Smith DW, Mackenzie JS, Weaver SC, 2009. Alphaviruses. Richman DD, Whitley RJ, Hayden FG, eds. Clinical Virology. Washington, DC: ASM Press, 1241–1274.
Weaver SC, Winegar R, Manger ID, Forrester NL, 2012. Alphaviruses: population genetics and determinants of emergence. Antiviral Res 94: 242–257.
Lindenbach BD, Rice CM, 2007. Flaviviridae: the viruses and their replication. Fields Virol 2: 1101–1151.
Tesh RB et al. 1999. Mayaro virus disease: an emerging mosquito-borne zoonosis in tropical South America. Clin Infect Dis 28: 67–73.
Aguilar PV, Estrada-Franco JG, Navarro-Lopez R, Ferro C, Haddow AD, Weaver SC, 2011. Endemic Venezuelan equine encephalitis in the Americas: hidden under the dengue umbrella. Future Virol 6: 721–740.
Arrigo NC, Adams AP, Weaver SC, 2010. Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision. J Virol 84: 1014–1025.
Carrera J-P et al. 2013. Eastern equine encephalitis in Latin America. N Engl J Med 369: 732–744.
Dietz WH, Galindo P, Johnson KM, 1980. Eastern equine encephalomyelitis in Panama: the epidemiology of the 1973 epizootic. Am J Trop Med Hyg 29: 133–140.
Sabattini MS, Daffner JF, Monath TP, Bianchi TI, Cropp CB, Mitchell CJ, Aviles G, 1991. Localized eastern equine encephalitis in Santiago del Estero Province, Argentina, without human infection. Medicina (B Aires) 51: 3–8.
Aguilar PV et al. 2007. Endemic eastern equine encephalitis in the Amazon region of Peru. Am J Trop Med Hyg 76: 293–298.
Johnson KM, Shelokov A, Peralta PH, Dammin GJ, Young NA, 1968. Recovery of Venezuelan equine encephalomyelitis virus in Panama. A fatal case in man. Am J Trop Med Hyg 17: 432–440.
Quiroz E, Aguilar PV, Cisneros J, Tesh RB, Weaver SC, 2009. Venezuelan equine encephalitis in Panama: fatal endemic disease and genetic diversity of etiologic viral strains. PLoS Negl Trop Dis 3: e472.
Vittor AY et al. 2016. Epidemiology of emergent Madariaga encephalitis in a region with endemic Venezuelan equine encephalitis: initial host studies and human cross-sectional study in Darien, Panama. PLoS Negl Trop Dis 10: e0004554.
Holdridge LRDG, 1956. Report on an ecological survey of the republic of Panama. Caribb For 17: 92–110.
Beaty BJ, Calisher CH, Shope RE, 1989. Arboviruses. Schmidt NJ, Emmons RW, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections. 6th edition. Washington, DC: American Public Health Association, 797–855.
Clarke DH, Casals J, 1958. Techniques for hemagglutinatination-inhibition with arthropod borned viruses. Am J Trop Med Hyg 7: 561–573.
Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE, 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70: 37–43.
Shope RE, 1963. The use of a micro-hemaglutination inhibition test to follow antibodie response after arthropod-borne virus infection in a community of forest animals. An Microbiol 11: 167–169 (Rio J).
Johnson BW, Kosoy O, Wang E, Delorey M, Russell B, Bowen RA, Weaver SC, 2011. Use of sindbis/eastern equine encephalitis chimeric viruses in plaque reduction neutralization tests for arboviral disease diagnostics. Clin Vaccin Immunol 18: 1486–1491.
Ni H, Yun NE, Zacks MA, Weaver SC, Tesh RB, Travassos Da Rosa AP, Powers AM, Frolov I, Paessler S, 2007. Recombinant alphaviruses are safe and useful serological diagnostic tools. Am J Trop Med Hyg 76: 774–781.
Weise WJ, Hermance ME, Forrester N, Adams AP, Langsjoen R, Gorchakov R, Wang E, Alcorn MDH, Tsetsarkin K, Weaver SC, 2014. A novel live-attenuated vaccine candidate for Mayaro fever. PLoS Negl Trop Dis 8: e2969.
Barros AJD, Hirakata VN, 2003. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 3: 21.
Obaldía Nicanor et al. 1991. Encefalomielitis Equina del Este, Epizootia de 1986 en Panamá. Notas Vetrinarias 1: 4–7.
Bayly NJ, Gómez C, Cárdenas LC, 2011. Darién—Migration Monitoring during 2011 in the Tacarcuna Natural Reserve. Bogotá. Available at: https://avesmigratoriascolombia.wordpress.com/. Accessed April 23, 2018.
