Isolation of Madre de Dios Virus (Orthobunyavirus; Bunyaviridae), an Oropouche Virus Species Reassortant, from a Monkey in Venezuela

Juan-Carlos Navarro Lab Biología de Vectores, Instituto de Zoología y Ecología Tropical, Universidad Central de Venezuela, Caracas, Venezuela.
Universidad Internacional SEK, Quito, Ecuador.

Search for other papers by Juan-Carlos Navarro in
Current site
Google Scholar
PubMed
Close
,
Dileyvic Giambalvo Lab Biología de Vectores, Instituto de Zoología y Ecología Tropical, Universidad Central de Venezuela, Caracas, Venezuela.

Search for other papers by Dileyvic Giambalvo in
Current site
Google Scholar
PubMed
Close
,
Rosa Hernandez Instituto Nacional de Higiene “Rafael Rangel” (INHRR), Ciudad Universitaria, Caracas, Venezuela.

Search for other papers by Rosa Hernandez in
Current site
Google Scholar
PubMed
Close
,
Albert J. Auguste Department of Microbiology and Immunology, Institute for Human Infections and Immunity, and Department of Pathology, University of Texas Medical Branch, Galveston, Texas.

Search for other papers by Albert J. Auguste in
Current site
Google Scholar
PubMed
Close
,
Robert B. Tesh Department of Microbiology and Immunology, Institute for Human Infections and Immunity, and Department of Pathology, University of Texas Medical Branch, Galveston, Texas.

Search for other papers by Robert B. Tesh in
Current site
Google Scholar
PubMed
Close
,
Scott C. Weaver Department of Microbiology and Immunology, Institute for Human Infections and Immunity, and Department of Pathology, University of Texas Medical Branch, Galveston, Texas.

Search for other papers by Scott C. Weaver in
Current site
Google Scholar
PubMed
Close
,
Humberto Montañez Dirección General de Salud Ambiental, Ministerio del Poder Popular para la Salud, Caracas, Venezuela.

Search for other papers by Humberto Montañez in
Current site
Google Scholar
PubMed
Close
,
Jonathan Liria Departamento de Biología, Facultad Experimental de Ciencias y Tecnología (FACYT), Universidad de Carabobo, Valencia, Venezuela.

Search for other papers by Jonathan Liria in
Current site
Google Scholar
PubMed
Close
,
Anderson Lima Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Anderson Lima in
Current site
Google Scholar
PubMed
Close
,
Jorge Fernando Soares Travassos da Rosa Departament of Arbovirology and Hemorrhagic Fevers, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Jorge Fernando Soares Travassos da Rosa in
Current site
Google Scholar
PubMed
Close
,
Sandro P. da Silva Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Sandro P. da Silva in
Current site
Google Scholar
PubMed
Close
,
Janaina M. Vasconcelos Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Janaina M. Vasconcelos in
Current site
Google Scholar
PubMed
Close
,
Rodrigo Oliveira Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Rodrigo Oliveira in
Current site
Google Scholar
PubMed
Close
,
João L. S. G. Vianez Jr. Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by João L. S. G. Vianez Jr. in
Current site
Google Scholar
PubMed
Close
, and
Marcio R. T. Nunes Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Ananindeua, Para, Brazil.

Search for other papers by Marcio R. T. Nunes in
Current site
Google Scholar
PubMed
Close
Restricted access

Oropouche virus (OROV), genus Orthobunyavirus, family Bunyaviridae, is an important cause of human illness in tropical South America. Herein, we report the isolation, complete genome sequence, genetic characterization, and phylogenetic analysis of an OROV species reassortant, Madre de Dios virus (MDDV), obtained from a sick monkey (Cebus olivaceus Schomburgk) collected in a forest near Atapirire, a small rural village located in Anzoategui State, Venezuela. MDDV is one of a growing number of naturally occurring OROV species reassortants isolated in South America and was known previously only from southern Peru.

Author Notes

* Address correspondence to Marcio R. T. Nunes, Center for Technological Innovation, Evandro Chagas Institute, Ministry of Health, Rod Br 316 s/n, Ananindeua, Para 67120-030, Brazil. E-mail: marcionunes@iec.pa.gov.br

Financial support: This work was supported by a grant from FONACIT-Mision Ciencia-Venezuela (2008000911-4) to Juan-Carlos Navarro; the Western Regional Center of Excellence for Biodefense and Emerging Infectious Disease Research, National Institutes of Health (NIH) grant U54 AIO57156; NIH contract HHSN272202000040I/HHSN200004/D04; the Robert E. Shope International Fellowship in Infectious Diseases from the American Society of Tropical Medicine and Hygiene; CNPq (Brazilian National Council for Research and Development) grant no. 302032/2011-8. Albert J. Auguste was supported by the James W. McLaughlin endowment fund.

