were JABV infections in all sampling months (regardless of host species) and a high prevalence of infection in the secondary host, A. paranaensis. Moreover, the spillover A. paranaensis/JABV was also reported in another area of the Mixed Ombrophilous Forest39 emphasizing the importance of this species in maintaining JABV. As in JUQV-like, JABV spillover infections seem to be important during periods of low viral prevalence in the primary host, because all spillover infections occurred in months of low A. montensis infection.

The JUQV-like is the genotype related to HPS cases in South and Southeastern Brazil.7,83,84 Until now, no studies have related JABV to HPS, even in endemic areas. The HPS cases in General Carneiro municipality appeared every year from 1999 to 2006, but no cases were reported from 2007 to 2011, probably as a result of epidemiological vigilance by the Health Division of the State of Paraná (SESA-PR). The main labor activity related to human infection in General Carneiro municipality was Pine Tree (Pinus elliotti and Pinus taeda) management.83,85 Pine tree workers usually occupied precarious, temporary structures near management areas, storing food, and thus, attracting wild rodents, mainly the habitat generalist species O. nigripes,85 thereby increasing probability of exposure to JUQV-like. From 2001, these precarious structures were modified to prevent wild rodent invasion. This resulted in a gradual decrease of HPS cases in the General Carneiro municipality (Health Division of State of Paraná, unpublished data).

Another explanation for the absence of HPS cases may be related to a possible change in hantavirus transmission patterns among rodents, because in the current study (2009–2011) we detected a higher prevalence of JABV (84.6% JABV and 15.4% JUQV-like), whereas in the previous study (2006), where HPS cases were reported, the prevalence of JUQV-like was higher (66.6%).5 Therefore, we point out that epidemiological vigilance and the low frequency of JUQV-like infection in rodents in the current study may be correlated to the absence of HPS cases in this period.

The results described here reinforce the importance of pluri-annual studies on hantavirus infection dynamics in rodent hosts. We observed a clear pattern of higher hantavirus prevalence in seasons with higher reproductive activity, greater numbers of adults, and lower population size. Increases in population occurred in cooler months with higher numbers of younger animals in accordance with resource availability.

Spillover infection reported in this study and in our previous study5 allows us to speculate that this host–virus association is common in this area. Therefore, we can infer that the spillover infection on secondary hosts plays an important role in maintaining JABV and JUQV-like in the hantavirus sylvatic cycle until the spillback infection for primary hosts.

ACKNOWLEDGMENTS

We thank the Health Secretary of the State of Paraná and the technicians Edson dos Santos, Edilsom Semczuk (Health Secretary of Foz do Iguaçu municipality), Ricardo Matsuo, Joel Lopes, Luiz Eduardo Pereira, Elizeu da Silva, Jorge Pinto (FIOCRUZ), and Jorge da Paixão (FIOCRUZ) for their assistance in the fieldwork expeditions. We are also grateful to Health Secretary of General Carneiro municipality and Pizzatto Industries for assisting in the rodent trapping logistics and Technological Institute SIMEPAR for climatic data. We also thank Fabiano Araújo Fernandes, Carolina Valença, and Fabiana Pellegrini Caramaschi for assistance in small mammal specific identification. English review and revision by Mitchell Raymond Lishon, native of Chicago, Illinois, USA-UCLA 1969.

  • 1.

    Lednicky JA, 2003. Hantaviruses: a short review. Arch Pathol Lab Med 127: 3035.

  • 2.

    Jonsson CB, Figueiredo LT, Vapalahti O, 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev 23: 412441.

    • Search Google Scholar
    • Export Citation
  • 3.

    Brazilian Ministry of Health, 2013. Report on Hantavirus Pulmonary Syndrome until May, 2013. Available at: http://portalsaude.saude.gov.br/portalsaude/arquivos/pdf/2013/Jun/21/ANEXOHANTA(2).pdf. Accessed July 8, 2013.

    • Search Google Scholar
    • Export Citation
  • 4.

    Raboni SM, Probst CM, Bordignon J, Zeferino A, Duarte dos Santos CN, 2005. Hantaviruses in Central South America: phylogenetic analysis of the S segment from HPS cases in Paraná, Brazil. J Med Virol 76: 553562.

    • Search Google Scholar
    • Export Citation
  • 5.