Bayly NJ, Ortiz LC, Rubio M, Gómez C, 2014. Migration of raptors, swallows and other diurnal migratory birds through the Darien of Colombia. Ornitol Neotrop 25: 63–71.
Goldfield M, Welsh JN, Taylor BF, 1968. The 1959 outbreak of eastern encephalitis in New Jersey. 5. The inapparent infection:disease ratio. Am J Epidemiol 87: 32–33.
Sunthorn S, Galindo P, 1967. The isolation of eastern equine encephalitis from Culex (Melanoconion) taeniopus Dyar and Knab in Panama. Mosq News 27: 74–76.
Galindo P, Srihongse S, De Rodaniche E, Grayson MA, 1966. An ecological survey for arboviruses in Almirante, Panama, 1959–1962. Am J Trop Med Hyg 15: 385–400.
Carrera J-P et al. 2017. Unusual pattern of chikungunya virus epidemic in the Americas, the Panamanian experience. PLoS Negl Trop Dis 11: e0005338.
Lednicky J et al. 2016. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerg Infect Dis 22: 2000–2002.
Nelson GC, Harris V, Stone SW, 2001. Deforestation, land use, and property rights: empirical evidence from Darien, Panama. Land Econ 77: 187–205.
Walton TE, Alvarez O Jr., Buckwalter RM, Johnson KM, 1973. Experimental infection of horses with enzootic and epizootic strains of Venezuelan equine encephalomyelitis virus. J Infect Dis 128: 271–282.
Monath TP, Sabattini MS, Pauli R, Daffner JF, Mitchell CJ, Bowen GS, Cropp CB, 1985. Arbovirus investigations in Argentina, 1977–1980. IV. Serologic surveys and sentinel equine program. Am J Trop Med Hyg 34: 966–975.
Pauvolid-Correa A, Tavares FN, Costa EV, Burlandy FM, Murta M, Pellegrin AO, Nogueira MF, Silva EE, 2010. Serologic evidence of the recent circulation of Saint Louis encephalitis virus and high prevalence of equine encephalitis viruses in horses in the Nhecolandia sub-region in south Pantanal, central-west Brazil. Mem Inst Oswaldo Cruz 105: 829–833.
Rodrigues SG, Oliva, O P, Francisco AAA, Martins LC, Chiang JO, Henriques DF, Pinto da Silva EV, Daniela SGR, Assis do, SCP, 2010. Epidemiology of Saint Louis encephalitis virus in the Brazilian Amazon region and in the State of Mato Grosso do Sul, Brazil: elevated prevalence of antibodies in horses. Rev Pan-Amazônica Saúde 1: 81–86.
Komar N, Clark GG, 2006. West Nile virus activity in Latin America and the Caribbean. Rev Panam Salud Publica 19: 112–117.
Tesh RB, Travassos da Rosa APA, Guzman H, Araujo TP, Xiao SY, 2002. Immunization with heterologous flaviviruses protective against fatal West Nile encephalitis. Emerg Infect Dis 8: 245–251.
Fleiss JL, 1986. Letters to the editor: confidence intervals vs significance tests: quantitative interpretation. Am J Public Health 76: 587.
Foxman B, Frerichs RR, 1986. Letters to the editor: response from Drs. Foxman and Frerichs. Am J Public Health 76: 587.
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Members of the genera Alphavirus (family Togaviridae) and Flavivirus (family Flaviridae) are important zoonotic human and equine etiologic agents of neurologic diseases in the New World. In 2010, an outbreak of Madariaga virus (MADV; formerly eastern equine encephalitis virus) and Venezuelan equine encephalitis virus (VEEV) infections was reported in eastern Panamá. We further characterized the epidemiology of the outbreak by studying household contacts of confirmed human cases and of equine cases with neurological disease signs. Serum samples were screened using a hemagglutination inhibition test, and human results were confirmed using plaque reduction neutralization tests. A generalized linear model was used to evaluate the human MADV and VEEV seroprevalence ratios by age (in tercile) and gender. Overall, antibody prevalence for human MADV infection was 19.4%, VEEV 33.3%, and Mayaro virus 1.4%. In comparison with individuals aged 2–20 years, people from older age groups (21–41 and > 41 years) were five times more likely to have antibodies against VEEV, whereas the MADV prevalence ratio was independent of age. The overall seroprevalence of MADV in equids was 26.3%, VEEV 29.4%, West Nile virus (WNV) 2.6%, and St. Louis encephalitis virus (SLEV) was 63.0%. Taken together, our results suggest that multiple arboviruses are circulating in human and equine populations in Panamá. Our findings of a lack of increase in the seroprevalence ratio with age support the hypothesis of recent MADV exposure to people living in the affected region.