Authors' addresses: Juan-Carlos Navarro, Lab Biología de Vectores, Instituto de Zoología y Ecología Tropical, Universidad Central de Venezuela, Caracas, Venezuela, and Universidad Internacional SEK, Quito, Ecuador, E-mail: jcnavac@gmail.com. Dileyvic Giambalvo, Lab Biología de Vectores, Instituto de Zoología y Ecología Tropical, Universidad Central de Venezuela, Caracas, Venezuela, E-mail: dileyvic@gmail.com. Rosa Hernandez, Instituto Nacional de Higiene “Rafael Rangel” (INHRR), Caracas, Venezuela, E-mail: rosahernandez08@gmail.com. Albert J. Auguste and Robert B. Tesh, Department of Microbiology and Immunology, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, and Department of Pathology, University of Texas Medical Branch, Galveston, TX, E-mails: aj1augus@utmb.edu and rtesh@utmb.edu. Scott C. Weaver, Department of Pathology, University of Texas Medical Branch, Galveston, TX, E-mail: sweaver@utmb.edu. Humberto Montañez, Dirección General de Salud Ambiental, Ministerio del Poder Popular Para la Salud, Caracas, Venezuela, E-mail: virus.arbo@yahoo.com. Jonathan Liria, Departamento de Biología, Facultad Experimental de Ciencias y Tecnología (FACYT), Universidad de Carabobo, Valencia, Venezuela, E-mail: jonathan.liria@gmail.com. Anderson Lima, Jorge Fernando Soares Travassos da Rosa, Sandro P. da Silva, Janaina M. Vasconcelos, Rodrigo Oliveira, João L. S. G. Vianez Jr., and Marcio R. T. Nunes, Centro de Inovações Tecnológicas, Instituto Evandro Chagas, Para, Ananindeua, Brazil, E-mails: andersonfcl@hotmail.com, jorgetravassos@iec.pa.gov.br, spatroca@gmail.com, janaina.mvasconcelos@yahoo.com.br, rodrigodeoliveira01@gmail.com, joao.vianezjr@gmail.com, and marcionunes@iec.pa.gov.br.

  • 1.

    Dietzgen RG, Calisher CH, Kurath G, Kuzman IV, Rodriguez LL, Stone DM, Tesh RB, Tordo N, Walker PJ, Wetzel T, Whitfield AE, 2012. Virus taxonomy. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. Ninth Report of the International Committee on Taxonomy of Viruses. San Diego, CA: Elsevier, 654681.

    • Search Google Scholar
    • Export Citation
  • 2.

    Schmaljohn CS, Nichol ST, 2007. Bunyaviridae. Knipe DM, Howley PM, eds. Fields Virology. 5th edition, Vol. 2. Philadelphia, PA: Wolters Kluwer/Lippincott Williams and Wilkins, 17411789.

    • Search Google Scholar
    • Export Citation
  • 3.

    Elliott RM, Schaljohn CS, 2013. Bunyaviridae. Knipe DM, Howley PM, eds. Fields Virology, 6th edition, Vol. 1. Philadelphia, PA: Wolter Kluwer/Lippincott Williams and Wilkins, 12441282.

    • Search Google Scholar
    • Export Citation
  • 4.

    Travassos da Rosa JFS, Travassos da Rosa APA, Vasconcelos PFC, Pinheiro FP, Rodrigues SG, Travassos da Rosa ES, Dias L, Cruz A, 1988. Arboviruses isolated in the Evandro Chagas Institute, including some described for the first time in the Brazilian Amazon region, their known host, and their pathology for man. Travassos da Rosa APA, Vasconcelos PFC, Travassos da Rosa JFS, eds. An Overview of Arbovirology in Brazil and Neighbouring Countries. Belem, Brazil: Instituto Evandro Chagas, 1931.

    • Search Google Scholar
    • Export Citation
  • 5.

    Vasconcelos PFC, Travassos da Rosa APA, Degallier N, Travassos da Rosa JFS, Pinheiro FP, 1992. Clinical and ecoepidemiological situation of human arboviruses in Brazilian Amazonia. Cienc e Cult (Sao Paulo) 44: 117124.

    • Search Google Scholar
    • Export Citation
  • 6.

