Nothing Special   »   [go: up one dir, main page]

Skip to main content
Log in

Global Diversity and Distribution of Hantaviruses and Their Hosts

  • Review
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Rodents represent 42% of the world’s mammalian biodiversity encompassing 2,277 species populating every continent (except Antarctica) and are reservoir hosts for a wide diversity of disease agents. Thus, knowing the identity, diversity, host–pathogen relationships, and geographic distribution of rodent-borne zoonotic pathogens, is essential for predicting and mitigating zoonotic disease outbreaks. Hantaviruses are hosted by numerous rodent reservoirs. However, the diversity of rodents harboring hantaviruses is likely unknown because research is biased toward specific reservoir hosts and viruses. An up-to-date, systematic review covering all known rodent hosts is lacking. Herein, we document gaps in our knowledge of the diversity and distribution of rodent species that host hantaviruses. Of the currently recognized 681 cricetid, 730 murid, 61 nesomyid, and 278 sciurid species, we determined that 11.3, 2.1, 1.6, and 1.1%, respectively, have known associations with hantaviruses. The diversity of hantaviruses hosted by rodents and their distribution among host species supports a reassessment of the paradigm that each virus is associated with a single-host species. We examine these host–virus associations on a global taxonomic and geographical scale with emphasis on the rodent host diversity and distribution. Previous reviews have been centered on the viruses and not the mammalian hosts. Thus, we provide a perspective not previously addressed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aberle SW, Lehner P, Ecker M, Aberle JH, Arneitz K, Khanakah G, Radda A, Radda I, Popow-Kraupp T, Kunz C, Heinz FX (1999) Nephropatia epidemica and Puumala virus in Austria European Journal of Clinical Microbiology and Infectious Diseases 18:467-472

    Article  PubMed  CAS  Google Scholar 

  • Aguirre AA, Ostfeld RS, Daszak P (editors) (2012) New Directions in Conservation Medicine: Applied Cases of Ecological Health. New York: Oxford University Press, 639 pp

  • Alemán A, Iguarán H, Puerta H, Cantillo C, Mills J, Ariz W, Mattar S (2006) Primera evidencia serológica de infección por hantavirus en roedores, en Colombia. Revista Panamericana de Salud Pública 8(1):1-12

    Article  Google Scholar 

  • Amman BR, Manangan AP, Flietstra TD, Calisher CH, Carroll DS, Wagoner KD, Mills JN (2013) Association between movement and Sin Nombre virus (Bunyaviridae: Hantavirus) infection in North American deermice (Peromyscus maniculatus) in Colorado. The Journal of Wildlife Diseases 49(1):132-142. https://doi.org/10.7589/2012-02-041

    Article  PubMed  Google Scholar 

  • Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM, Solovyov A, Ojeda-Flores R, Arrigo NC, Islam A, Khan SA, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JAK, Daszak P, Lipkin WI (2013) A strategy to estimate unknown viral diversity in mammals. mBio 4(5):e00598-13. https://doi.org/10.1128/mbio.00598-13

  • Arai S, Song JW, Sumibcay L, Bennett SN, Nerurkar VR, Parmenter C, Cook J a., Yates TL, Yanagihara R (2007) Hantavirus in northern short-tailed shrew, United States. Emerging Infectious Diseases 13(9):1420–1423. https://doi.org/10.3201/eid1309.070484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arai S, Bennett SN, Sumibcay L, Cook J, Song JW, Hope A, Parmenter C, Nerurkar VR, Yates TL, Yanagihara R (2008a) Short report: Phylogenetically distinct hantaviruses in the masked shrew (Sorex cinereus) and dusky shrew (Sorex monticolus) in the United States. American Journal of Tropical Medicine and Hygiene 78(2):348-351

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aria S, Ohdachi SD, Asakawa M, Kang HJ, Mocz G, Arikawa J, Okabe N, Yanagihara R (2008b) Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole (Urotrichus talpoides). Proceedings of the National Academy of Sciences 105(42):16296-16301 https://doi.org/10.1073/pnas.0808942105

    Article  Google Scholar 

  • Arai S, Gu SH, Baek LJ, Tabara K, Bennett SN, Oh HS, Takada N, Kang HJ, Tanaka-Taya K, Morikawa S, Okabe N, Yanagihara R, Song JW (2012) Divergent lineages of newfound hantaviruses harbored by phylogenetically related crocidurine shrew species in Korea Virology 424(2):99-105 https://doi.org/10.1016/j.virol.2011.11.013

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Arai S, Nguyen ST, Boldgiv B, Fukui D, Araki K, Dang CN, Ohdachi SD, Pham TD, Boldbaatar B, Satoh H, Yoshikawa Y, Morikawa S, Tanaka-Taya K, Yanagihara R, Oishi K (2013) Novel bat-borne hantavirus, Vietnam. Emerging Infectious Diseases 19(7):1159-1161

    Article  PubMed  PubMed Central  Google Scholar 

  • Araujo J, Pereira A, Nardi M, Henriques D, Lautenschalager D, Dutra L, Ometto T, Hurtado R, Maue´s F, Nava A, Morais FA, Aires CC, Favorito S, Durigon EL (2011) Detection of hantaviruses in Brazilian rodents by sybr-green-based realtime RT- PCR. Archives of Virology. https://doi.org/10.1007/s00705-011-0968-1

    Article  PubMed  Google Scholar 

  • Arellano E, Castro-Arellano I, Suzán G, González-Cózatl FX, Jiménez RM (2012) Antibody Seroprevalence to hantaviruses in rodents from Reserva De La Biosfera Sierra De Huautla, Morelos. Western North American Naturalist 72(1):105-109 https://doi.org/10.3398/064.072.0114

    Article  Google Scholar 

  • Armién A, Armie´n B, Koster F, Pascale J, Avila M, Gonzalez P, de la Cruz M, Zaldivar Y, Mendoza Y, Gracia F, Hjelle B, Lee SJ, Yates TL, Salazar-Bravo J (2009) Hantavirus infection and habitat associations among rodent populations in agroecosystems of Panama: implications for human disease risk. The American Journal of Tropical Medicine and Hygiene 81(1):59–66

    Article  PubMed  Google Scholar 

  • Arthur RR, Lofts RS, Gomez J, Glass GE, LeDuc JW, Childs JE (1992) Grouping of hantaviruses by small (s) genome segment polymerase chain reaction and amplification of viral RNA from wild-caught rats. American Journal of Tropical Medicine and Hygiene 47(2):210-224

    Article  PubMed  CAS  Google Scholar 

  • Avšić-Županc T, Xiao SY, Stojanovic R, Gligic A, Van Der Groen G, Leduc JW (1992) Characterization of Dobrava virus: a hantavirus from Slovenia, Yugoslavia. Journal of Medical Virology 38:132-137

    Article  PubMed  Google Scholar 

  • Baek LJ, Yanagihara R, Gibbs CJ Jr, Miyazaki M, Gajdusek DC (1988) Leaky virus: a new hantavirus isolated from Mus musculus in the United States. Journal of General Virology 69:3129-3132

    Article  PubMed  Google Scholar 

  • Baek LJ, Kariwa H, Lokugamage K, Yoshimatsu K, Arikawa J, Takashima I, Kang JI, Moon SS, Chung SY, Kim EJ, Kang HJ, Song KJ, Klein TA, Yanagihara R, Song JW (2006) Soochong virus: an antigenically and genetically distinct hantavirus isolated from Apodemus peninsulae. Journal of Medical Virology 78:290-297

    Article  PubMed  CAS  Google Scholar 

  • Bennett, SN, Gu SH, Kang HJ, Arai S, Yanagihara R (2014) Reconstructing the evolutionary origins and phylogeography of hantaviruses. Trends in Microbiology 22(8):473-482

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bharadwaj M, Botten J, Torrez-Martinez N, Hjelle B (1997) Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the pygmy rice rat, Oligoryzomys microtus, from Bolivia. American Journal of Tropical Medicine and Hygiene 57:368-34

    Article  PubMed  CAS  Google Scholar 

  • Bi Z, Formenty PBH, Roth CE (2008) Hantavirus infection: a review and global update. Journal of Infection in Developing Countries 2(1):3-23 https://doi.org/10.3855/jidc.317

    Article  PubMed  Google Scholar 

  • Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507-512 https://doi.org/10.1038/nature05634

    Article  PubMed  CAS  Google Scholar 

  • Blasdell K, Cosson JF, Chaval Y, Herbreteau V, Douangboupha B, Jittapalapong S, Lundqvist Å, Hugot JP, Morand S, Buchy P (2011) Rodent-borne hantaviruses in Cambodia, Lao PDR, and Thailand. EcoHealth 8:432-443 https://doi.org/10.1007/s10393-011-0725-7

    Article  PubMed  Google Scholar 

  • Bohlman MC, Morzunov SP, Meissner J, Taylor MB, Ishibashi K, Rowe J, Levis S, Enria D, St Jeor SC (2002) Analysis of hantavirus genetic diversity in Argentina: s segment-derived phylogeny. Journal of Virology 76:3765-73 https://doi.org/10.1128/jvi.76.8.3765

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bradley RD, Durish ND, Rogers DS, Miller JR, Engstrom MD, Kilpatrick CW (2007) Toward a molecular phylogeny for Peromyscus: evidence from mitochondrial cytochrome-b sequences. Journal of Mammalogy 88(5):1146-1159

    Article  PubMed  PubMed Central  Google Scholar 

  • Brummer-Korvenkontio M, Vaheri A, Hovi T, Von Bonsdorff CH, Vuorimies J, Manni T, Penttinen K, Oker-Blom N, Lähdevirta J (1980) Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. Journal of Infectious Diseases 141(2):131-134 https://doi.org/10.1093/infdis/141.2.131

    Article  PubMed  CAS  Google Scholar 

  • Calisher CH, Mills JN, Sweeney WP, Choate JR, Sharp DE, Canestorp KM, Beaty BJ (2001) Do unusual site-specific population dynamics of rodent reservoirs provide clues to the natural history of hantaviruses? The Journal of Wildlife Diseases 37(2):280-288 https://doi.org/10.7589/0090-3558-37.2.280

    Article  PubMed  CAS  Google Scholar 

  • Calisher CH, Root JJ, Mills JN, Beaty BJ (2002) Assessment of ecologic and biologic factors leading to hantavirus pulmonary syndrome, Colorado, U.S.A. Croatian Medical Journal 43(3):330-337

    PubMed  Google Scholar 

  • Calisher CH, Mills JN, Root JJ, Doty JB, Beaty BJ (2011) The relative abundance of deer mice with antibody to Sin Nombre virus corresponds to the occurrence of hantavirus pulmonary syndrome in nearby humans. Vector-Borne and Zoonotic Diseases 11(5):577-582 https://doi.org/10.1089/vbz.2010.0122

    Article  PubMed  Google Scholar 

  • Carey DE, Reuben R, Panicker KN, Shope RE, Myers RM (1971) Thottapalayam virus: a presumptive arborvirus isolated from a shrew in India. Indian Journal of Medical Research 59:1758-1760

    PubMed  CAS  Google Scholar 

  • 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. American Journal of Tropical Medicine and Hygiene 72(1):42-46

    Article  PubMed  Google Scholar 

  • Castro-Arellano I, Suzán G, León RF, Jiménez RM, Lacher TE Jr. (2009) Survey for antibody to hantaviruses in Tamaulipas, México. Journal of Wildlife Diseases 45(1):207-212

    Article  PubMed  Google Scholar 

  • Ceballos G (2014) Mammals of Mexico. John Hopkins University Press, Baltimore, Maryland.