    Raboni SM, Hoffmann FG, Oliveira RC, Teixeira BR, Bonvicino CR, Stella V, Carstensen S, Bordignon J, D'Andrea PS, Lemos ER, Duarte dos Santos CN, 2009. Phylogenetic characterization of hantaviruses from wild rodents and hantavirus pulmonary syndrome cases in the State of Parana (Southern Brazil). J Gen Virol 90: 21662171.

    • Search Google Scholar
    • Export Citation
  • 6.

    Raboni SM, Delfraro A, de Borba L, Teixeira BR, Stella V, Araujo MR, Carstensen S, Rubio G, Maron A, Lemos ER, D'Andrea PS, Duarte dos Santos CN, 2012. Hantavirus infection prevalence in wild rodents and human anti-hantavirus serological profiles from different geographic areas of South Brazil. Am J Trop Med Hyg 87: 371378.

    • Search Google Scholar
    • Export Citation
  • 7.

    Suzuki A, Bisordi I, Levis S, Garcia J, Pereira LE, Souza RP, Sugahara TK, Pini N, Enria D, Souza LT, 2004. Identifying rodent hantavirus reservoirs, Brazil. Emerg Infect Dis 10: 21272134.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oliveira RC, Teixeira BR, Mello FC, Pereira AP, Duarte AS, Bonaldo MC, Bonvicino CR, D'Andrea PS, Lemos ER, 2009. Genetic characterization of a Juquitiba-like viral lineage in Oligoryzomys nigripes in Rio de Janeiro, Brazil. Acta Trop 112: 212218.

    • Search Google Scholar
    • Export Citation
  • 9.

    Oliveira RC, Padula PJ, Gomes R, Martinez VP, Bellomo C, Bonvicino CR, Freire e Lima DI, Bragagnolo C, Caldas AC, D'Andrea PS, Lemos ER, 2011. Genetic characterization of hantaviruses associated with sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in Southern Brazil. Vector Borne Zoonotic Dis 11: 301314.

    • Search Google Scholar
    • Export Citation
  • 10.

    Pereira LE, Suzuki A, Bisord I, Souza RP, Souza LT, Oshiro FM, Cerroni MP, Neto RS, Pinho JR, 2007. Estudo longitudinal da prevalência dos Vírus Juquitiba e Araraquara em roedores das regiões da Mata Atlântica e do Cerrado do Brasil. Bol Epidemiol Paul 4: 213.

    • Search Google Scholar
    • Export Citation
  • 11.

    Figueiredo GG, Borges AA, Campos GM, Machado AM, Saggioro FP, Sabino GS Jr, Badra SJ, Ortiz AA, Figueiredo LT, 2010. Diagnosis of hantavirus infection in humans and rodents in Ribeirão Preto, State of São Paulo, Brazil. Rev Soc Bras Med Trop 43: 348354.

    • Search Google Scholar
    • Export Citation
  • 12.

    Limongi JE, Moreira FG, Peres JB, Suzuki A, Ferreira IB, Souza RP, Pinto RM, Pereira LE, 2013. Serological survey of hantavirus in rodents in Uberlândia, Minas Gerais, Brazil. Rev Inst Med Trop Sao Paulo 55: 155158.

    • Search Google Scholar
    • Export Citation
  • 13.

    Rosa ES, Medeiros DB, Nunes MR, Simith DB, Pereira AD, Elkhoury MR, Santos ED, Lavocat M, Marques AA, Via AV, Kohl VA, Terças AC, D'Andrea PS, Bonvicino CR, 2012. Molecular epidemiology of Laguna Negra virus, Mato Grosso State, Brazil. Emerg Infect Dis 18: 982985.

    • Search Google Scholar
    • Export Citation
  • 14.

    Raboni SM, de Borba L, Hoffmann FG, Noronha L, Azevedo ML, Carstensen S, Mazzarotto GA, Bordignon J, Duarte dos Santos CN, 2009. Evidence of circulation of Laguna Negra-like hantavirus in the Central West of Brazil: case report. J Clin Virol 45: 153156.

    • Search Google Scholar
    • Export Citation
  • 15.

    Johnson AM, Souza LT, Ferreira IB, Pereira LE, Ksiazek TG, Rollin PE, Peters CJ, Nichol ST, 1999. Genetic investigation of novel hantaviruses causing fatal HPS in Brazil. J Med Virol 59: 527535.

    • Search Google Scholar
    • Export Citation
  • 16.