Financial support: This work was supported grants FID-09-103 from Secretaria Nacional de Ciencia y Tecnología Panamá to J-P. C.; US National Institutes of Health grants AI120942 and AI116030 to S. C. W. and T32 grant AI007536 support to A. Y. V., and neglected diseases grant 1.11.1.3.703.01.55.120, from the Ministry of Economy and Finance of Panamá to J. M. P. J. M. C. was also supported by Columbus University of Panamá, Research grant CU-VIP-P-003-2015.
Authors’ addresses: Jean-Paul Carrera, Department of Research in Virology and Biotechnology, Gorgas Memorial Institute of Health Studies, Panamá, Panamá, E-mail: jean1450@gmail.com. Karoun H. Bagamian, Environmental and Global Health and Emerging Pathogens Institute, University of Florida, Gainesville, FL, and Bagamian Scientific Consulting, LLC, Gainesville, FL, E-mail: karoun11@gmail.com. Amelia P. Travassos da Rosa, Robert B. Tesh, Eryu Wang, and Scott C. Weaver, Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, E-mails: aptravas@utmb.edu, rtesh@utmb.edu, erwang@utmb.edu, and sweaver@utmb.edu. Davis Beltran, Department of Virology and Biotechnology Research, Gorgas Memorial Institute of Health Studies, Panamá City, FL, and Department of Medical Entomology, Gorgas Memorial Institute of Health Studies, Panamá City, FL, E-mail: dbelt16@gmail.com. Nathan D. Gundaker, Division of Infectious Diseases, University of Alabama at Birmingham, Birmingham, AL, E-mail: ndgundacker@gmail.com. Blas Armien, Departamento de Investigacion de Enfermedades Emergentes y Zoonóticas, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panamá City, Panamá, E-mail: barmien@gorgas.gob.pa. Gianfranco Arroyo, Facultad de Salud Pública y Administración, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: arroyogianfranco@gmail.com. Néstor Sosa, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panamá City, Panamá, E-mail: drnsosa@gmail.com. Juan Miguel Pascale, Department of Microbiology, Gorgas Memorial Institute for Health Research, Panamá City, Panamá, E-mail: jmpascal@yahoo.com. Anayansi Valderrama, Department of Medical Entomology, Instituto Conmemorativo Gorgas de Estudios de la Salud, Panamá City, Panamá, and Universidad de Panamá, Panamá City, Panamá, E-mail: avalderrama@gorgas.gob.pa. Amy Y. Vittor, Emerging Pathogens Institute, University of Florida, Gainesville, FL, E-mail: amy.vittor@medicine.ufl.edu.
Smith DW, Mackenzie JS, Weaver SC, 2009. Alphaviruses. Richman DD, Whitley RJ, Hayden FG, eds. Clinical Virology. Washington, DC: ASM Press, 1241–1274.
Weaver SC, Winegar R, Manger ID, Forrester NL, 2012. Alphaviruses: population genetics and determinants of emergence. Antiviral Res 94: 242–257.
Lindenbach BD, Rice CM, 2007. Flaviviridae: the viruses and their replication. Fields Virol 2: 1101–1151.
Tesh RB et al. 1999. Mayaro virus disease: an emerging mosquito-borne zoonosis in tropical South America. Clin Infect Dis 28: 67–73.
Aguilar PV, Estrada-Franco JG, Navarro-Lopez R, Ferro C, Haddow AD, Weaver SC, 2011. Endemic Venezuelan equine encephalitis in the Americas: hidden under the dengue umbrella. Future Virol 6: 721–740.
Arrigo NC, Adams AP, Weaver SC, 2010. Evolutionary patterns of eastern equine encephalitis virus in North versus South America suggest ecological differences and taxonomic revision. J Virol 84: 1014–1025.
Carrera J-P et al. 2013. Eastern equine encephalitis in Latin America. N Engl J Med 369: 732–744.
Dietz WH, Galindo P, Johnson KM, 1980. Eastern equine encephalomyelitis in Panama: the epidemiology of the 1973 epizootic. Am J Trop Med Hyg 29: 133–140.
Sabattini MS, Daffner JF, Monath TP, Bianchi TI, Cropp CB, Mitchell CJ, Aviles G, 1991. Localized eastern equine encephalitis in Santiago del Estero Province, Argentina, without human infection. Medicina (B Aires) 51: 3–8.
Aguilar PV et al. 2007. Endemic eastern equine encephalitis in the Amazon region of Peru. Am J Trop Med Hyg 76: 293–298.
Johnson KM, Shelokov A, Peralta PH, Dammin GJ, Young NA, 1968. Recovery of Venezuelan equine encephalomyelitis virus in Panama. A fatal case in man. Am J Trop Med Hyg 17: 432–440.