    LeDuc JW, Pinheiro FP, 1988. Oropouch fever. Monath TP, ed. The Arboviruses: Epidemiology and Ecology, Vol. 4. Boca Raton, FL: CRC Press Inc., 114.

    • Search Google Scholar
    • Export Citation
  • 7.

    Anderson CR, Spence L, Downs WG, Aitken THG, 1961. Oropouche virus: a new human disease agent from Trinidad, West Indies. Am J Trop Med Hyg 10: 574578.

    • Search Google Scholar
    • Export Citation
  • 8.

    Pinheiro FP, Travassos da Rosa APA, Ishak R, Freitas RB, Gomes MLC, LeDuc JW, Oliva OFP, 1981. Oropouche virus. 1. A review of clinical, epidemiological, and ecological findings. Am J Trop Med Hyg 30: 149160.

    • Search Google Scholar
    • Export Citation
  • 9.

    Pinheiro FP, Hoch AL, Gomes MLC, Roberts DR, 1981. Oropouche virus. IV. Laboratory transmission by Culicoides paraensis. Am J Trop Med Hyg 30: 172176.

    • Search Google Scholar
    • Export Citation
  • 10.

    Roberts DR, Hock AL, Dixon KE, Llewellyn CH, 1981. Oropouche virus. III. Entomological observations from three epidemics in Para, Brazil, 1975. Am Trop Med Hyg 30: 165171.

    • Search Google Scholar
    • Export Citation
  • 11.

    Pinheiro FP, Travassos da Rosa AP, Travassos da Rosa JF, Bensabath G, 1976. An outbreak of Oropouche virus disease in the vicinity of Santarem, Para, Brazil. Tropenmed Parasitol 27: 213223.

    • Search Google Scholar
    • Export Citation
  • 12.

    Nunes MR, Caricio Martins L, Guerreiro Rodrigues S, Chiang JO, Da Silva Azevedo RDS, Travassos da Rosa APA, da Costa Vasconcelos PF, 2005. Oropouche virus isolation, southeast Brazil. Emerg Infect Dis 11: 16101613.

    • Search Google Scholar
    • Export Citation
  • 13.

    Bowen MD, Trappier SG, Sanchez AJ, Meyer RF, Goldsmith CS, Zaki SR, Dunster LM, Peters CJ, Ksiazek TG, Nichol ST, 2001. A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 29: 185190.

    • Search Google Scholar
    • Export Citation
  • 14.

    Tilston-Lunel N, Hughes J, Acrani G, da Silva D, Azevedo R, Rodrigues S, Vasconcelos P, Nunes M, Elliott R, 2015. A genetic analysis of the Oropouche virus species and identification of a novel M segment sequence. J Gen Virol 96: 16361650.

    • Search Google Scholar
    • Export Citation
  • 15.

    Aguilar PV, Barrett AD, Saeed MF, Watts DM, Russell K, Guevara C, Ampuero JS, Suarez L, Cespedes M, Montgomery JM, Halsey ES, Kochel TJ, 2011. Iquitos virus: a novel reassortant Orthobunyavirus associated with human illness in Peru. PLoS Negl Trop Dis 5: e1315, doi:10.1371/journal.pntd.0001315.

    • Search Google Scholar
    • Export Citation
  • 16.

    Ladner J, Savji N, Lofts L, Travassos da Rosa A, Wiley M, Gestole M, Rosen G, Guzman H, Vasconcelos P, Nunes M, Kochel T, Lipkin W, Tesh R, Palacios G, 2014. Genomic and phylogenetic characterization of viruses included in the Manzanilla and Oropouche species complexes of the genus Orthobunyavirus, family Bunyaviridae. J Gen Virol 95: 10551066.

    • Search Google Scholar
    • Export Citation
  • 17.

    Tan R, Ksiazek TG, Olson JG, 1981. Comparative sensitivity of mosquito inoculation and mammalian cell culture for isolation of some arboviruses in Indonesia. Southeast Asian J Trop Med Public Health 12: 544548.

    • Search Google Scholar
    • Export Citation
  • 18.

    Auguste AJ, Liria J, Forrester NL, Giambalvo D, Long KC, Morón D, De Manzione N, Tesh RB, Halsey S, Kochel TJ, Hernandez R, Navarro J-C, Weaver SC, 2015. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela. Emerg Infect Dis 21: 17421750.

    • Search Google Scholar
    • Export Citation
  • 19.