    Rosa ES, Medeiros DB, Nunes MR, Simith DB, Pereira AS, Elkhoury MR, Lavocat M, Marques AA, Via AV, D'Andrea PS, Bonvicino CR, Lemos ER, Vasconcelos PF, 2011. Pygmy rice rat as potential host of Castelo dos Sonhos Hantavirus. Emerg Infect Dis 17: 15271530.

    • Search Google Scholar
    • Export Citation
  • 17.

    Agrellos R, Bonvicino CR, Rosa ES, Marques AA, D'Andrea PS, Weksler M, 2012. The taxonomic status of the Castelo dos Sonhos Hantavirus reservoir. Zootaxa 3220: 128.

    • Search Google Scholar
    • Export Citation
  • 18.

    Rosa ES, Mills JN, Padula PJ, Elkhoury MR, Ksiazek TG, Mendes WS, Santos ED, Araújo GC, Martinez VP, Rosa JF, Edelstein A, Vasconcelos PF, 2005. Newly recognized hantaviruses associated with hantavirus pulmonary syndrome in northern Brazil: partial genetic characterization of viruses and serologic implication of likely reservoirs. Vector Borne Zoonotic Dis 5: 1119.

    • Search Google Scholar
    • Export Citation
  • 19.

    Leduc JW, Smith GA, Pinheiro FP, Vasconcelos PF, Rosa ES, Maiztegui JI, 1985. Isolation of a Hantaan-related virus from Brazilian rats and serologic evidence of its widespread distribution in South America. Am J Trop Med Hyg 34: 810815.

    • Search Google Scholar
    • Export Citation
  • 20.

    Xiao S, Chu Y, Knauert FK, Lofts R, Dalrymple JM, Leduc JW, 1992. Comparison of hantavirus isolates using a genus-reactive primer pair polymerase chain reaction. J Gen Virol 73: 567573.

    • Search Google Scholar
    • Export Citation
  • 21.

    Firth C, Tokarz R, Simith DB, Nunes MR, Bhat M, Rosa ES, Medeiros DB, Palacios G, Vasconcelos PF, Lipkin WI, 2012. Diversity and distribution of hantaviruses in South America. J Virol 86: 1375613766.

    • Search Google Scholar
    • Export Citation
  • 22.

    Chan YC, Wong TW, Yap EH, 1987. Hemorrhagic fever with renal syndrome: clinical, virological and epidemiological perspectives. Ann Acad Med Singapore 16: 696701.

    • Search Google Scholar
    • Export Citation
  • 23.

    Casapia M, Mamani E, Garcia MP, Miraval ML, Valencia P, Quino AH, Álvarez C, Donaires LF, 2012. Síndrome pulmonar por hantavirus (Virus Río Mamoré) en la Amazonía Peruana. Rev Peru Med Exp Salud Publica 29: 390395.

    • Search Google Scholar
    • Export Citation
  • 24.

    Chu YK, Goodin D, Owen RD, Koch D, Jonsson CB, 2009. Sympatry of 2 hantavirus strains, Paraguay, 2003–2007. Emerg Infect Dis 15: 20072010.

  • 25.

    Padula P, Martinez VP, Bellomo C, Maidana S, Juan JS, Tagliaferri P, Bargardi S, Vazquez C, Colucci N, Estévez J, Almirón M, 2007. Pathogenic hantaviruses, northeastern Argentina and eastern Paraguay. Emerg Infect Dis 13: 12111214.

    • Search Google Scholar
    • Export Citation
  • 26.

    Delfraro A, Tomé L, D’Elía G, Clara M, Achával F, Russi JC, Rodonz JR, 2008. Juquitiba-like hantavirus from 2 nonrelated rodent species, Uruguay. Emerg Infect Dis 14: 14471451.

    • Search Google Scholar
    • Export Citation
  • 27.

    Johnson AM, Bowen MD, Ksiazek TG, Williams RJ, Bryan RT, Mills JN, Peters CJ, Nichol ST, 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238: 115127.

    • Search Google Scholar
    • Export Citation
  • 28.

    Carroll DS, Mills JN, Montgomery JM, Bausch DG, Blair PJ, Burans JP, Felices V, Gianella A, Iihoshi N, Nichol ST, Olson JG, Rogers DS, Salazar M, Ksiazek TG, 2005. Hantavirus pulmonary syndrome in Central Bolivia: relationships between reservoir hosts, habitats, and viral genotypes. Am J Trop Med Hyg 72: 4246.

