• 1.

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

    • Search Google Scholar
    • Export Citation
  • 2.

    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: 1419.

    • Search Google Scholar
    • Export Citation
  • 3.

    Bayard V, Kitsutani PT, Barria EO, Ruedas LA, Tinnin DS, Munoz C, de Mosca IB, Guerrero G, Kant R, Garcia A, Caceres L, Gracia F, Quiroz E, de Castillo Z, Armien B, Libel M, Mills JN, Khan AS, Nichol ST, Rollin PE, Ksiazek TG, Peters CJ, 2004. Outbreak of hantavirus pulmonary syndrome, Los Santos, Panama, 1999–2000. Emerg Infect Dis 10: 16351642.

    • Search Google Scholar
    • Export Citation
  • 4.

    Armien AG, Armien B, Koster FT, Pascale JM, 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. Am J Trop Med Hyg 81: 5966.

    • Search Google Scholar
    • Export Citation
  • 5.

    Nelson R, Canate R, Pascale JM, Dragoo JW, Armien B, Armien AG, Koster F, 2010. Confirmation of Choclo virus as the cause of hantavirus cardiopulmonary syndrome and high serum antibody prevalence in Panama. J Med Virol 70: 22892295.

    • Search Google Scholar
    • Export Citation
  • 6.

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

    • Search Google Scholar
    • Export Citation
  • 7.

    Armien B, Pascale JM, Bayard V, Munoz C, Mosca I, Guerrero G, Armien A, Quiroz E, Castillo Z, Zaldivar Y, Gracia F, Hjelle B, Koster F, 2004. High seroprevalence of hantavirus infection on the Azuero peninsula of Panama. Am J Trop Med Hyg 70: 682687.

    • Search Google Scholar
    • Export Citation
  • 8.

    Armien B, Pascale JM, Munoz C, Lee S-J, Choi KL, Avila M, Broce C, Armien AG, Gracia F, Hjelle B, Koster F, 2011. Incidence rate for hantavirus infections without pulmonary syndrome, Panama. Emerg Infect Dis 17: 19361939.

    • Search Google Scholar
    • Export Citation
  • 9.

    Ferrer JF, Jonsson CB, Esteban E, Galligan D, Basombrio MA, Peralta-Ramos M, Bharadwaj M, Torrez-Martinez N, Callahan J, Segovia A, Hjelle B, 1998. High prevalence of hantavirus infection in Indian communities of the Paraguayan and Argentinean Gran Chaco. Am J Trop Med Hyg 59: 438444.

    • Search Google Scholar
    • Export Citation
  • 10.

    Campos GM, Moro de Sousa RL, Badra SJ, Pane C, Gomes UA, Figueiredo LT, 2003. Serological survey of hantavirus in Jardinopolis County, Brazil. J Med Virol 71: 417422.

    • Search Google Scholar
    • Export Citation
  • 11.

    Mendes WS, da Silva AAM, Aragao LFC, Aragao NJL, Raposo M de L, Elkhoury MR, Suzuky A, Ferreira IB, de Sousa LT, Pannuti CS, 2004. Hantavirus infection in Anajatuba, Maranhao, Brazil. Emerg Infect Dis 10: 14961498.

    • Search Google Scholar
    • Export Citation
  • 12.

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

    • Search Google Scholar
    • Export Citation
  • 13.

    Levis S, Rowe JE, Morzunov S, Enria DA, St. Joan S, 1997. New hantaviruses causing hantavirus pulmonary syndrome in Central Argentina [letter]. Lancet 349: 998999.

    • Search Google Scholar
    • Export Citation
  • 14.

    Castillo HC, Sanhueza HL, Tager FM, Munoz NS, Ossa AG, Vial CP, 2002. Seroprevalence of antibodies against hantavirus in 10 communities of the IX region of Chile where hantavirus cardiopulmonary syndrome cases were reported. Rev Med Chil 130: 110.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hjelle B, Jenison S, Torrez-Martinez N, Herring B, Quan S, Polito A, Pichuantes S, Yamada T, Morris C, Eigh F, Lee HW, Artsob H, Dinello R, 1997. Rapid and specific detection of Sin Nombre virus antibodies in patients with hantavirus pulmonary syndrome by a strip immunoblot assay suitable for field diagnosis. J Clin Microbiol 35: 600608.