    Google Scholar 

  • Chandy S, Abraham P, Sridharan G (2008) Hantaviruses: an emerging public health threat in India? A review. Journal of Biosciences 33(4):495-504 https://doi.org/10.1007/s12038-008-0068-x

    Article  PubMed  CAS  Google Scholar 

  • Childs JE, Ksiazek TG, Spiropoulou CF, Krebs JW, Morzunov S, Maupin GO, Gage KL, Rollin PE, Sarisky J, Enscore RE (1994) Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. Journal of Infectious Diseases 169:1271-1280 https://doi.org/10.1093/infdis/169.6.1271

    Article  PubMed  CAS  Google Scholar 

  • Chin C, Chiueh TS, Yang WC, Yang TH, Shih CM, Lin HT, Lin CK, Lien JC, Tsai TF, Ruo SL, Nichol ST, Ksiazek TG, Rollin PE, Peters CJ, Wu TN, Shen CY (2000) Hantavirus infection in Taiwan: the experience of a geographically unique area. Journal of Medical Virology 60:237-247

    Article  PubMed  CAS  Google Scholar 

  • Chu Y-K, Owen RD, Gonzalez LM, Jonsson CB (2003) The complex ecology of hantavirus in Paraguay. American Journal of Tropical Medicine and Hygiene 69(3):263-268

    Article  PubMed  Google Scholar 

  • Chu YK, Milligan B, Owen RD, Goodin DG, Jonsson CB (2006) Phylogenetic and geographical relationships of hantavirus strains in eastern and western Paraguay. American Journal of Tropical Medicine and Hygiene 75(6):1127-34

    Article  PubMed  PubMed Central  Google Scholar 

  • Chu YK, Owen RD, Sánchez-Hernández C, Romero-Almaraz MDL, Jonsson CB (2008) Genetic characterization and phylogeny of a hantavirus from Western Mexico. Virus Research 131:180-188 https://doi.org/10.1016/j.virusres.2007.09.007

    Article  PubMed  CAS  Google Scholar 

  • Chu Y-K, Goodin D, Owen RD, Koch D, Jonsson CB (2009) Sympatry of 2 hantavirus strains, Paraguay, 2003-2007. Emerging Infectious Diseases 15(12):1977-1980 https://doi.org/10.3201/eid1512.090338

    Article  PubMed  PubMed Central  Google Scholar 

  • Cross RW, Waffa B, Freeman A, Riegel C, Moses LM, Bennett A, Safronetz D, Fischer ER, Feldmann H, Voss TG, Bausch DG (2014) Old World hantaviruses in rodents in New Orleans, Louisiana. American Journal of Tropical Medicine and Hygiene 90(5):897-901 https://doi.org/10.4269/ajtmh.13-0683

    Article  PubMed  PubMed Central  Google Scholar 

  • Cuong NV, Carrique-Mas J, Be HV, An NN, Tue NT, Anh NL, Anh PH, Phuc NT, Baker S, Voutilainen L, Jääskeläinen A, Huhtamo E, Utrianen M, Sironen T, Vaheri A, Henttonen H, Vapalahti O, Chaval Y, Morand S, Bryant JE (2015) Rodents and risk in the Mekong Delta of Vietnam: seroplrevalence of selected zoonotic viruses in rodents and humans. Vector-Borne and Zoonotic Diseases 15(1):65-72 https://doi.org/10.1089/vbz.2014.1603

    Article  PubMed  PubMed Central  Google Scholar 

  • Cvetko L, Markotić A, Plyusnina A, Margaletić J, Miletić-Medved M, Turk N, Milas Z, Avšič-Županc T, Plyusnin A (2005) Puumala virus in Croatia in the 2002 HFRS outbreak. Journal of Medical Virology 77:290-294 https://doi.org/10.1002/jmv.20448

    Article  PubMed  Google Scholar 

  • Davies TJ, Pedersen AB (2008) Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society B 275:1695–1701. https://759doi.org/10.1098/rspb.2008.0284

  • de 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 Research Notes 5:690. http://www.biomedcentral.com/1756-0500/5/690

  • de Oliveira RC, Padula PJ, Gomes R, Martinez VP, Bellomo C, Bonvicino CR, e Lima DIF, Bragagnolo C, Caldas ACS, D’Andrea PS, de Lemos ERS (2011) Genetic characterization of hantaviruses associated with Sigmodontine rodents in an endemic area for hantavirus pulmonary syndrome in southern Brazil. Vector-Borne and Zoonotic Diseases 11:301–314 https://doi.org/10.1089/vbz.2010.0001

    Article  PubMed  Google Scholar 

  • de Oliveira RC, Guterres A, Guerra Schrago C, Fernandes J, Rodrigues Teixeira B, Zeccer S, Bonvicino CR, D’Andrea PS, Sampaio de Lemos ER (2012) Detection of the first incidence of Akodon paranensis naturally infected with the Jabora virus strain (Hantavirus) in Brazil. Memórias do Instituto Oswaldo Cruz 107(3):424-428

    Article  PubMed  Google Scholar 

  • de Thoisy B, Matheus S, Catzeflis F, Clement L, Barrioz S, Guidez a., Donato D, Cornu J-F, Brunaux O, Guitet S, Lacoste V, Lavergne a. (2014) Maripa hantavirus in French Guiana: phylogenetic position and predicted spatial distribution of rodent hosts. American Journal of Tropical Medicine and Hygiene 90(6):988-992 https://doi.org/10.4269/ajtmh.13-0257

    Article  PubMed  PubMed Central  Google Scholar 

  • Dearing MD, Dizney L (2010) Ecology of hantavirus in a changing world. Annals of the New York Academy of Sciences 1195:99-112 https://doi.org/10.1111/j.1749-6632.2010.05452.x

    Article  PubMed  Google Scholar 

  • Dearing MD, Mangione AM, Karasov WH, Morzunov S, Otteson E, St Jeor S (1998) Prevalence of hantavirus in four species of Neotoma from Arizona and Utah. Journal of Mammalogy 79(4):1254–1259

    Article  Google Scholar 

  • Dekonenko A, Yakimenko V, Ivanov A, Morozov, Nikitin P, Khasanova S, Dzagurova T, Tkachenko E, Schmaljohn C (2003) Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin. Infection, Genetics, and Evolution 3:245-257 https://doi.org/10.1016/s1567-1348(03)00088-1

    Article  CAS  Google Scholar 

  • Delfraro A, Clara M, Tomé L, Achaval F, Levis S, Calderón G, Enria D, Lozano M, Russi J, Arbiza J (2003) Yellow pygmy rice rat (Oligoryzomys flavescens) and hantavirus pulmonary syndrome in Uruguay. Emerging Infectious Diseases 9:846-852 https://doi.org/10.3201/eid0907.030044

    Article  PubMed  PubMed Central  Google Scholar 

  • Delfraro A, Tomé L, D’Elía G, Clara M, Achával F, Russi JC, Rodonz JRA (2008) Juquitiba-like hantavirus from 2 nonrelated rodent species, Uruguay. Emerging Infectious Diseases 14:1447-1451 https://doi.org/10.3201/eid1409.080455

    Article  PubMed  PubMed Central  Google Scholar 

  • Drebot MA, Gavrilovskaya I, Mackow ER, Chen Z, Lindsay R, Sanchez AJ, Nichol ST, Artsob H (2001) Genetic and serotypic characterization of Sin Nombre-like viruses in Canadian Peromyscus maniculatus mice. Virus Research 75:75-86 https://doi.org/10.1016/s0168-1702(01)00227-1

    Article  PubMed  CAS  Google Scholar 

  • Dupinay T, Pounder KC, Ayral F, Laaberki MH, Martson DA, Lacôte S, Rey C, Barbet F, Voller K, Nazaret N, Artois M, Marianneau P, Lachuer J, Fooks AR, Pépin M, Legras-Lachuer C, McElhinney LM (2014) Detection and genetic characterization of Seoul virus from commensal brown rats in France. Virology Journal 11:32 http://www.virologyj.com/content/11/1/32

  • Dzagurova TK, Witkowski PT, Tkachenko EA, Klempa B, Morozov VG, Auste B, Zavora DL, Iunicheva IV, Mutnih ES, Kruger DH (2012) Isolation of Sochi virus from a fatal case of hantavirus disease with fulminant clinical course. Clinical Infectious Diseases 54(1):e1-e4 https://doi.org/10.1093/cid/cir476

    Article  PubMed  Google Scholar 

  • Elwell MR, Ward GS, Tingpalapong M, LeDuc JW (1985) Serologic evidence of Hantaan-like virus in rodents and man in Thailand. Southeast Asian Journal of Tropical Medicine and Public Health 16:349-354

    PubMed  CAS  Google Scholar 

  • Enria DA, Briggiler AM, Pini N, Levis S (2001) Clinical manifestations of New World hantaviruses. Current Topics in Microbiology and Immunology 256:117-34 https://doi.org/10.1007/978-3-642-56753-7_7

    Article  PubMed  CAS  Google Scholar 

  • Ezenwa VO, Prieur-Richard AH, Roche B, Bailly X, Becquart P, García-Peña GE, Hosseini PR, Keesing F, Rizzoli A, Suzán G, Vignuzzi M, Vittecoq M, Mills JN, Guégan JF (2015) Interdisciplinarity and infectious diseases: an ebola case study. PLOS Pathogens https://doi.org/10.1371/journal.ppat.1004992

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernández J, Villagra E, Yung V, Tognarelli J, Araya P, Mora J, Cattan P, Ramírez E (2008) Identificacio´n de hantavirus Andes en Rattus norvegicus. Archivos de medicina veterinaria 40:295–298. https://doi.org/10.4067/S0301-732X2008000300011

    Article  Google Scholar 

  • Figueiredo LTM, Moreli ML, de Sousa RLM, Borges AA, de Figueiredo GG, Machado AM, Bisordi I, Nagasse-Sugahara TK, Suzuki A, Pereira LE, de Souza RP, de Souza LTM, Braconi CT, Harsi CM, de Andrade Zanotto PM, the Viral Diversity Network Consortium (2009) Hantavirus pulmonary syndrome, Central Plateau, southeastern, and southern Brazil. Emerging Infectious Diseases 15(4):561-567

    Article  CAS  Google Scholar 

  • Figueiredo GG, Borges AA, Campos GM, Machado AM, Saggioro FB, dos Santos Sabino Ju´ nior G, Jabur Badra SJ, Ortiz AAA, Figueiredo LTM (2010) Diagnosis of hantavirus infection in humans and rodents in Riberão, Preto, state of São Paulo, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 43:348–354

    Article  PubMed  Google Scholar 

  • Firth C, Tokarz R, Simith DB, Nunes MRT, Bhat M, Rosa EST, Medeiros DBA, Palacios G, Vasconcelos PFC, Lipkin WI (2012) Diversity and distribution of hantaviruses in South America. Journal of Virology 86:13756-13766 https://doi.org/10.1128/jvi.02341-12