    • Search Google Scholar
    • Export Citation
  • 29.

    Levis S, Garcia J, Pini N, Calderón G, Ramírez J, Bravo D, St Jeor S, Ripoll C, Bego M, Lozano E, Barquez R, Ksiazek TG, Enria D, 2004. Hantavirus pulmonary syndrome in northwestern Argentina: circulation of Laguna Negra virus associated with Calomys callosus. Am J Trop Med Hyg 71: 658663.

    • Search Google Scholar
    • Export Citation
  • 30.

    Williams RJ, Bryan RT, Mills JN, Palma RE, Vera I, De Velasquez F, Baez E, Schmidt WE, Figueroa RE, Peters CJ, Zaki SR, Khan AS, Ksiazek TG, 1997. An outbreak of hantavirus pulmonary syndrome in western Paraguay. Am J Trop Med Hyg 57: 274282.

    • Search Google Scholar
    • Export Citation
  • 31.

    Hjelle BL, Torrez-Martinez N, Koster FT, 1996. Hantavirus pulmonary syndrome-related virus from Bolivia. Lancet 347: 57.

  • 32.

    Bharadwaj M, Boten J, Torrez-Martinez N, Hjelle BL, 1997. Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the Pygmy Rice rat, Oligoryzomys microtis, from Bolivia. Am J Trop Med Hyg 57: 368374.

    • Search Google Scholar
    • Export Citation
  • 33.

    Richter MH, Hanson JD, Cajimat MN, Milazzo ML, Fulhorst CF, 2010. Geographical range of Rio Mamoré virus (family Bunyaviridae, genus Hantavirus) in association with the small-eared pygmy rice rat (Oligoryzomys microtis). Vector Borne Zoonotic Dis 10: 613.

    • Search Google Scholar
    • Export Citation
  • 34.

    Hjelle B, Torres-Pérez F, 2010. Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2: 25592586.

  • 35.

    Chu Y-K, Owen RD, Jonsson CB, 2011. Phylogenetic exploration of hantaviruses in Paraguay reveals reassortment and host switching in South America. Virol J 8: 399.

    • Search Google Scholar
    • Export Citation
  • 36.

    Figueiredo LT, Moreli ML, de Sousa RL, Borges AA, Figueiredo GG, Machado AM, Bisordi I, Nagasse-Sugahara TK, Suzuki A, Pereira LE, Souza RP, Souza LT, Braconi CT, Harsi CM, Zanotto PM, 2009. Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg Infect Dis 15: 561567.

    • Search Google Scholar
    • Export Citation
  • 37.

    Araujo J, Pereira A, Nardi MS, Henriques DA, Lautenschalager DA, Dutra LM, Ometto TL, Hurtado RF, Maués F, Nava A, Morais FA, Aires CC, Favorito S, Durigon EL, 2011. Detection of hantaviruses in Brazilian rodents by SYBR-Green-based real-time RT-PCR. Arch Virol 156: 12691274.

    • Search Google Scholar
    • Export Citation
  • 38.

    Araujo J, Thomazelli LM, Henriques DA, Lautenschalager D, Ometto T, Dutra LM, Aires CC, Favorito S, Durigon EL, 2012. Detection of hantavirus in bats from remaining rain forest in São Paulo, Brazil. BMC Res Notes 5: 690.

    • Search Google Scholar
    • Export Citation
  • 39.

    Oliveira RC, Guterres A, Schrago CG, Fernandes J, Teixeira BR, Zeccer S, Bonvicino CR, D'Andrea PS, Lemos ER, 2012. Detection of the first incidence of Akodon paranaensis naturally infected with the Jabora Virus strain (Hantavirus) in Brazil. Mem Inst Oswaldo Cruz 107: 424428.

    • Search Google Scholar
    • Export Citation
  • 40.

    Cerqueira R, Gentile R, Fernandez FA, D'Andrea PS, 1993. A five-year population study of an assemblage of small mammals in southeastern Brazil. Mammalia 57: 507517.

    • Search Google Scholar
    • Export Citation
  • 41.

    D'Andrea PS, Gentile R, Cerqueira R, Grelle CE, Horta C, Rey L, 1999. Ecology of small mammals in a Brazilian rural area. Rev Bras Zool 16: 611620.

  • 42.

    D'Andrea PS, Gentile R, Maroja LS, Fernandes FA, Coura R, Cerqueira R, 2007. Small mammal populations of an agroecosystem in the Atlantic Forest domain, southeastern Brazil. Braz J Biol 67: 179186.