    • Search Google Scholar
    • Export Citation
  • 16.

    Feldmann H, Sanchez A, Morzunov S, Spiropoulou CF, Rollin PE, Ksiazek TG, Peters CJ, Nichol ST, 1993. Utilization of autopsy RNA for the synthesis of the nucleocapsid antigen of a newly recognized virus associated with hantavirus pulmonary syndrome. Virus Res 30: 351367.

    • Search Google Scholar
    • Export Citation
  • 17.

    Cardona MN, Moros RM, Lopez EA, Perez JL, Hernandez RC, 2008. Diagnostico de leptospirosis mediante la PCR en pacientes con sindrome febril icterohemorragico. Rev Soc Venez Microbiol 28: 2430.

    • Search Google Scholar
    • Export Citation
  • 18.

    Zavasky DM, Hjelle B, Peterson MC, Denton RW, Reimer L, 1999. Acute infection with Sin Nombre hantavirus without pulmonary complications. Clin Infect Dis 29: 664666.

    • Search Google Scholar
    • Export Citation
  • 19.

    Kitsutani PT, Denton RW, Fritz CL, Murray RA, Todd RL, Pape WJ, Wyatt Frampton J, Young JC, Khan AS, Peters CJ, Ksiazek TG, 1999. Acute Sin Nombre hantavirus infection without pulmonary syndrome, United States. Emerg Infect Dis 5: 701705.

    • Search Google Scholar
    • Export Citation
  • 20.

    Galeno H, Mora J, Villagra E, Fernandez J, Hernandez J, Mertz GJ, Ramirez E, 2002. First human isolate of hantavirus (Andes virus) in the Americas. Emerg Infect Dis 8: 657661.

    • Search Google Scholar
    • Export Citation
  • 21.

    Bruce MG, Sanders EJ, Leake JA, Zaidel O, Bragg SL, Aye T, Shutt KA, Deseda CC, Rigau-Perez JG, Tappero JW, Perkins BA, Spiegel RA, Ashford DA, 2005. Leptospirosis among patients presenting with dengue-like illness in Puerto Rico. Acta Trop 96: 3646.

    • Search Google Scholar
    • Export Citation
  • 22.

    Ellis T, Imrie A, Katz AR, Effler PV, 2008. Underrecognition of leptospirosis during a dengue fever outbreak in Hawaii, 2001–2002. Vector Borne Zoonotic Dis 8: 541547.

    • Search Google Scholar
    • Export Citation
  • 23.

    Koster F, Foucar K, Hjelle B, Scott A, Chong Y-Y, Larson R, McCabe M, 2011. Rapid presumptive diagnosis of hantavirus cardiopulmonary syndrome by peripheral blood smear review. Am J Clin Pathol 116: 665672.

    • Search Google Scholar
    • Export Citation
  • 24.

    Gavrilovskaya IN, Shepley M, Shaw R, Ginsberg MH, Mackow ER, 1998. Beta3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci USA 95: 70747079.

    • Search Google Scholar
    • Export Citation
  • 25.

    Hooper JW, Larsen T, Custer DM, Schmaljohn CS, 2001. A lethal disease model for hantavirus pulmonary syndrome. Virology 289: 614.

  • 26.

    Campen MJ, Milazzo ML, Fulhorst CF, Obot Akata CJ, Koster F, 2006. Characterization of shock in a hamster model of hantavirus infection. Virology 356: 4549.

    • Search Google Scholar
    • Export Citation
  • 27.

    Matthys VS, Gorbunova EE, Gavrilovskaya IN, Mackow ER, 2010. Andes virus recognition of human and Syrian hamster beta3-integrins is determined by an L33P substitution in the PSI domain. J Virol 84: 352360.

    • Search Google Scholar
    • Export Citation
  • 28.

    Eyraguirre EJ, Milazzo ML, Koster FT, Fulhorst CF, 2008. Choclo virus infection in the Syrian golden hamster. Am J Trop Med Hyg 78: 669674.

  • 29.