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fulhorst CF, Monroe MC, Salas RA, Duno G, Utrera A, Ksiazek TG, Nichol ST, De Manzione NMC, Tovar D, Tesh RB (1997) Isolation, characterization and geographic distribution of Cano Delgadito virus, a newly discovered South American hantavirus (family Bunyaviridae). Virus Research 51:159-171 https://doi.org/10.1016/s0168-1702(97)00091-9

    Article  PubMed  CAS  Google Scholar 

  • Fulhorst CF, Cajimat MN., Utrera A, Milazzo ML, Duno GM (2004) Maporal virus, a hantavirus associated with the fulvous pygmy rice rat (Oligoryzomys fulvescens) in western Venezuela. Virus Research 104:139-144 https://doi.org/10.1016/j.virusres.2004.03.009

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez Della Valle M, Edelstein A, Miguel S, Martinez V, Cortez J, Cacace ML, Jurgelenas G, Sosa Estani S, Padula P (2002) Andes virus associated with hantavirus pulmonary syndrome in northern Argentina and determination of the precise site of infection. American Journal of Tropical Medicine and Hygiene 66(6):713-720

    Article  PubMed  CAS  Google Scholar 

  • González-Ittig RE, Rivera PC, Levis SC, Calderón GE, Gardenal CN (2014) The molecular phylogenetics of the genus Oligoryzomys (Rodentia: Cricetidae) clarifies rodent host-hantavirus associations. Zoological Journal of the Linnean Society 171:457-474 https://doi.org/10.1111/zoj.12133

    Article  Google Scholar 

  • Goodin DG, Paige R, Owen RD, Ghimire K, Koch DE, Chu Y-K, Jonsson CB (2009) Microhabitat characteristics of Akodon montensis, a reservoir for hantavirus, and hantaviral seroprevalence in an Atlantic forest site in eastern Paraguay. Journal of Vector Ecology 34:104-113. https://doi.org/10.1111/j.1948-7134.2009.00013.x

    Article  PubMed  Google Scholar 

  • Gu SH, Markowski J, Kang HJ, Hejduk J, Sikorska B, Liberski PP, Yanagihara R (2013a) Boginia virus, a newfound hantavirus harbored by the Eurasian water shrew (Neomys fodiens) in Poland. Virology Journal 10:160 http://www.virologyj.com/content/10/1/160

  • Gu SH, Nicolas V, Lalis A, Sathirapongsasuti N, Yanagihara R (2013b) Complete genome sequence and molecular phylogeny of a newfound hantavirus harbored by the Doucet’s musk shrew (Crocidura douceti) in Guinea. Infection, Genetics, and Evolution 20:118-123 https://doi.org/10.1016/j.meegid.2013.08.016

    Article  CAS  Google Scholar 

  • Guo WP, Lin XD, Wang, Zhang XH, Chen Y, Cao JH, Ni QX, Li WC, Li MH, Plyusnin A, Zhang YZ (2011) A new subtype of Thottapalayam virus carried by the Asian house shrew (Suncus murinus) in China. Infection, Genetics, and Evolution 11:1862-1867 https://doi.org/10.1016/j.meegid.2011.07.013

    Article  CAS  Google Scholar 

  • Guo WP, Lin XD, Wang W, Tian JH, Cong ML, Zhang HL, Wang MR, Zhou RH, Wang JB, Li MH, Xu J, Holmes EC, Zhang YZ (2013) Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLOS Pathogens 9(2):e1003159 https://doi.org/10.1371/journal.ppat.1003159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guterres A, de Oliveira R, Fernandes J, Strecht L, Casado F, Gomes de Oliveira F, D’Andrea P, Bonvicino C, Schrago C, Sampaio de Lemos E (2014) Characterization of Juquitiba Virus in Oligoryzomys fornesi from Brazilian Cerrado. Viruses 6:1473-1482 https://doi.org/10.3390/v6041473

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Halliday J, Daborn C, Auty H, Mtema Z, Lembo T, Bronsvoort BMD, Handel I, Knobel D, Hampson K, Cleaveland S (2012) Bringing together emerging and endemic zoonoses surveillance: shared challenges and a common solution. Philosophical Transactions of the Royal Society Biological Sciences 367:2872-2880 https://doi.org/10.1098/rstb.2011.0362

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanson JD, Utrera A, Fulhorst CF (2011) The delicate pygmy rice rat (Oligoryzomys delicatus) is the principal host of Maporal Virus (Family Bunyaviridae, Genus Hantavirus). Vector-Borne and Zoonotic Diseases 11:691-696 https://doi.org/10.1089/vbz.2010.0128

    Article  PubMed  PubMed Central  Google Scholar 

  • Hepojoki J, Strandin T, Lankinen H, Vaheri A (2012) Hantavirus structure- molecular interactions behind the scene. Journal of General Virology 93:1631-1644 https://doi.org/10.1099/vir.0.042218-0

    Article  PubMed  CAS  Google Scholar 

  • Herbreteau V, Gonzalez JP, Hugot JP (2006) Implication of phylogenetic systematics of rodent-borne hantaviruses allows understanding of their distribution. Annals of the New York Academy of Sciences 1081:39-56 https://doi.org/10.1196/annals.1373.004

    Article  PubMed  CAS  Google Scholar 

  • Heyman P, Van Mele R, De Jaegere F, Klingström J, Vandenvelde C, Lundkvist Å, Rozenfeld F, Zizi M (2002) Distribution of hantavirus in Belgium. Acta Tropica 84:183-188

    Article  PubMed  CAS  Google Scholar 

  • Heyman P, Plyusnina A, Berny P, Cochez C, Atrois M, Zizi M, Pirnay JP, Plyusnin A (2004) Seoul hantavirus in Europe: first demonstration of the virus genome in wild Rattus norvegicus captured in France. European Journal of Clinical Microbiology & Infectious Diseases 23:711-717 https://doi.org/10.1007/s10096-004-1196-3

    Article  CAS  Google Scholar 

  • Heyman P, Baert K, Plyusnina A, Cochez C, Lundkvist Å, Van Esbroeck M, Goossens E, Vandenvelde C, Plyusnin A, Stuyck J (2009) Serological and genetic evidence for the presence of Seoul hantavirus in Rattus norvegicus in Flanders, Belgium. Scandinavian Journal of Infectious Diseases 41:51-56 https://doi.org/10.1080/00365540802459994

    Article  PubMed  Google Scholar 

  • Heyman P, Ceianu CS, Christova I, Tordo N, Beersma M, Alves MJ, Lundkvist Å, Hukic M, Papa A, Tenorio A, Zelená H, Eßbauer S, Visontai I, Golovljova I, Connell J, Nicoletti L, Van Esbroeck M, Dudman SG, Aberle SW, Avšić-Županc T, Korukluoglu G, Nowakowska A, Klempa B, Ulrich RG, Bino S, Engler O, Opp M, Vaheri A (2011a) A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005-2010. Eurosurveillance 16:2005-2010

  • Heyman P, Cochez C, Korukluoğlu G, Gözalan A, Uyar Y, Lundkvist Å (2011b) Bridging continents; hantaviruses of Europe and Asia Minor. Türk Hijyen ve Deneysel Biyoloji Dergisi 68(1):41-48. https://doi.org/10.5505/turkhijyen.2011.33254

  • Hjelle B, Chavez-Giles F, Torrez-Martinez N, Yates T, Sarisky J, Webb J, Ascher M (1994) Genetic identification of a novel hantavirus of the harvest mouse Reithrodontomys megalotis. Journal of Virology 68:6751–6754

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hjelle B, Anderson B, Torrez-Martinez N, Song W, Gannon WL, Yates TL (1995a) Prevalence and geographic genetic variation of hantaviruses of New World harvest mice (Reithrodontomys): identification of a divergent genotype from a Costa Rican Reithrodontomys mexicanus. Virology 207:452–459

    Article  PubMed  CAS  Google Scholar 

  • Hjelle BF, Jenison SA, Goade DE, Green WB, Feddersen RM, Scott AA (1995b) Hantaviruses: clinical, microbiologic, and epidemiologic aspects. Critical Reviews in Clinical Laboratory Sciences 32:469-508

    Article  PubMed  CAS  Google Scholar 

  • Hjelle B, Lee SW, Song W, Torrez-Martinez N, Song JW, Yanagihara R, Gavrilovskaya I, Mackow ER (1995c) Molecular linkage of hantavirus pulmonary syndrome to the white-footed mouse, Peromyscus leucopus: genetic characterization of the m genome of New York virus. Journal of Virology 69:8137-8141

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hjelle B, Torrez-Martinez N, Koster FT, Jay M, Ascher MS, Brown T, Reynolds P, Ettestad P, Voorhees RE, Sarisky J, Enscore RE, Sands L, Mosley DG, Kioski C, Bryan RT, Sewell CM (1996) Epidemiologic linkage of rodent and human hantavirus genomic sequences in case investigations of hantavirus pulmonary syndrome. Journal of Infectious Diseases 173:781-786

    Article  PubMed  CAS  Google Scholar 

  • Holmes EC, Zhang YZ (2015) The evolution and emergence of hantaviruses. Current Opinion in Virology 10:27-33 https://doi.org/10.1016/j.coviro.2014.12.007

    Article  PubMed  Google Scholar 

  • Hörling J, Chizhikov V, Lundkvist A, Jonsson M, Ivanov L, Dekonenko A, Niklasson B, Dzagurova T, Peters CJ, Tkachenko E, Nichol S (1996) Khabarovsk virus: a phylogenetically and serologically distinct hantavirus isolated from Microtus fortis trapped in far-east Russia. Journal of General Virology 77(4):687-94 https://doi.org/10.1099/0022-1317-77-4-687

    Article  PubMed  Google Scholar 

  • Huong VTQ, Yoshimatsu K, Luan VD, Tuan LV, Nhi L, Arikawa J, Nguyen TMN (2010) Hemorrhagic fever with renal syndrome, Vietnam. Emerging Infectious Diseases 16(2):363-365

    Article  PubMed  PubMed Central  Google Scholar 

  • Jakab F, Horváth G, Ferenczi E, Sebők J, Varecza Z, Szűcs G (2007) Detection of Dobrava hantaviruses in Apodemus agrarius mice in the Transdanubian region of Hungary. Virus Research 128:149-152 https://doi.org/10.1016/j.viruses.2007.04.015

    Article  PubMed  CAS  Google Scholar 

  • Jameson LJ, Logue CH, Atkinson, Baker N, Galbraith SE, Carroll MW, Brooks T Hewson R (2013) The continued emergence of hantaviruses: isolation of a Seoul virus implicated in human disease, United Kingdom, October 2012. Euro Surveillance 18(1):pii = 20344

  • Jiang JF, Zhang WY, Wu XM, Zhang PH, Cao WC (2007) Soochong virus and Amur virus might be the same entities of hantavirus. Journal of Medical Virology 79:1792-1795

    Article  PubMed  Google Scholar 

  • Jiang JF, Zuo SQ, Zhang WY, Wu XM, Tang F, De Vlas SJ, Zhao WJ, Zhang PH, Dun Z, Wang RM, Cao WC (2008) Prevalence and genetic diversities of hantaviruses in rodents in Beijing, China American Journal of Tropical Medicine and Hygiene 78(1):98-105

    Article  PubMed  CAS  Google Scholar 

  • Johansson P, Yap G, Low HT, Siew CC, Kek R, Ng LC, Bucht G (2010) Molecular characterization of two hantavirus strains from different Rattus species in Singapore. Virology Journal 7:15 https://doi.org/10.1186/1743-422x-7-15