    • Search Google Scholar
    • Export Citation
  • 43.

    Gentile R, D'Andrea PS, Cerqueira R, Maroja LS, 2000. Population dynamics and reproduction of marsupials and rodents in a Brazilian rural area: a five-year study. Stud Neotrop Fauna Environ 9: 19.

    • Search Google Scholar
    • Export Citation
  • 44.

    Feliciano BR, Fernandez FA, Freitas D, Figueiredo MS, 2002. Population dynamics of small rodents in a grassland between fragments of Atlantic Forest in southeastern Brazil. Mamm Biol 67: 304314.

    • Search Google Scholar
    • Export Citation
  • 45.

    Cademartori CV, Fabián ME, Menegheti JO, 2004. Variações na abundância de roedores (Rodentia, Sigmodontinae) em duas áreas de Floresta Ombrófila Mista, Rio Grande do Sul, Brasil. Rev Bras Zoociências 6: 147167.

    • Search Google Scholar
    • Export Citation
  • 46.

    Cademartori CV, Fabián ME, Menegheti JO, 2005. Biologia reprodutiva de Delomys dorsalis (Hensel, 1872) - Rodentia, Sigmodontinae - em área de floresta ombrófila mista, Rio Grande do Sul, Brasil. Mastozool Neotrop 12: 133144.

    • Search Google Scholar
    • Export Citation
  • 47.

    Bonecker ST, Portugal LG, Costa-Neto SF, Gentile R, 2009. A long term study of small mammal populations in a Brazilian agricultural landscape. Mamm Biol 74: 467477.

    • Search Google Scholar
    • Export Citation
  • 48.

    Antunes PC, Campos MA, Oliveira-Santos LG, Graipel ME, 2010. Population dynamics of Akodon montensis (Rodentia, Cricetidae) in the Atlantic forest of Southern Brazil, 2010. Mamm Biol 75: 186190.

    • Search Google Scholar
    • Export Citation
  • 49.

    Galiano D, Kubiak BB, Marinho JR, Freitas TR, 2013. Population dynamics of Akodon montensis and Oligoryzomys nigripes in an Araucaria forest of Southern Brazil. Mammalia 77: 173179.

    • Search Google Scholar
    • Export Citation
  • 50.

    Bonvicino CR, Oliveira JA, D'Andrea PS, 2008. Guia dos roedores do Brasil, com chaves para gêneros baseadas em caracteres externos. Rio de Janeiro: Centro Pan-Americano de Febre Aftosa - OPAS/OMS.

    • Search Google Scholar
    • Export Citation
  • 51.

    Oliveira JA, Bonvicino CR, 2011. Ordem Rodentia. Reis NR, Peracchi AL, Pedro WA, Lima IP, eds. Mamíferos do Brasil. Second edition. Londrina, PR: Universidade Estadual de Londrina, 358414.

    • Search Google Scholar
    • Export Citation
  • 52.

    Boone JD, Otteson EW, McGwire KC, Villard P, Rowe JE, St Jeor SC, 1998. Ecology and demographics of hantavirus infections in rodent populations in the Walker River Basin of Nevada and California. Am J Trop Med Hyg 59: 445451.

    • Search Google Scholar
    • Export Citation
  • 53.

    Mills JN, Ksiazek TG, Peters CJ, Childs JE, 1999. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg Infect Dis 5: 135142.

    • Search Google Scholar
    • Export Citation
  • 54.

    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 Zoonotic Dis 7: 229240.

    • Search Google Scholar
    • Export Citation
  • 55.

    Suárez OV, Cueto GR, Cavia R, Villafañe IE, Bilenca DN, Edelstein A, Martínez P, Miguel S, Bellomo C, Hodara K, Padula PJ, Busch M, 2003. Prevalence of infection with hantavirus in rodent populations of central Argentina. Mem Inst Oswaldo Cruz 98: 727732.

    • Search Google Scholar
    • Export Citation
  • 56.

    Yahnke CJ, Meserve PL, Ksiazek TG, Mills JN, 2001. Patterns of infection with Laguna Negra virus in wild populations of Calomys laucha in the central Paraguayan chaco. Am J Trop Med Hyg 65: 768776.

    • Search Google Scholar
    • Export Citation
  • 57.