    Rothberg JM, Hinz W, Rearick TM, Schultz J, Mileski W, Davey M, Leamon JH, Johnson K, Milgrew MJ, Edwards M, Hoon J, Simons JF, Marran D, Myers JW, Davidson JF, Branting A, Nobile JR, Puc BP, Light D, Clark TA, Huber M, Branciforte JT, Stoner IB, Cawley SE, Lyons M, Fu Y, Homer N, Sedova M, Miao X, Reed B, Sabina J, Feierstein E, Schorn M, Alanjary M, Dimalanta E, Dressman D, Kasinskas R, Sokolsky T, Fidanza JA, Namsaraev E, McKernan KJ, Williams A, Roth GT, Bustillo J, 2011. An integrated semiconductor device enabling non-optical genome sequencing. Nature 475: 348352.

    • Search Google Scholar
    • Export Citation
  • 20.

    Wanzeller ALM, Martins LC, Diniz Júnior JAP, de Almeida Medeiros DB, Cardoso JF, da Silva DEA, de Oliveira LF, de Vasconcelos JM, Nunes MRT, Vianez JL Jr, Vasconcelos PF, 2014. Xiburema virus, a hitherto undescribed virus within the family Rhabdoviridae isolated in the Brazilian Amazon region. Genome Announc 2: e00454e14.

    • Search Google Scholar
    • Export Citation
  • 21.

    Chevreux B, Pfisterer T, Drescher B, Driesel AJ, Müller WEG, Wetter T, Suhai S, 2004. Using the miraEST assembler for reliable and automated mRNA transcript assembly and SNP detection in sequenced ESTs. Genome Res 14: 11471159.

    • Search Google Scholar
    • Export Citation
  • 22.

    Roche, 2011. 5/3 RACE Kit, 2nd Generation. Manual. Vol. 1–31. doi:10.1016/j.eurpsy.2007.01.525.

  • 23.

    Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A, 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 16471649.

    • Search Google Scholar
    • Export Citation
  • 24.

    Williamson DF, Parker RA, Kendrick JS, 1989. The box plot: a simple visual method to interpret data. Ann Intern Med 110: 916921.

  • 25.

    Stamatakis A, 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 13121313.

    • Search Google Scholar
    • Export Citation
  • 26.

    Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O, 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307321, doi:10.1093/sysbio/syq010.

    • Search Google Scholar
    • Export Citation
  • 27.

    Drummond AJ, Suchard MA, Xie D, Rambaut A, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 19691973.

  • 28.

    Rambaut A, 2009. FigTree, a Graphical Viewer of Phylogenetic Trees. Inst Evol Biol Univ Edinburgh. Available at: http://tree.bio.ed.ac.uk/software/figtree/.

    • Search Google Scholar
    • Export Citation
  • 29.

    Escoto-Delgadillo M, Flores Romero L, Gomez Flores-Ramos L, Vazquez Torres BM, Torres Mendoza BM, Vazquez Valls E, 2008. Comparing RIP, REGA and SIMPLOT Software to Define the HIV-1 Recombination in Mexican Population. XVII International AIDS Conference. August 3–8, 2008, Mexico City, Mexico.

    • Search Google Scholar
    • Export Citation
  • 30.

    Savji N, Palacios G, Travassos Da Rosa A, Hutchison S, Celone C, Hui J, Briese T, Calisher CH, Tesh RB, Lipkin WI, 2011. Genomic and phylogenetic characterization of Leanyer virus, a novel Orthobunyavirus isolated in northern Australia. J Gen Virol 92: 16761687.

    • Search Google Scholar
    • Export Citation
  • 31.

    Mares MA, 1992. Neotropical mammals and the myth of Amazonian biodiversity. Science 255: 976979.

  • 32.

    Regalado A, 2010. Biodiversity. Brazil says rate of deforestation in Amazon continues to plunge. Science 329: 12701271.

  • 33.

    Jones-Walters L, Čivić K, 2010. Wilderness and biodiversity. J Nat Conserv 18: 338339.

  • 34.

    Moura NG, Lees AC, Andretti CB, Davis BJW, Solar RRC, Aleixo A, Barlow J, Ferreira J, Gardner TA, 2013. Avian biodiversity in multiple-use landscapes of the Brazilian Amazon. Biol Conserv 167: 339348.

    • Search Google Scholar
    • Export Citation
  • 35.

    Dixon KE, Travassos da Rosa APA, Travassos da Rosa JF, Llewellyn CH, 1981. Oropouche virus. II. Epidemiological observations during an epidemic in Santarem, Para, Brazil in 1975. Am J Trop Med Hyg 30: 161164.

    • Search Google Scholar
    • Export Citation
  • 36.