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 238:115-27 https://doi.org/10.1006/viro.1997.8840

    Article  PubMed  CAS  Google Scholar 

  • Johnson AM, De Souza LTM, Ferreira IB, Pereira LE, Ksiazek TG, Rollin PE, Peters CJ, Nichol ST (1999) Genetic investigation of novel hantaviruses causing fatal HPS in Brazil. Journal of Medical Virology 59:527-535 https://doi.org/10.1002/(sici)1096-9071(199912)59:4<527::aid-jmv17>3.0.co;2-y

    Article  PubMed  CAS  Google Scholar 

  • Johnson PTJ, de Roode JC, Fenton A (2015) Why infectious disease research needs community ecology. Science 349(6252):1259504-1-9 https://doi.org/10.1126/science.1259504

  • Jones KE, Patel NG, Levy M a. (2008) Global trends in emerging infectious diseases. Nature 451:990–993 https://doi.org/10.1038/nature06536

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jonsson CB, Figueiredo LTM, Vapalahti O (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical Microbiology Reviews 23:412–441 https://doi.org/10.1128/cmr.00062-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang HJ, Bennett SN, Dizney L, Sumibcay L, Arai S, Ruedas L a., Song J-W, Yanagihara R (2009a) Host switch during evolution of a genetically distinct hantavirus in the American shrew mole (Neurotrichus gibbsii). Virology 388:8–14 https://doi.org/10.1016/j.virol.2009.03.019

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang HJ, Bennett SN, Sumibcay L, Arai S, Hope AG, Mocz G, Song JW, Cook JA, Yanagihara R (2009b) Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea). PLOS One 4:e6149 https://doi.org/10.1371/journal.pone.0006149

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang JK, Arai S, Hope AG, Song JW, Cook JA, Yanagihara R (2009c) Genetic diversity and phylogeography of Seewis virus in the Eurasian common shrew in Finland and Hungary. Virology Journal 6:208 https://doi.org/10.1186/1743-422x-6-208

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Arai S, Hope AG, Cook JA, Yanagihara R (2010) Novel hantavirus in the flat-skulled shrew (Sorex roboratus). Vector-Borne and Zoonotic Diseases 10:593–597 https://doi.org/10.1089/vbz.2009.0159

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Bennett SN, Hope AG, Cook JA, Yanagihara R (2011a) Shared ancestry between a newfound mole-borne hantavirus and hantavirus harbored by Cricetid rodents. Journal of Virology 85:7496-7503

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kang HJ, Kadjo B, Dubey S, Jacquet F, Yanagihara R (2011b) Molecular evolution of Azagny virus, a newfound hantavirus harbored by the West African pygmy shrew (Crocidura obscurior) in Côte d’Ivoire. Virology Journal 8:373 https://doi.org/10.1186/1743-422x-8-373

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang HJ, Kosoy MY, Shrestha SK, Shrestha MP, Pavlin JA, Gibbons RV, Yanagihara R (2011c) Short report: genetic diversity of Thottapalayam virus, a hantavirus harbored by the Asian house shrew (Suncus murinus) in Nepal. American Journal of Tropical Medicine and Hygiene 85(3):540-545 https://doi.org/10.4269/atmh.2011.11-0034

    Article  PubMed  PubMed Central  Google Scholar 

  • Karesh WB, Dobson A, Lloyd-Smith JO, Lubroth J, Dixon MA, Bennett M, Aldrich S, Harrington T, Formenty P, Loh EH, Machalaba CC, Thomas MJ, Heymann DL (2012) Ecology of zoonoses: natural and unnatural histories. Lancet 380:1936–1945 https://doi.org/10.1016/s0140-6736(12)61678-x

    Article  PubMed  Google Scholar 

  • Kariwa H, Yoshizumi S, Arikawa J, Yoshimatsu K, Takahashi K, Takashia I, Hashimoto N (1995) Evidence for the existence of Puumala-related virus among Clethrionomys rufocanus in Hokkaido, Japan. American Journal of Tropical Medicine and Hygiene 53:222-227

    Article  PubMed  CAS  Google Scholar 

  • Kariwa H, Yoshimatsu K, Sawabe J, Yokota E, Arikawa J, Takashima I, Fukushima H, Lundkvist Å, Shubin FN, Isachkova LM, Slonova RA, Leonova GN, Hashimoto N (1999) Genetic diversities of hantaviruses among rodents in Hokkaido, Japan and far east Russia. Virus Research 59:219-228

    Article  PubMed  CAS  Google Scholar 

  • Kariwa H, Yoshimatsu K, Arikawa J (2007) Hantavirus infection in East Asia. Comparative Immunology, Microbiology and Infectious Diseases 30:341-356 https://doi.org/10.1016/j.cimid.2007.05.011

    Article  PubMed  Google Scholar 

  • Kariwa H, Yoshida H, Sánchez-Hernández C, Romero-Almaraz MDL, Almazán-Catalán JA, Ramos C, Miyashita D, Seto T, Takano A, Totani M, Murata R, Saasa N, Ishizuka M, Sanada T, Yoshii K, Yoshimatsu K, Arikawa J, Takashima I (2012) Genetic diversity of hantaviruses in Mexico: identification of three novel hantaviruses from Neotominae rodents. Virus Research 163:486–494 https://doi.org/10.1016/j.virusres.2011.11.013

    Article  PubMed  CAS  Google Scholar 

  • Khan AS, Spiropoulou CF, Morzunov S, Zaki SR, Kohn MA, NAWAS SR (1995) Fatal illness associated with a new hantavirus in Louisiana. Journal of Medical Virology 46:281-286 https://doi.org/10.1002/jmv.1890460320

    Article  PubMed  CAS  Google Scholar 

  • Khan AS, Khabbaz RF, Armstrong LR, Holman RC, Bauer SP, Graber J, Strine T, Miller G, Reef S, Tappero J, Rollin PE, Nichol ST, Zaki SR, Bryan RT, Chapman LE, Peters CJ, Ksiazek TG (1996) Hantavirus pulmonary syndrome: the first 100 US cases. The Journal of Infectious Diseases 173:1297-1303

    Article  PubMed  CAS  Google Scholar 

  • King AMQ, Adams MJ, Carstens EB, Keftkowitz EJ (2012) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press http://ictvonline.org/

  • Klempa B (2009) Hantaviruses and climate change. Clinical Microbiology and Infection 15:518-23 https://doi.org/10.1111/j.1469-0691.2009.02848.x

    Article  PubMed  CAS  Google Scholar 

  • Klempa B, Meisel H, Räth S, Bartel J, Ulrich R, Krüger DH (2003a) Occurrence of renal and pulmonary syndrome in a region of northwest Germany where Tula hantavirus circulates. Journal of Clinical Microbiology 41(10):4894-4897 https://doi.org/10.1128/jcm.41.10.4894-1897.2003

    Article  PubMed  PubMed Central  Google Scholar 

  • Klempa B, Schmidt HA, Ulrich R, Kaluz S, Labuda M, Meisel H, Hjelle B, Krüger DH (2003b) Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature. Journal of Virology 77:804–809 https://doi.org/10.1128/jvi.77.1.804

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Denys C, Koivogui L, ter Meulen J, Krüger DH (2006) Hantavirus in African wood mouse, Guinea. Emerging Infectious Diseases 12:838-40 https://doi.org/10.3201/eid1205.051487

    Article  PubMed  PubMed Central  Google Scholar 

  • Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, Meisel H, Barrière P, Koivogui L, ter Meulen J, Krüger DH (2007) Novel hantavirus sequences in shrew, Guinea. Emerging Infectious Diseases 13:3-5 https://doi.org/10.3201/eid1303.061198

    Article  Google Scholar 

  • Klempa B, Tkachenko EA, Dzagurova TK, Yunivheva YV, Morozov VG, Okulova NM, Slyusareva GP, Smirnov A, Kruger DH (2008) Hemorrhagic fever with renal syndrome caused by 2 lineages of Dobrava hantavirus Russia. Emerging Infectious Diseases 14:617-625 https://doi.org/10.3201/eid1404.071310

    Article  PubMed  PubMed Central  Google Scholar 

  • Klempa B, Witkowski PT, Popugaeva E, Auste B, Koivogui L, Fichet-Calvet E, Strecker T, ter Meulen J, Kruger DH (2012) Sangassou Virus, the first hantavirus isolate from Africa, displays genetic and functional properties distinct from those of other Murinae-associated hantaviruses. Journal of Virology 86:3819-3827 https://doi.org/10.1128/jvi.05879-11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klempa B, Avsic-Zupanc T, Clement J, Dzagurova TK, Henttonen H, Heyman P, Jakab F, Kruger DH, Maes P, Papa A, Tzachenko EA, Ulrich RG, Vapalahti O, Vaheri A (2013) Complex evolution and epidemiology of Drobrava-Belgrade hantavirus: definition of genotypes and their characteristics. Archives of Virology 158:521-529 https://doi.org/10.1007/s00705-012-1514-5

    Article  PubMed  CAS  Google Scholar 

  • Knust B, Rollin PE (2013) Twenty-year summary of surveillance for human hantavirus infections, United States. Emerging Infectious Diseases 19:1934–1937 https://doi.org/10.3201/eid1912.131217

    Article  PubMed  PubMed Central  Google Scholar 

  • Krüger DH, Schonrich G, Klempa B (2011) Human pathogenic hantaviruses and prevention of infection. Human Vaccines 7:685-693

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kuenzi AJ, Douglass RJ, Bond CW (2000) Sin Nombre virus in deer mice captured inside homes, southwestern Montana. Emerging Infectious Diseases 6:386-388 https://doi.org/10.3201/eid0604.000411

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee HW, Lee PW, Johnson KM (1978) Isolation of the etiologic agent of Korean Hemorrhagic fever. Journal of Infectious Diseases 137:298-308 https://doi.org/10.1016/j.jviromet.2009.04.006

    Article  PubMed  CAS  Google Scholar 

  • Lee PW, Amyx HL, Gadjusek DC, Yanagihara RT, Goldgaber D, Gibbs CJ Jr (1982a) New haemorrhagic fever with renal syndrome-related virus in indigenous wild rodents in United States. Lancet 2:1405

  • Lee HW, Baek LJ, Johnson KM (1982b) Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. Journal of Infectious Diseases 146:638–644. https://doi.org/10.1093/infdis/146.5.638

  • Lee PW, Yanagihara R, Franko MC, Amyx HL, Gajdusek DC, Gibbs CJ Jr (1982c) Preliminary evidence that Hantaan or a closely related virus is enzootic in domestic rodents. The New England Journal of Medicine 307:624–625. https://doi.org/10.1056/nejm198209023071013

  • Lee PW, Amyx HL, Yanagihara R, Gajdusek DC, Goldgaber D, Gibbs CJ (1985) Partial characterization of Prospect Hill virus isolated from meadow voles in the United States. Journal of Infectious Diseases 152:826-829 https://doi.org/10.1093/infdis/152.4.826

    Article  PubMed  CAS  Google Scholar 

  • Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A (2004) The metacommunity concept: A framework for multi-scale community ecology. Ecology Letters 7:601-613 https://doi.org/10.1111/j.1461-0248.2004.00608.x