    Suzan G, Marce E, Giermakowski JT, Armien B, Pascale J, Mills J, Ceballos G, Gomez A, Aguirre AA, Salazar-Brazo J, Armien A, Parmenter R, Yates T, 2008. The effect of habitat fragmentation and species diversity loss on hantavirus prevalence in Panama. Ann N Y Acad Sci 1149: 8083.

    • Search Google Scholar
    • Export Citation
  • 30.

    Suzan G, Marce E, Giermakowski JT, Mills JN, Ceballos G, Ostfeld RS, Armien B, Pascale JM, Yates TL, 2009. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence. PLoS One 4: e5461.

    • Search Google Scholar
    • Export Citation
 
 
 
 

 

 
 

 

 

 

 

 

 

Hantavirus Fever without Pulmonary Syndrome in Panama

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  • Epidemiology and Microbiology, Gorgas Memorial Institute for Health Research, Panama City, Panama; Epidemiology, Ministry of Health, Panama City, Panama; Clinical Medicine, Social Security Health System, Panama City, Panama; Pulmonary Medicine, Santo Tomas Hospital, Panama City, Panama; Departments of Pathology, Biology, and Molecular Genetics and Microbiology, University of New Mexico Health Sciences Center, Albuquerque, New Mexico; Lovelace Respiratory Research Institute, Albuquerque, New Mexico

In Panama, hantavirus pulmonary syndrome (HPS) is caused by Choclo virus, a species phylogenetically related to Andes and Maporal viruses. Up to 60% of the population has been positive for specific serum antibody in community-based surveys, but mortality is very uncommon. In four western Panama clinics, we tested individuals presenting with a severe febrile prodrome for acute hantavirus (HV) infection by immunoglobulin M enzyme-linked immunosorbent assay and reverse transcription polymerase chain reaction as well as clinically similar infections, such as dengue and leptospirosis. From 2006 to 2009, at least 21% of 117 patients diagnosed with HV infection had HV Fever (HF) with no evidence of pulmonary edema (no respiratory distress or radiographic lung infiltrates), and 44% of patients had very mild HPS (radiographic pulmonary edema but no respiratory insufficiency). HV infection caused by Choclo virus in Panama presents often as HF, which contrasts with HV in the Americas but is consistent with the high seroprevalence in endemic regions.

Author Notes

* Address correspondence to Frederick Koster, Lovelace Respiratory Research Institute, 2425 Ridgecrest Drive SE, Albuquerque, NM 87108. E-mail: fkoster@lrri.org

Financial support: This study was supported by an Opportunity Pool Award and supplement from the International Centers for Infectious Diseases Research program of the National Institutes of Health (U19-AI 45452); funds from Instituto Conmemorativo Gorgas de Estudios de la Salud, Hantavirus Research Project 04-90-0075-8; the Ministry of Health, Panama; and Secretaria Nacional de Ciencia y Tecnología, Innovation and Technology Program ftd06-089.

Authors' addresses: Blas Armien, Epidemiology, Gorgas Memorial Institute for Health Research, Panama City, Panama, E-mail: barmien@gorgas.gob.pa. Juan M. Pascale and Yaxelis Mendoza, Microbiology, Gorgas Memorial Institute for Health Research, Panama City, Panama, E-mails: jmpascal@yahoo.com and ymendoza@gorgas.gob.pa. Carlos Muñoz, Jamileth Mariñas, and Deyanira Sánchez, Epidemiology, Ministry of Health, Panama City, Panama, E-mails: cbmunozg@cableonda.net, drajamilethm@gmail.com, and deyaluly@hotmail.com. Heydy Núñez and Milagro Herrera, Clinical Medicine, Social Security Health System, Panama City, Panama, E-mails: hmnm07@hotmail.com and dramherrera@yahoo.es. José Trujillo, Pulmonary Medicine, Santo Tomas Hospital, Panama City, Panama, E-mail: jmtmrt14@cableonda.net. Brian Hjelle, Department of Pathology, University of New Mexico Health Sciences Center, Albuquerque, NM, E-mail: bhjelle@salud.unm.edu. Frederick Koster, Lovelace Respiratory Research Institute, Albuquerque, NM, E-mail: fkoster@lrri.org.

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