    Owen RD, Goodin DG, Koch DE, Chu Y-K, Jonsson CB, 2010. Spatiotemporal variation in Akodon montensis (Cricetidae: Sigmodontinae) and hantaviral seroprevalence in a subtropical forest ecosystem. J Mammal 91: 467481.

    • Search Google Scholar
    • Export Citation
  • 58.

    Piudo L, Monteverde MJ, Walker RS, Douglass RJ, 2011. Rodent community structure and Andes virus infection in sylvan and peridomestic habitats in northwestern Patagonia, Argentina. Vector Borne Zoonotic Dis 11: 315324.

    • Search Google Scholar
    • Export Citation
  • 59.

    Vadell MV, Bellomo C, San Martín A, Padula P, Villafañe IG, 2011. Hantavirus ecology in rodent populations in three protected areas of Argentina. Trop Med Int Health 16: 13421352.

    • Search Google Scholar
    • Export Citation
  • 60.

    Palma RE, Polop JJ, Owen RD, Mills JN, 2012. Ecology of rodent-associated hantaviruses in the Southern Cone of South America: Argentina, Chile, Paraguay, and Uruguay. J Wildl Dis 48: 267281.

    • Search Google Scholar
    • Export Citation
  • 61.

    Balbinot R, Valério ÁF, Sanquetta CR, Caldeira MV, Silvestre R, 2008. Estoque de carbono em plantações de Pinus spp. em diferentes idades no Sul do Estado do Paraná. Floresta 38: 317324.

    • Search Google Scholar
    • Export Citation
  • 62.

    Mills JN, Childs JE, Ksiazek TG, Peters CJ, 1995. Methods for Trapping and Sampling Small Mammals for Virologic Testing. Atlanta, GA: Center for Disease Control and Prevention.

    • Search Google Scholar
    • Export Citation
  • 63.

    Bonvicino C, Oliveira JA, Gentile R, 2010. A new species of Calomys (Rodentia: Sigmodontinae) from Eastern Brazil. Zootaxa 2336: 1925.

  • 64.

    Bonvicino CR, 2011. Diversidade cariotípica em roedores Akodontini do Brasil. Bol Soc Bras Mastozoologia 62: 711.

  • 65.

    Figueiredo LT, Moreli ML, Borges AA, Figueiredo GG, Badra SJ, Bisordi I, Suzuki A, Capria S, Padula P, 2009. Evaluation of an enzyme-linked immunosorbent assay based on Araraquara virus recombinant nucleocapsid protein. Am J Trop Med Hyg 81: 273276.

    • Search Google Scholar
    • Export Citation
  • 66.

    Mazzarotto GA, Raboni SM, Stella V, Carstensen S, Noronha L, Levis S, Zanluca C, Zanetti CR, Bordignon J, Santos CN, 2009. Production and characterization of monoclonal antibodies against the recombinant nucleoprotein of Araucaria hantavirus. J Virol Methods 162: 96100.

    • Search Google Scholar
    • Export Citation
  • 67.

    Guterres A, Oliveira RC, Fernandes J, D'Andrea PS, Bonvicino CR, Bragagnolo C, Guimarães GD, Almada GL, Machado RR, Lavocat M, Elkhoury MD, Schrago CG, Lemos ER, 2013. Phylogenetic analysis of the S segment from Juquitiba hantavirus: Identification of two distinct lineages in Oligoryzomys nigripes. Infect Genet Evol 18: 262268.

    • Search Google Scholar
    • Export Citation
  • 68.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403410.

  • 69.

    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 27312739.

    • Search Google Scholar
    • Export Citation
  • 70.

    Glass GE, Childs JE, Korch GW, Leduc JW, 1988. Association of intraspecific wounding with hantaviral infection in wild rats (Rattus norvegicus). Epidemiol Infect 101: 459472.

    • Search Google Scholar
    • Export Citation
  • 71.

    Paise G, Vieira EM, 2005. Produção de frutos e distribuição espacial de angiospermas com frutos zoocóricos em uma Floresta Ombrófila Mista no Rio Grande do Sul, Brasil. Rev Bras Bot 28: 615625.

    • Search Google Scholar
    • Export Citation
  • 72.

    Iob G, Vieira EM, 2008. Seed predation of Araucaria angustifolia (Araucariaceae) in the Brazilian Araucaria Forest: influence of deposition site and comparative role of small and “large” mammals. Plant Ecol 198: 185196.

    • Search Google Scholar
    • Export Citation
  • 73.