    Article  Google Scholar 

  • Levis S, Roew JE, Morzunov S, Enria DA, St Jeor S (1997) New hantaviruses causing hantavirus pulmonary syndrome in central Argentina. Lancet 349:998-999

    Article  PubMed  CAS  Google Scholar 

  • Levis S, Morzunov SP, Rowe JE, Enria D, Pini N, Calderon G, Sabattini M, St Jeor SC (1998) Genetic diversity and epidemiology of hantaviruses in Argentina. Journal of Infectious Diseases 177:529–538 https://doi.org/10.1086/514221

    Article  PubMed  CAS  Google Scholar 

  • 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. American Journal of Tropical Medicine and Hygiene 71(5):658-663

    Article  PubMed  CAS  Google Scholar 

  • Li J, Zhao ZT, Wang ZQ, Liu YX, Hu MH (2007) Nucleotide sequence characterization and phylogenetic analysis of hantaviruses isolated in Shandong Province, China. Chinese Medical Journal 120(9):825-830

    PubMed  CAS  Google Scholar 

  • Lin XD, Zhou RH, Fan FN, Ying XH, Sun XY, Wang W, Holmes EC, Zhang YZ (2014) Biodiversity and evolution of Imjin virus and Thottapalayam virus in Crocidurinae shrews in Zhejiang Province, China. Virus Research 189:114-120 https://doi.org/10.1016/j.viruses.2014.05.014

    Article  PubMed  Google Scholar 

  • Liu J, Liu DY, Chen W, Li JL, Luo F, Li Q, Ling JX, Liu YY, Xiong HR, Ding XH, Hou W, Zhang Y, Li SY, Wang J, Yang ZQ (2012) Genetic analysis of hantaviruses and their rodent hosts in central-south China. Virus Research 163:439-447 https://doi.org/10.1016/j.virusres.2011.11.006

    Article  PubMed  CAS  Google Scholar 

  • Londoño AF, Díaz FJ, Agudelo-Flórez P, Levis S, Rodas JD (2011) Genetic evidence of hantavirus infections in wild rodents from northwestern Colombia. Vector-Borne and Zoonotic Diseases 11:701–708 https://doi.org/10.1089/vbz.2010.0129

    Article  PubMed  Google Scholar 

  • Longdon B, Brockhurst MA, Russel CA, Welch JJ, Jiggins FM (2014) The evolution and genetics of virus host shifts. PLOS Pathogens 10(11):e1004395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lonner BN, Douglass RJ, Kuenzi AJ, Hughes K (2008) Seroprevalence against Sin Nombre virus in resident and dispersing deer mice. Vector-Borne and Zoonotic Diseases 8:433-442 https://doi.org/10.1089/vbz.2007.0232

    Article  PubMed  PubMed Central  Google Scholar 

  • López N, Padula P, ROSSI C, Lázaro ME, Franze-Fernández MT (1996) Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220:223-226

    Article  PubMed  Google Scholar 

  • Luan VD, Yoshimatsu K, Endo R, Taruishi M, Huong VT, Dat DT, Tien PC, Shimizu K, Koma T, Yasuda SP, Nhi L, Huong VTQ, Arikawa J (2012) Studies on hantavirus infection in small mammals captured in southern and central highland area of Vietnam. Journal of Veterinary Medical Science 74(9):1155-1162 https://doi.org/10.1292/jvms.11-0567

    Article  PubMed  Google Scholar 

  • Luis AD, Douglass RJ, Mills JN, Bjørnstad ON (2010) The effect of seasonality, density and climate on the population dynamics of Montana deer mice, important reservoir hosts for Sin Nombre hantavirus. Journal of Animal Ecology 79:462–470 https://doi.org/10.1111/j.1365-2656.2009.01646.x

    Article  PubMed  Google Scholar 

  • Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B 280:20122753. https://doi.org/10.1098/rspb.2012.2753

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 https://doi.org/10.1111/ele.12491

    Article  PubMed  PubMed Central  Google Scholar 

  • Lundkvist Å, Wiger D, Hörling J, Sjölander KB, Plyusnina A, Mehl R, Vaheri A, Plusnin A (1998) Isolation and characterization of Puumala hantavirus from Norway: evidence for a distinct phylogenetic sublineage. Journal of General Virology 79:2603-2614

    Article  PubMed  CAS  Google Scholar 

  • Lundkvist Å, Verner-Carlsson J, Plyusnina a., Forslund L, Feinstein R, Plyusnin A (2013) Pet rat harbouring Seoul hantavirus in Sweden, June 2013. Eurosurveillance 18:1-4 https://doi.org/10.2807/1560-7917.es2013.18.27.20521

    Article  Google Scholar 

  • Madhav NK, Wagoner KD, Douglass RJ, Mills JN (2007) Delayed density-dependent prevalence of Sin Nombre virus antibody in Montana deer mice (Peromyscus maniculatus) and implications for human disease risk. Vector-Borne and Zoonotic Diseases 7:353-364 https://doi.org/10.1089/vbz.2006.0605

    Article  PubMed  Google Scholar 

  • Mantooth SJ, Milazzo ML, Bradley RD, Hice CL, Ceballos G, Tesh RB, Fulhorst CF (2001) Geographical distribution of rodent-associated hantaviruses in Texas. Journal of Vector Ecology 26:7-14

    PubMed  CAS  Google Scholar 

  • Medina R, Torres-Perez F, Galeno H, Navarrete M, Vial P, Palma R, Ferres M, Cook J, Hjelle B (2009) Ecology, genetic diversity, and phylogeographic structure of Andes virus in humans and rodents in Chile. Journal of Virology 83(6):2446–2459. https://doi.org/10.1128/JVI.01057-08

    Article  PubMed  CAS  Google Scholar 

  • Meerburg BG, Singleton GR, Kijlstra A (2009) Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology 35(3):221-270

    Article  PubMed  Google Scholar 

  • Meheretu Y, Cížková D, Těšíková J, Welegerima K, Tomas Z, Kidane D, Girmay K, Schmidt-Chanasit J, Bryja J, Günther S, Bryjová A, Leirs H, Goüy de Bellocq J (2012) High diversity of RNA viruses in rodents, Ethiopia. Emerging Infectious Diseases 18:2047-50 https://doi.org/10.3201/eid1812.120596

    Article  PubMed  PubMed Central  Google Scholar 

  • Meissner JD, Rowe JE, Borucki MK, St. Jeor SC (2002) Complete nucleotide sequence of a Chilean hantavirus. Virus Research 89:131-143

    Article  PubMed  CAS  Google Scholar 

  • Milazzo ML, Cajimat MN, Hanson JD, Bradley RD, Quintana M, Sherman C, Velasquez RT, Fulhorst CF (2006) Catacamas virus, a hantaviral species naturally associated with Oryzomys couesi (Coues’ Oryzomys) in Honduras. American Journal of Tropical Medicine and Hygiene 75:1003-1010

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milazzo ML, Duno G, Utrera A, Richter MH, Duno F, de Manzione N, Fulhorst CF (2010) Natural host relationships of hantaviruses native to western Venezuela. Vector-Borne and Zoonotic Diseases 10(6):605-611 https://doi.org/10.1089/vbz.2009.0118

    Article  PubMed  PubMed Central  Google Scholar 

  • Milazzo ML, Cajimat MNB, Romo HE, Estrada-Franco JG, Ignacio Iñiguez-Dávalos L, Bradley RD, Fulhorst CF (2012) Geographic distribution of hantaviruses associated with neotomine and sigmodontine rodents, Mexico. Emerging Infectious Diseases 18:571–576 https://doi.org/10.3201/eid1804.111028

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Milholland MT, Castro-Arellano I, Arellano E, Nava-García E, Rangel-Altamirano G, Gonzalez-Cozatl FX, Suzán G, Schountz, T, González-Padrón S, Vigueras A, Rubio AV, Maikis TJ, Westrich BJ, Martinez III JA, Esteve-Gassent MD, Torres MB, Rodriguez-Ruiz ER, Hahn D, Lacher Jr TE (2018) Species identity supersedes the dilution effect concerning hantavirus prevalence at sites across Texas and México. ILAR Journal 58(3):401–412

    Article  Google Scholar 

  • Mills JN, Childs JE (1998) Ecologic studies of rodent reservoirs: their relevance for human health. Emerging Infectious Diseases 4:529–537. https://doi.org/10.3201/eid0404.980403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mills JN, Ksiazek TG, Ellis BA, Rollin PE, Nichol ST, Yates TL, Gannon WL, Levy CE, Engelthaler DM, Davis TED, Tanda D, Frampton JW, Nichols CR, Peters CJ, Childs JE (1997) Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. American Journal of Tropical Medicine and Hygiene 56:273–284

    Article  PubMed  CAS  Google Scholar 

  • Mills JN, Amman BR, Glass GE (2010) Ecology of hantaviruses and their hosts in North America. Vector-Borne and Zoonotic Diseases 10:563-574 https://doi.org/10.1089/vbz.2009.0018

    Article  PubMed  Google Scholar 

  • Morand S, Jittapalapong S, Kosoy M (2015) Rodents as hosts of infectious diseases: biological and ecological characteristics. Vector-Borne and Zoonotic Diseases 15(1):1-2 https://doi.org/10.1089/vbz.2015.15.1.intro

    Article  PubMed  PubMed Central  Google Scholar 

  • Morzunov SP, Feldmann H, Spiropoulou CF, Semenova VA, Rollin PE, Ksiazek TG, Peters CJ, Nichol ST (1995) A newly recognized virus associated with a fatal case of hantavirus pulmonary syndrome in Louisiana. Journal of Virology 69:1980-1983

    PubMed  PubMed Central  CAS  Google Scholar 

  • Morzunov SP, Rowe JE, Ksiazek TG, Peters CJ, St Jeor SC, Nichol ST (1998) Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. Journal of Virology 72:57–64

    PubMed  PubMed Central  CAS  Google Scholar 

  • Muranyi W, Bahr U, Zeier M, van der Woude FJ (2005) Hantavirus infection. Journal of the American Society of Nephrology 16:3669-3679 https://doi.org/10.1681/asn.2005050561

    Article  PubMed  CAS  Google Scholar 

  • Nemirov K, Vapalahti O, Lundkvist Å, Vasilenko V, Golovljova I, Plyusnina A, Niemimaa J, Laakkonen J, Henttonen H, Vaheri A, Plyusnin A (1999) Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. Journal of General Virology 80:371–379

    Article  PubMed  CAS  Google Scholar 

  • Nisbett RA, Caire W, Stuart MD, Caddell GM, Crutcher JM, Calisher CH (2001) Serologic survey of Oklahoma rodents: evidence for the presence of a hantavirus and an arenavirus. Proceedings of the Oklahoma Academy of Science 81:53–66

    Google Scholar 

  • Olsson GE, Dalerum F, Hörnfeldt B, Elgh F, Palo TR, Juto P, Ahlm C (2003) Human hantavirus infections, Sweden. Emerging Infectious Diseases 9:1395-1401

    Article  PubMed  PubMed Central  Google Scholar 

  • Olsson GE, Leirs H, Henttonen H (2010) Hantaviruses and their hosts in Europe: reservoirs here and there, but not everywhere? Vector-Borne and Zoonotic Diseases 10:549–561 https://doi.org/10.1089/vbz.2009.0138