    Vasconcelos HB, Azevedo RSS, Casseb SM, Nunes-Neto JP, Chiang JO, Cantuária PC, Segura MNO, Martins LC, Monteiro HAO, Rodrigues SG, Nunes MRT, Vasconcelos PFC, 2009. Oropouche fever epidemic in northern Brazil: epidemiology and molecular characterization of isolates. J Clin Virol 44: 129133.

    • Search Google Scholar
    • Export Citation
  • 37.

    Nunes MRT, Martins LC, Rodrigues SG, Chiang JO, Azevedo RDSDS, Da Rosa APAT, Vasconcelos PFDC, 2005. Oropouche virus isolation, southeast Brazil. Emerg Infect Dis 11: 16101613.

    • Search Google Scholar
    • Export Citation
  • 38.

    Azevedo RDSDS, Nunes MRT, Chiang JO, Bensabath G, Vasconcelos HB, Pinto AYDN, Martins LC, Monteiro HADO, Rodrigues SG, Vasconcelos PFDC, 2007. Reemergence of Oropouche fever, northern Brazil. Emerg Infect Dis 13: 912915.

    • Search Google Scholar
    • Export Citation
  • 39.

    Vasconcelos HB, Nunes MRT, Casseb LMN, Carvalho VL, da Silva EVP, Silva M, Casseb SMM, Vasconcelos PFC, 2011. Molecular epidemiology of Oropouche virus, Brazil. Emerg Infect Dis 17: 800806.

    • Search Google Scholar
    • Export Citation
  • 40.

    Saeed MF, Wang H, Nunes M, Vasconcelos PFC, Weaver SC, Shope RE, Watts DM, Tesh RB, Barrett ADT, 2000. Nucleotide sequences and phylogeny of the nucleocapsid gene of Oropouche virus. J Gen Virol 81: 743748.

    • Search Google Scholar
    • Export Citation
  • 41.

    Monath TP, Vasconcelos PF, 2015. Yellow fever. J Clin Virol 64: 160173.

  • 42.

    Nunes MRT, Palacios G, Cardoso JF, Martins LC, Sousa EC, de Lima CPS, Medeiros DBA, Savji N, Desai A, Rodrigues SG, Carvalho VL, Lipkin WI, Vasconcelos PFC, 2012. Genomic and phylogenetic characterization of Brazilian yellow fever virus strains. J Virol 86: 1326313271.

    • Search Google Scholar
    • Export Citation
  • 43.

    Villordo SM, Gamarnik AV, 2009. Genome cyclization as strategy for flavivirus RNA replication. Virus Res 139: 230239.

  • 44.

    Guu TSY, Zheng W, Tao YJ, 2012. Bunyavirus: structure and replication. Adv Exp Med Biol 726: 245266.

  • 45.

    Bryant JE, Vasconcelos PFC, Rijnbrand RCA, Mutebi JP, Higgs S, Barrett ADT, 2005. Size heterogeneity in the 3′ noncoding region of South American isolates of yellow fever virus. J Virol 79: 38073821.

    • Search Google Scholar
    • Export Citation
  • 46.

    Yanase T, Yoshida K, Ohashi S, Kato T, Tsuda T, 2003. Sequence analysis of the medium RNA segment of three Simbu serogroup viruses, Akabane, Aino, and Peaton viruses. Virus Res 93: 6369.

    • Search Google Scholar
    • Export Citation
  • 47.

    Saeed MF, Li L, Wang H, Weaver SC, Barrett ADT, 2001. Phylogeny of the Simbu serogroup of the genus Bunyavirus. J Gen Virol 82: 21732181.

  • 48.

    Briese T, Bird B, Kapoor V, Nichol ST, Lipkin WI, 2006. Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in east Africa. J Virol 80: 56275630.

    • Search Google Scholar
    • Export Citation
  • 49.

    Chowdhary R, Street C, Travassos Da Rosa A, Nunes M, Tee KK, Hutchison SK, Vasconcelos PFC, Tesh R, Lipkin IW, Briese T, 2012. Genetic characterization of the Wyeomyia group of orthobunyaviruses and their phylogenetic relationships. J Gen Virol 93: 10231034.

    • Search Google Scholar
    • Export Citation
  • 50.

    Terzian ACB, De Bronzoni RVM, Drumond BP, Da Silva-Nunes M, Da Silva NS, Ferreira MU, Sperança MA, Nogueira ML, 2009. Sporadic Oropouche virus infection, Acre, Brazil. Emerg Infect Dis 15: 348350.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 58 58 21
Full Text Views 476 144 0
PDF Downloads 177 46 0
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save