    Vieira EM, Ribeiro JF, Iob G, 2011. Seed predation of Araucaria angustifolia (Araucariaceae) by small rodents in two areas with contrasting seed densities in the Brazilian Araucaria Forest. J Nat Hist 45: 843854.

    • Search Google Scholar
    • Export Citation
  • 74.

    Fonseca GA, Kierulff MC, 1989. Biology and natural history of Brazilian Atlantic forest small mammals. Bull Fla State Mus Biol Sci 34: 99152.

    • Search Google Scholar
    • Export Citation
  • 75.

    Graipel ME, Cherem JJ, Monteiro-Filho EL, Glock L, 2006. Dinâmica populacional de marsupiais e roedores no Parque Municipal da Lagoa do Peri, Ilha de Santa Catarina, sul do Brasil. Mastozoología Neotrop 13: 3149.

    • Search Google Scholar
    • Export Citation
  • 76.

    Hardestam J, Karlsson M, Falk KI, Olsson G, Klingström J, Lundkvist A, 2008. Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg Infect Dis 14: 12091215.

    • Search Google Scholar
    • Export Citation
  • 77.

    Calisher CH, Sweeney W, Mills JN, Beaty BJ, 1999. Natural history of Sin Nombre virus in western Colorado. Emerg Infect Dis 5: 126134.

  • 78.

    Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL, 2004. Wounding: the primary mode of Seoul virus transmission among male Norway Rats. Am J Trop Med Hyg 70: 310317.

    • Search Google Scholar
    • Export Citation
  • 79.

    Escutenaire S, Chalon P, De Jaegere F, Karelle-bui L, Mees G, Brochier B, Rozenfeld F, Pastoret P, 2002. Behavioral, physiologic, and habitat influences on the dynamics of Puumala Virus infection in Bank Voles (Clethrionomys glareolus). Emerg Infect Dis 8: 930936.

    • Search Google Scholar
    • Export Citation
  • 80.

    Vieira EM, Paise G, Machado PH, 2006. Feeding of small rodents on seeds and fruits: a comparative analysis of three species of rodents of the Araucaria Forest, southern Brazil. Acta Theriol (Warsz) 51: 311318.

    • Search Google Scholar
    • Export Citation
  • 81.

    Bohlman MC, Morzunov SP, Meissner J, Taylor MB, Ishibashi K, Rowe J, Levis S, Enria D, Jeor SC, 2002. Analysis of hantavirus genetic diversity in Argentina: S segment-derived phylogeny. J Virol 76: 37653773.

    • Search Google Scholar
    • Export Citation
  • 82.

    Salazar-Bravo J, Armién B, Suzán G, Armién A, Ruedas LA, Avila M, Zaldívar Y, Pascale JM, Gracia F, Yates TL, 2004. Serosurvey of wild rodents for hantaviruses in Panama, 2000–2002. J Wildl Dis 40: 103109.

    • Search Google Scholar
    • Export Citation
  • 83.

    Raboni SM, Rubio G, de Borba L, Zeferino A, Skraba I, Goldenberg S, Dos Santos CN, 2005. Clinical survey of hantavirus in southern Brazil and the development of specific molecular diagnosis tools. Am J Trop Med Hyg 72: 800804.

    • Search Google Scholar
    • Export Citation
  • 84.

    Monroe MC, Morzunov SP, Johnson AM, Bowen MD, Artsob H, Yates T, Peters CJ, Rollin PE, Ksiazek TG, Nichol ST, 1999. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg Infect Dis 5: 7586.

    • Search Google Scholar
    • Export Citation
  • 85.

    Santos ED, Coelho GE, Silva LR, Camargo NJ, Rúbio GG, Correa DS, Stremel N, Elkhoury MR, Oliveira RC, Martins EC, Ferreira IB, Pereira LE, Hatch DL, 2002. Fatores de risco para infecção por hantavirus entre trabalhadores florestais no Paraná, agosto a novembro de 2000. Boletim eletrônico epidemiológico - Ministério da Saúde, Brasil Ano 2: 89. Available at: http://portal.saude.gov.br/portal/arquivos/pdf/ano02_n01_fatores_risco_hantavirus_pr.pdf. Accessed July 8, 2013.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Paulo S. D'Andrea and Bernardo R. Teixeira, Laboratório de Biologia e Parasitologia de Mamíferos Silvestres Reservatórios, Instituto Oswaldo Cruz/FIOCRUZ - Av. Brasil,