    Article  PubMed  Google Scholar 

  • Padula P, Martinez VP, Bellomo C, Maidana S, San Juan J, Tagliaferri P, Bargardi S, Vazquez C, Colucci N, Estévez J, Almiron M (2007) Pathogenic hantaviruses, northeastern Argentina and eastern Paraguay. Emerging Infectious Diseases 13:1211-1214 https://doi.org/10.3201/eid1308.061090

    Article  PubMed  PubMed Central  Google Scholar 

  • Pettersson L, Boman J, Juto P, Evander M, Ahlm C (2008) Outbreak of Puumala virus infection, Sweden. Emerging Infectious Diseases 14:808-810 https://doi.org/10.3201/eid1405.071124

    Article  PubMed  PubMed Central  Google Scholar 

  • Plyusnin A, Vapalahti O, Lankinen H, Lehväslaiho H, Apekina N, Myasnikov Y, Kallio-Kokko H, Henttonen H, Lundkvist Å, Brummer-Korvenkontio M (1994) Tula virus: a newly detected hantavirus carried by European common voles. Journal of Virology 68:7833–7839

    PubMed  PubMed Central  CAS  Google Scholar 

  • Plyusnin A, Cheng Y, Vapalahti O, Pejcoch M, Unar J, Jelinkova Z, Lehväslaiho H, Lundkvist Å (1995) Genetic variation in Tula hantaviruses: sequence analysis of the s and m segments of strains from central Europe. Virus Research 39:237-250

    Article  PubMed  CAS  Google Scholar 

  • Plyusnin A, Hörling J, Kanerva M, Mustonen J, Cheng Y, Partanen J, Vapalahti O, Kukkonen SK, Niemimaa J, Henttonen H, Niklasson B, Lundkvist Å, Vaheri A (1997) Puumala hantavirus genome in patients with nephropathia epidemica: correlation of PCR positivity with HLA haplotype and link to viral sequences in local rodents. Journal of Clinical Microbiology 35:1090–6

    PubMed  PubMed Central  CAS  Google Scholar 

  • Plyusnin A, Vaheri A, Lundkvist Å (2003) Genetic interactions between Dobrava and Saaremaa hantaviruses: now or millions of years ago? Journal of Virology 77:7156-7158 https://doi.org/10.1128/jvi.77.12.7156-7158.2003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plyusnin A, Vaheri A, Lundkvist Å (2006) Saaremaa hantavirus should not be confused with its dangerous relative, Dobrava virus. Journal of Clinical Microbiology 44(4):1608-1611 https://doi.org/10.1128/jcm.44.4.1608-1611.2006

    Article  PubMed  PubMed Central  Google Scholar 

  • Plyusnin A, Sironen T (2014) Evolution of hantaviruses: co-speciation with reservoir hosts for more than 100MYR. Virus Research 187:22–26 https://doi.org/10.1016/j.virusres.2014.01.008

    Article  PubMed  CAS  Google Scholar 

  • Plyusnina A, Ibrahim IN, Winoto I, Porter KR, Gotama IBI, Lundkvist Å, Vaheri A, Plyusnin A (2004) Identification of Seoul hantavirus in Rattus norvegicus in Indonesia. Scandinavian Journal of Infectious Diseases 36:356-359 https://doi.org/10.1080/00365540410019264

    Article  PubMed  CAS  Google Scholar 

  • Plyusnina A, Laakkonen J, Niemimmaa J, Henttonen H, Plyusnin A (2008a) New genetic lineage of Tula hantavirus in Microtus arvalis obscurus in eastern Kazakhstan. The Open Virology Journal 2:32-36

  • Plyusnina A, Laakkonen J, Niemimaa J, Nemirov K, Muruyeva G, Pohodiev B, Lundkvist Å, Vaheri A, Henttonen H, Vapalahti O, Plyusnin A (2008b) Genetic analysis of hantaviruses carried by Myodes and Microtus rodents in Buryatia. Virology Journal 5:4. https://doi.org/10.1186/1743-422X-5-4

  • Plyusnina A, Ferenczi E, Rácz GR, Nemirov K, Lundkvist Å, Vaheri A, Vapalahti O, Plyusnin A (2009a) Co-circulation of three pathogenic hantaviruses: Puumala, Dobrava, and Saaremaa in Hungary. Journal of Medical Virology 81:2045-2052. https://doi.org/10.1002/jmv.21635

  • Plyusnina A, Ibrahim IN, Plyusnin A. (2009b) A newly recognized hantavirus in the Asian house rat (Rattus tanezumi) in Indonesia. Journal of General Virology 90:205–209. https://doi.org/10.1099/vir.0.006155-0

  • Powers AM, Mercer DR, Watts DM, Guzman H, Fulhorst CF, Popov VL, Tesh RB (1999) Isolation and genetic characterization of a hantavirus (Bunyaviridae: Hantavirus) from a rodent, Oligoryzomys microtis (Muridae), collected in northeastern Peru. American Journal of Tropical Medicine and Hygiene 61:92–98.

    Article  PubMed  CAS  Google Scholar 

  • Raboni SM, Probst CM, Bordignon J, Zeferino A, dos Santos CND (2005) Hantaviruses in central South America: phylogenetic analysis of the s segment from HPS cases in Paraná, Brazil. Journal of Medical Virology 76:553–562 https://doi.org/10.1002/jmv.20398

    Article  PubMed  CAS  Google Scholar 

  • Raboni SM, Hoffmann FG, Oliveira RC, Teixeira BR, Bonvicino CR, Stella V, Cartensen S, Bordignon J, D’Andrea PS, Lemos ERS, Duarte dos Santos CN (2009) Phylogenetic characterization of hantaviruses from wild rodents and hantaviruses pulmonary syndrome cases in the state of Paraná. General Journal of Virology 90:2166-2171 https://doi.org/10.1099/vir.0.011585-0

    Article  CAS  Google Scholar 

  • Raboni SM, Delfraro A, de Borba L, Teixeira BR, Stella V, de Araujo MR, Carstensen S, Rubio G, Maron A, Lemos ERS, 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. American Journal of Tropical Medicine and Hygiene 87(2):371-378 https://doi.org/10.4269/ajtmh.2012.11-0762

    Article  PubMed  PubMed Central  Google Scholar 

  • Radosa L, Schlegel M, Gerbauer P, Ansorge H, Heroldová M, Jánová E, Stanko M, Mošanky L, Fričová J, Pejčoch M, Suchomel J, Purchart L, Groschup MH, Krüger DH, Ulrich RG, Klempa B (2013) Detection of shrew-borne hantavirus in Eurasian pygmy shrew (Sorex minutus) in central Europe. Infection, Genetics and Evolution https://doi.org/10.1016/j.meegid.2013.04.008

    Article  PubMed  Google Scholar 

  • Ramsden C, Holmes EC, Charleston MA (2009) Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Molecular Biology and Evolution 26:143–153 https://doi.org/10.1093/molbev/msn234

    Article  PubMed  CAS  Google Scholar 

  • Ravkov EV, Rollin PE, Ksiazek TG, Peters CJ, Nichol ST (1995) Genetic and serologic analysis of Black Creek Canal virus and its association with human disease and Sigmodon hispidus infection. Virology 210:482-489

    Article  PubMed  CAS  Google Scholar 

  • Rawlings JA, Torrez-Martinez N, Neill SU, Moore GM, Hicks BN, Pichuantes S, Nguyen A, Bharadwaj M, Hjelle B (1996) Cocirculation of multiple hantaviruses in Texas, with characterization of the small (s) genome of a previously undescribed virus of cotton rats (Sigmodon hispidus). American Journal of Tropical Medicine and Hygiene 55:672-679

    Article  PubMed  CAS  Google Scholar 

  • Razuri H, Tokarz R, Ghersi BM, Salmon-Mulanovich G, Guezala MC, Albujar C, Mendoza AP, Tinoco YO, Cruz C, Silva M, Vasquez A, Pacheco V, Stöher U, Guerrero LW, Cannon D, Nichol ST, Hirschberg DL, Lipkin WI, Bausch DG, Montgomery JM (2014) Andes hantavirus variant in rodents, southern Amazon Basin, Peru. Emerging Infectious Diseases 20(2):257-260 https://doi.org/10.3201/eid2002.131418

    Article  PubMed  PubMed Central  Google Scholar 

  • Razzauti M, Plyusnina A, Sironen T, Henttonen H, Plyusnin A (2009) Analysis of Puumala hantavirus in a bank vole population in northern Finland: evidence for co-circulation of two genetic lineages and frequent reassortment between strains. Journal of General Virology 90:1923-1931

    Article  PubMed  CAS  Google Scholar 

  • Reusken C, de Vries A, Adema J, Vos W, van der Giessen J, Bekker D, Heyman P (2008) First detection of Tula hantavirus in wild rodents in the Netherlands. Journal of Infection 57(6):500-503 https://doi.org/10.1016/j.jinf.2008.09.032

    Article  PubMed  Google Scholar 

  • Reusken C, Heyman P (2013) Factors driving hantavirus emergence in Europe. Current Opinion in Virology 3:92-99 https://doi.org/10.1016/j.coviro.2013.01.002

    Article  PubMed  Google Scholar 

  • Reynes JM, Soares JL, Hüe T, Bouloy M, Sun S, Kruy SL, Flye Sainte Marie F, Zeller H (2003) Evidence of the presence of Seoul virus in Cambodia. Microbes and Infection 5:769–773 https://doi.org/10.1016/s1286-4579(03)00149-7

    Article  PubMed  Google Scholar 

  • Reynes JM, Razafindralambo NK, Lacoste V, Olive MM, Barivelo TA, Soarimalala V, Heraud JM, Lavergne A (2014) Anjozorobe Hantavirus, a new genetic variant of Thailand virus detected in rodents from Madagascar. Vector-Borne and Zoonotic Diseases 14:212–219 https://doi.org/10.1089/vbz.2013.1359

    Article  PubMed  PubMed Central  Google Scholar 

  • Rico-Chávez O, Ojeda Flores R, Sotomayor Bonilla J, Zambrana-Torrelio C, Loza Rubio E, Alonso Aguirre A, Suzán G (2015) Viral diversity of bat communities in human-dominated landscapes in Mexico. Veterinaria México OA 2(1):1-22

    Article  Google Scholar 

  • Rocha RG, Ferreira E, Costa BMA, Martins ICM, Leite YLR, Costa LP, Fonseca C (2011) Small mammals of the mid-Araguaia River in central Brazil, with the description of a new species of climbing rat. Zootaxa 2789:1-34

    Google Scholar 

  • Rhodes LV III, Huang C, Sanchez AJ, Nichol ST, Zaki SR, Ksiazek TG, Humphreys JG, Freeman JJ, Knecht KR (2000) Hantavirus pulmonary syndrome associated with Monongahela virus, Pennsylvania. Emerging Infectious Diseases 6:616–621. https://doi.org/10.3201/eid0606.000610

    Article  PubMed  PubMed Central  Google Scholar 

  • Rollin PE, Ksiazek TG, Elliot LH, Ravkov EV, Martin ML, Morzunov S, Livingstone W, Monroe M, Glass G, Ruo S, Khan AS, Childs JE, Nichol S, Peters CJ (1995) Isolation of Black Creek Canal virus, a new hantavirus from Sigmodon hispidus in Florida. Journal of Medical Virology 46:35-39

    Article  PubMed  CAS  Google Scholar 

  • Rosa EST, Mills JN, Padula PJ, Elkhoury MR, Ksiazek TG, Mendes WS, Santos ED, Araújo GCB, Martinez VP, Rosa JFST, Edelstein A, Vasconcelos PFC (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 and Zoonotic Diseases 5:11–9 https://doi.org/10.1089/vbz.2005.5.11

    Article  PubMed  Google Scholar 

  • Rowe JE, St. Jeor SC, Riolo J, Ottenson EW, Monroe MC, Henderson WW, Ksiazek TG, Rollin PE, Nichol ST (1995) Coexistence of several novel hantaviruses in rodents indigenous to North America. Virology 213:122-130

    Article  PubMed  CAS  Google Scholar 

  • Saasa N, Sánchez-Hernández C, Romero-Almaraz MDL, Guerrero-Ibarra E, Almazán-Catalán A, Yoshida H, Miyashita D, Ishizuka M, Sanada T, Seto T, Yoshii K, Ramos C, Yoshimatsu K, Arikawa J, Takashima I, Kariwa H (2012) Ecology of hantaviruses in Mexico: genetic identification of rodent host species and spillover infection. Virus Research 168:88-96 https://doi.org/10.1016/j.virusres.2012.06.020

    Article  PubMed  CAS  Google Scholar 

  • Safi K, Cianciaruso MV, Loyola RD, Brito D, Armour-Marshall K, Diniz-Filho JAF (2011) Understanding global patterns of mammalian functional and phylogenetic diversity. Philosophical Transactions of the Royal Society Biological Sciences 366:2536-2544 https://doi.org/10.1098/rstb.2011.0024

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. Journal of Wildlife Diseases 40:103–109

    Article  PubMed  Google Scholar 

  • Sanchez AJ, Abbott KD, Nichol ST (2001) Genetic identification and characterization of Limestone Canyon virus, a unique Peromyscus-Borne hantavirus. Virology 286:345–353. https://doi.org/10.1006/viro.2001.0983

    Article  PubMed  CAS  Google Scholar 

  • Scharninghausen JJ, Pfeffer, Meyer H, Davis DS, Honeycutt RL, Faulde M (2002) Genetic evidence for Tula virus in Microtus arvalis and Microtus agrestis populations in Croatia. Vector-Borne and Zoonotic Diseases 2:19-27 https://doi.org/10.1089/153036602760260742

    Article  PubMed  Google Scholar 

  • Schilling S, Emmerich P, Klempa B, Auste B, Schnaith E, Schmitz H, Krüger DH, Günther S, Meisel H (2007) Hantavirus disease outbreak in Germany: limitations of routine serological diagnostics and clustering of virus sequences of human and rodent origin. Journal of Clinical Microbiology 45(9):3008-3014 https://doi.org/10.1128/jcm.02573-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schlegel M, Klempa B, Auste B, Bemmann M, Schmidt-Chanasit J, Büchner T, Groschup MH, Meier M, Balkema-Buschmann B, Zoller H, Krüger DH, Ulrich RG (2009) Dobrava-Belgrade virus spillover infections, Germany. Emerging Infectious Diseases 15(12):2017-2020 https://doi.org/10.3201/eid1512.090923

    Article  PubMed  Google Scholar 

  • Schlegel M, Radosa L, Rosenfeld UM, Schmidt S, Triebacher C, Löhr PW, Fuchs D, Heroldová M, Jánová E, Stanko M, Mošanský L, Fričová J, Pejčoch M, Suchomel J, Purchart L, Groschup MH, Krüger DH, Klempa B, Ulrich RG (2012) Broad geographical distribution and high genetic diversity of shrew-borne Seewis hantavirus in central Europe. Virus Genes 45:48-55 https://doi.org/10.1007/s11262-012-0736-7

    Article  PubMed  CAS  Google Scholar 

  • Schlegel M, Jacob J, Krüger DH, Rang A, Ulrich RG (2014) Hantavirus emergence in rodents, insectivores and bats what comes next? Pp. 235-292 In: The role of animals in emerging viral diseases https://doi.org/10.1016/b978-0-12-405191.00010-7

  • Schmaljohn AL, Li D, Negley DL, Bressler DS, Turell MJ, Korch GW, Ascher MS, Schmaljohn CS (1995) Isolation and initial characterization of a newfound hantavirus from California. Virology 206:963-972

    Article  PubMed  CAS  Google Scholar 

  • Schmidt S, Essbauer SS, Mayer-Scholl A, Poppert S, Schmidt-Chanasit J, Klempa B, Henning K, Schares G, Groschup MH, Spitzenberger F, Richter D, Heckel G, Ulrich RG (2014) Multiple infections of rodents with zoonotic pathogens in Austria. Vector-Borne and Zoonotic Diseases 14(7):1-9 https://doi.org/10.1089/vbz.2013.1504

    Article  CAS  Google Scholar 

  • Schmidt-Chanasit J, Essbauer S, Petraityte R, Yoshimatsu K, Tackman K, Conraths FJ, Sasnauskas K, Arikawa J, Thomas A, Pfeffer M, Scharninghausen JJ, Splettstoesser W, Wenk M, Heckel, Ulrich RG (2010) Extensive host sharing of central European Tula virus. Journal of Virology 84(1):459-474 https://doi.org/10.1128/jvi.01226-09

    Article  PubMed  CAS  Google Scholar 

  • Semenza JC, Menne B (2009) Climate change and infectious diseases in Europe. Lancet Infectious Diseases 9:365-375 https://doi.org/10.1016/s1473-3099(09)70104-5

    Article  PubMed  Google Scholar 

  • Sibold C, Sparr S, Schulz A, Labuda M, Kozuch O, Lysý J, Krüger DH, Meisel H (1995) Genetic characterization of a new hantavirus detected in Microtus arvalis from Slovakia. Virus Genes 10(3):277-281

    Article  PubMed  CAS  Google Scholar 

  • Sinclair JR, Carroll DS, Montgomery JM, Pavlin B, McCombs K, Mills JN, Comer JA, Ksiazek TG, Rollin PE, Nichol ST, Sanchez AJ, Hutson CL, Bell M, Rooney JA (2007) Two cases of hantavirus pulmonary syndrome in Randolph County, West Virginia: a coincidence of time and place? American Journal of Tropical Medicine and Hygiene 76:438–42

    Article  PubMed  Google Scholar 

  • Sironen T, Vaheri A, Plyusnin A (2005) Phylogenetic evidence for the distinction of Saaremaa and Dobrava hantaviruses. Virology Journal 2:90 https://doi.org/10.1186/1743-422x-2-90

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Song W, Torrez-Martinez N, Irwin W, Harrison FJ, Davis R, Ascher M, Jay M, Hjelle B (1995) Isla Vista virus: a genetically novel hantavirus of the California vole Microtus californicus. Journal of General Virology 76:3195-3199 https://doi.org/10.1099/0022-1317-76-12-3195

    Article  PubMed  CAS  Google Scholar 

  • Song JW, Baek LJ, Nagle JW, Schlitter D, YANAGIHARA R (1996) Genetic and phylogenetic analyses of hantaviral sequences amplified from archival tissues of deer mice (Peromyscus maniculatus nubiterrae) captured in the eastern United States. Archives of Virology 141:959-967

    Article  PubMed  CAS  Google Scholar 

  • Song JW, Gligic A, Yanagihara R (2002) Identification of Tula hantavirus in Pitymys subterraneus captured in the Cacak region of Serbia-Yugoslavia. International Journal of Infectious Diseases 6:31-36

    Article  PubMed  Google Scholar 

  • Song JW, Baek LJ, Song KJ, Skrok A, Markowski J, Bratosiewicz-Wasik J, Kordek R, Liberski PP, Yanagihara R (2004) Characterization of Tula virus from common voles (Microtus arvalis) in Poland: evidence for geographic-specific phylogenetic clustering. Virus Genes 29(2):239-247

    Article  PubMed  CAS  Google Scholar 

  • Song KJ, Baek LJ, Moon S, Ha SJ, Kim SH, Park KS, Klein TA, Sames W, Kim HCC, Lee JS, Yanagihara R, Song J-W (2007a) Muju virus, a novel hantavirus harboured by the arvicolid rodent Myodes regulus in Korea. Journal of General Virology 88:3121-3129. https://doi.org/10.1099/vir.0.83139-0

  • Song JW, Gu SH, Bennett SN, Arai S, Puorger M, Hilbe M, Yanagihara R (2007b) Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew (Sorex araneus). Virology Journal 4:114. https://doi.org/10.1186/1743-422x-4-114

  • Song JW, Hae JK, Song KJ, Truong TT, Bennett SN, Arai S, Truong NU, Yanagihara R (2007c) Newfound hantavirus in Chinese mole shrew, Vietnam. Emerging Infectious Diseases 13:1784-1787. https://doi.org/10.3201/eid1311.070492

  • Song JW, Kang HJ, Gu SH, Moon SS, Bennett SN, Song KJ, Baek LJ, Kim HC, O’Guinn ML, Chong ST, Klein TA, Yanagihara R (2009) Characterization of Imjin Virus, a newly isolated hantavirus from the Ussuri white-toothed shrew (Crocidura lasiura). Journal of Virology 83:6184-6191 https://doi.org/10.1128/jvi.00371-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Steffen W, Rockström J, Costanza R (2011) How defining planetary boundaries can transform our approach to growth. Solutions 2:59-65

    Google Scholar 

  • Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE (2010) Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 329:676-679 https://doi.org/10.1126/science.1188836

    Article  PubMed  CAS  Google Scholar 

  • Sumibcay L, Kadjo B, Gu SH, Kang HJ, Lim BK, Cook JA, Song JW, Yanagihara R (2012) Divergent lineage of a novel hantavirus in the banana pipistrelle (Neoromicia nanus) in Côte d’Ivoire. Virology Journal 9:34 https://doi.org/10.1186/1743-422x-9-34

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzán G, García-Peña GE, Castro-Arellano I, Rico O, Rubio AV, Tolsá MJ, Roche B, Hosseini PR, Rizzoli A, Murray KA, Zambrana-Torrelio C, Vittecoq M, Bailly X, Aguirre AA, Daszak P, Prieur-Richard AH, Mills JN, Guégan JF (2015) Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Ecology and Evolution 5:865-873 https://doi.org/10.1002/ece3.1404

    Article  PubMed  PubMed Central  Google Scholar 

  • Suzuki A, Bisordi I, Levis S, Garcia J, Pereira LE, Souza RP, Sugahara TKN, Pini N, Enria D, Souza LTM (2004) Identifying rodent hantavirus reservoirs, Brazil. Emerging Infectious Diseases 10:2127-34 https://doi.org/10.3201/eid1012.040295

    Article  PubMed  PubMed Central  Google Scholar 

  • Tatem A, Rogers D (2006) Global transport networks and infectious disease spread. Advances in Parasitology 62:293-343 https://doi.org/10.1016/s0065-308x(05)62009-x.global

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease. Philosophical Transactions:The Royal Society Biological Sciences 356:983-989

    Article  CAS  Google Scholar 

  • Torrez-Martinez N, Bharadwaj M, Goade D, Delury J, Moran P, Hicks B, Nix B, Davis JL, Hjelle B (1998) Bayou virus-associated hantavirus pulmonary syndrome in eastern Texas: identification of the rice rat, Oryzomys palustris, as reservoir host. Emerging Infectious Diseases 4(1):105-111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Travassos da Rosa ES, Medeiros DBA, Nunes MRT, Simith DB, Pereira ADS, Elkhoury MR, Santos ED, Lavocat M, Marques AA, Via AVG, Kohl VA, Terças ACP, D’Andrea P, Bonvícino CR, Sampaio de Lemos ER, Vasconcelos PFC (2012) Molecular epidemiology of Laguna Negra virus, Mato Grosso State, Brazil. Emerging Infectious Diseases 18(6):982-985 https://doi.org/10.3201/eid1806.110948

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsai TF, Bauer SP, Sasso DR, Whitfield SG, McCormick JB, Caraway TC, McFarland L, Bradford H, Kurata T (1985) Serological and virological evidence of a Hantaan virus-related enzootic in the United States. Journal of Infectious Diseases 152:126-36 https://doi.org/10.1093/infdis/152.1.126

    Article  PubMed  CAS  Google Scholar 

  • Turell MJ, Korch GW, Rossi CA, Sesline D, Enge BA, Dondero DV, Jay M, Ludwig GV, Li D, Schmaljohn CS, Jackson RJ, Ascher MS (1995) Short report: prevalence of hantavirus infection in rodents associated with two fatal human infections in California. American Journal of Tropical Medicine and Hygiene 52(2):180-182

    Article  PubMed  CAS  Google Scholar 

  • Vadell MV, Bellomo C, San Martin A, Padula P, Gómez Villafañe I (2011) Hantavirus ecology in rodent populations in three protected areas of Argentina. Tropical Medicine and International Health 16(10):1342-1352 https://doi.org/10.1111/j.1365-3156.2011.02838.x

    Article  PubMed  CAS  Google Scholar 

  • Vaheri A, Strandin T, Hepojoki J, Sironen T, Henttonen H, Mäkelä S, Mustonen J (2013) Uncovering the mysteries of hantavirus infections. Nature Reviews Microbiology 11:539-550

    Article  PubMed  CAS  Google Scholar 

  • Vahlenkamp M, Müller T, Tackman K, Löschner U, Schmitz H, Schreiber M (1998) The muskrat (Ondatra zibethicus) as a new reservoir for Puumala-like hantavirus strains in Europe. Virus Research 57:139-150

    Article  PubMed  CAS  Google Scholar 

  • Vapalahti O, Lundkvist Å, Fedorov V, Conroy CJ, Hirvonen S, Plyusnina a, Nemirov K, Fredga K, Cook JA, Niemimaa J, Kaikusalo A, Henttonen H, Vaheri A, Plyusnin A (1999) Isolation and characterization of a hantavirus from Lemmus sibiricus: evidence for host switch during hantavirus evolution. Journal of Virology 73:5586–5592

    PubMed  PubMed Central  CAS  Google Scholar 

  • Vasconcelos MI, Lima VP, Iversson LB, Rosa MDB, Travassos da Rosa APA, Travassos da Rosa ES, Pereira LE, Nassar E, Katz G, Matida LH, Zaparoli MA, Ferreira JJ, Peters CJ (1997) Hantavirus pulmonary syndrome in the rural area of Juquitiba, São Paulo metropolitan area, Brazil. Revista Do Instituto De Medicina Tropical De São Paulo 39:237-238 https://doi.org/10.1590/s0036-46651997000400012

    Article  PubMed  CAS  Google Scholar 

  • Verner-Carlsson J, Lõhmus M, Sundström K, Strand TM, Verkerk M, Reusken C, Yoshimatsu K, Arikawa J, van de Goot F, Lundkvist Å (2015) First evidence of Seoul hantavirus in the wild rat population in the Netherlands. Infection Ecology and Epidemiology 5:27215 https://doi.org/10.3402/iee.v5.27215

    Article  PubMed  Google Scholar 

  • Vincent MJ, Quiroz E, Gracia F, Sanchez AJ, Ksiazek TG, Kitsutani PT, Ruedas LA, Tinnin DS, Caceres L, Garcia A, Rollin PE, Mills JN, Peters CJ, Nichol ST (2000) Hantavirus pulmonary syndrome in Panama: identification of novel hantaviruses and their likely reservoirs. Virology 277:14-19 https://doi.org/10.1006/viro.2000.0563

    Article  PubMed  CAS  Google Scholar 

  • Wallace AR (1894) The Palæarctic and Nearctic regions compared as regards the families and genera of their mammalia and birds. Natural Science accessed through http://people.wku.edu/charles.smith/wallace/S500.htm

  • Waltee D, Lonner BN, Kuenzi AJ, Douglass RJ (2009) Seasonal dispersal patterns of sylvan deer mice (Peromyscus maniculatus) within Montana rangelands. The Journal of Wildlife Diseases 45:998-1007 https://doi.org/10.7589/0090-3558-45.4.998

    Article  PubMed  Google Scholar 

  • Wang H, Yoshimatsu K, Ebihara H, Ogino M, Araki K, Kariwa H, Wang Z, Luo Z, Li D, Hang C, Arikawa J (2000) Genetic diversity of hantaviruses isolated in China and characterization of novel hantaviruses isolated from Niviventer confucianus and Rattus rattus. Virology 278:332-345 https://doi.org/10.1006/viro.2000.0630

    Article  PubMed  CAS  Google Scholar 

  • Wang CQ, Gao JH, Li M, Guo WP, Lu MQ, Wang W, Hu MX, Li MH, Yang J, Liang HJ, Tian XF, Holmes EC, Zhang YZ (2014) Co-circulation of Hantaan, Kenkeme, and Khabarovsk hantaviruses in Bolshoy Ussuriysky Island, China. Virus Research 191:51-58 https://doi.org/10.1016/j.virusres.2014.07.021

    Article  PubMed  CAS  Google Scholar 

  • Weidmann M, Schmidt P, Vackova M, Krivanec K, Munclinger P, Hufert FT (2005) Identification of genetic evidence for Dobrava virus spillover in rodents by nested reverse transpriction (RT)-PCR and TaqMan RT-PCR. Journal of Clinical Microbiology 43(2):808-812 https://doi.org/10.1128/jcm.43.2.808-812.2005

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Weiss S, Witkowski PT, Auste B, Nowak K, Weber N, Fahr J, Mombouli JV, Wolfe ND, Drexler JF, Drosten C, Klempa B, Leendertz FH, Krüger DH (2012) Hantavirus in bat, Sierra Leone. Emerging Infectious Diseases 18:159-161

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiens JJ, Graham CH (2005) Niche conservatism: integrating evolution, ecology, and conservation biology. Annual Review in Ecology and Systematics 36:519-539 https://doi.org/10.1146/annurev.ecolsys.36.102803.095431

    Article  Google Scholar 

  • Wilson DE, Reeder DM (2005) Mammal species of the world a taxonomic and geographic reference, 3rd edition, volume 2. Baltimore, MA: The Johns Hopkins University Press

    Google Scholar 

  • Wilson K (2009) Climate change and the spread of infectious ideas. Ecology 90:901-902

    Article  PubMed  Google Scholar 

  • Wobeser GA (2007) Disease in wild animals investigation and management. Springer-Verlag Berlin Heidelberg Publishers, pp. 3-16, New York, NY

  • Woolhouse ME, Haydon DT, Antia R (2005) Emerging pathogens: the epidemiology and evolution of species jumps. TREE 20:238-244 https://doi.org/10.1016/j.tree.2005.02.009

    Article  PubMed  Google Scholar 

  • Xiao SY, Leduc JW, Chu YK, Schmaljohn CS (1994) Phylogenetic analyses of virus isolates in the genus Hantavirus, family Bunyaviridae. Virology 198:205–17

    Article  PubMed  CAS  Google Scholar 

  • Yanagihara R, Gu SH, Arai S, Kang HJ, Song J-W (2014) Hantaviruses: rediscovery and new beginnings. Virus Research 187:6-14 https://doi.org/10.1016/j.virusres.2013.12.038

    Article  PubMed  CAS  Google Scholar 

  • Yashina LN, Patrushev NA, Ivanov LI, Slonova RA, Mishin VP, Kompanez GG, Zdanovskaya NI, Kuzina II, Safronov PF, Chizhikov VE, Schmaljohn C, Netesov S V (2000) Genetic diversity of hantaviruses associated with hemorrhagic fever with renal syndrome in the far east of Russia. Virus Research 70:31-44 https://doi.org/10.1016/s0168-1702(00)00203-3

    Article  PubMed  CAS  Google Scholar 

  • Yashina L, Mishin V, Zdanovskaya N, Schmaljohn C, Ivanov L (2001) A newly discovered variant of a hantavirus in Apodemus peninsulae, far eastern Russia. Emerging Infectious Diseases 7:912-913

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yashina LN, Abramov SA, Gutorov VV, Dupal TA, Krivopalov AV, Panov VV, Danchinova GA, Vinogradov VV, Luchnikova EM, Hay J, Kang HJ, Yanagihara R (2010) Seewis virus: phylogeography of a shrew-borne hantavirus in Siberia, Russia. Vector-Borne and Zoonotic Diseases 10:585-91 https://doi.org/10.1089/vbz.2009.0154

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeier M, Handermann M, Bahr U, Rensch B, Müller S, Kehm R, Muranyi W, Darai G (2005) New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention - a review. Virus Genes 30:157-180 https://doi.org/10.1007/s11262-004-5625-2

    Article  PubMed  CAS  Google Scholar 

  • Zhang YZ, Zou Y, Yan YZ, Hu GW, Yao LS, Du ZS, Jin LZ, Liu YY, Li MH, Chen HX, Fu ZF (2007) Detection of phylogenetically distinct Puumala-like viruses from red-grey vole Clethrionomys rufocanus in China. Journal of Medical Virology 79:1208-1218

    Article  PubMed  CAS  Google Scholar 

  • Zhang YZ, Zou Y, Fu ZF, Plyusnin A (2010) Hantavirus infections in humans and animals, China. Emerging Infectious Diseases 16:1195-1203 https://doi.org/10.3201/eid1608.090470

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang YZ, Yuan J, Yang X, Zhou J, Yang W, Peng C, Zhang H-L, Shi Z (2011) A novel hantavirus detected in Yunnan red-backed vole (Eothenomys miletus) in China. Journal of General Virology 92:1454–1457 https://doi.org/10.1099/vir.0.030122-0

    Article  PubMed  CAS  Google Scholar 

  • Zou Y, Xiao QY, Dong X, Lv W, Zhang SP, Li MH, Plyusnin A, Zhang YZ (2008) Genetic analysis of hantaviruses carried by reed voles Microtus fortis in China. Virus Research 137:122-128 https://doi.org/10.1016/j.virusres.2008.06.012

    Article  PubMed  CAS  Google Scholar 

  • Zuo SQ, Gong ZD, Fang LQ, Jiang JF, Zhang JS, Zhao QM, Cao WC (2014) A new hantavirus from the stripe-backed shrew (Sorex cylindricauda) in the People’s Republic of China. Virus Research 184:82-86 https://doi.org/10.1016/j.virusres.2014.02.004016/j.virusres.2014.02.004

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Iván Castro-Arellano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Milholland, M.T., Castro-Arellano, I., Suzán, G. et al. Global Diversity and Distribution of Hantaviruses and Their Hosts. EcoHealth 15, 163–208 (2018). https://doi.org/10.1007/s10393-017-1305-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-017-1305-2

Keywords

Navigation