Quiroz E, Aguilar PV, Cisneros J, Tesh RB, Weaver SC, 2009. Venezuelan equine encephalitis in Panama: fatal endemic disease and genetic diversity of etiologic viral strains. PLoS Negl Trop Dis 3: e472.
Vittor AY et al. 2016. Epidemiology of emergent Madariaga encephalitis in a region with endemic Venezuelan equine encephalitis: initial host studies and human cross-sectional study in Darien, Panama. PLoS Negl Trop Dis 10: e0004554.
Holdridge LRDG, 1956. Report on an ecological survey of the republic of Panama. Caribb For 17: 92–110.
Beaty BJ, Calisher CH, Shope RE, 1989. Arboviruses. Schmidt NJ, Emmons RW, eds. Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections. 6th edition. Washington, DC: American Public Health Association, 797–855.
Clarke DH, Casals J, 1958. Techniques for hemagglutinatination-inhibition with arthropod borned viruses. Am J Trop Med Hyg 7: 561–573.
Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE, 1989. Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70: 37–43.
Shope RE, 1963. The use of a micro-hemaglutination inhibition test to follow antibodie response after arthropod-borne virus infection in a community of forest animals. An Microbiol 11: 167–169 (Rio J).
Johnson BW, Kosoy O, Wang E, Delorey M, Russell B, Bowen RA, Weaver SC, 2011. Use of sindbis/eastern equine encephalitis chimeric viruses in plaque reduction neutralization tests for arboviral disease diagnostics. Clin Vaccin Immunol 18: 1486–1491.
Ni H, Yun NE, Zacks MA, Weaver SC, Tesh RB, Travassos Da Rosa AP, Powers AM, Frolov I, Paessler S, 2007. Recombinant alphaviruses are safe and useful serological diagnostic tools. Am J Trop Med Hyg 76: 774–781.
Weise WJ, Hermance ME, Forrester N, Adams AP, Langsjoen R, Gorchakov R, Wang E, Alcorn MDH, Tsetsarkin K, Weaver SC, 2014. A novel live-attenuated vaccine candidate for Mayaro fever. PLoS Negl Trop Dis 8: e2969.
Barros AJD, Hirakata VN, 2003. Alternatives for logistic regression in cross-sectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 3: 21.
Obaldía Nicanor et al. 1991. Encefalomielitis Equina del Este, Epizootia de 1986 en Panamá. Notas Vetrinarias 1: 4–7.
Bayly NJ, Gómez C, Cárdenas LC, 2011. Darién—Migration Monitoring during 2011 in the Tacarcuna Natural Reserve. Bogotá. Available at: https://avesmigratoriascolombia.wordpress.com/. Accessed April 23, 2018.
Bayly NJ, Ortiz LC, Rubio M, Gómez C, 2014. Migration of raptors, swallows and other diurnal migratory birds through the Darien of Colombia. Ornitol Neotrop 25: 63–71.
Goldfield M, Welsh JN, Taylor BF, 1968. The 1959 outbreak of eastern encephalitis in New Jersey. 5. The inapparent infection:disease ratio. Am J Epidemiol 87: 32–33.
Sunthorn S, Galindo P, 1967. The isolation of eastern equine encephalitis from Culex (Melanoconion) taeniopus Dyar and Knab in Panama. Mosq News 27: 74–76.
Galindo P, Srihongse S, De Rodaniche E, Grayson MA, 1966. An ecological survey for arboviruses in Almirante, Panama, 1959–1962. Am J Trop Med Hyg 15: 385–400.
Carrera J-P et al. 2017. Unusual pattern of chikungunya virus epidemic in the Americas, the Panamanian experience. PLoS Negl Trop Dis 11: e0005338.
Lednicky J et al. 2016. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerg Infect Dis 22: 2000–2002.
Nelson GC, Harris V, Stone SW, 2001. Deforestation, land use, and property rights: empirical evidence from Darien, Panama. Land Econ 77: 187–205.
Walton TE, Alvarez O Jr., Buckwalter RM, Johnson KM, 1973. Experimental infection of horses with enzootic and epizootic strains of Venezuelan equine encephalomyelitis virus. J Infect Dis 128: 271–282.
Monath TP, Sabattini MS, Pauli R, Daffner JF, Mitchell CJ, Bowen GS, Cropp CB, 1985. Arbovirus investigations in Argentina, 1977–1980. IV. Serologic surveys and sentinel equine program. Am J Trop Med Hyg 34: 966–975.
Pauvolid-Correa A, Tavares FN, Costa EV, Burlandy FM, Murta M, Pellegrin AO, Nogueira MF, Silva EE, 2010. Serologic evidence of the recent circulation of Saint Louis encephalitis virus and high prevalence of equine encephalitis viruses in horses in the Nhecolandia sub-region in south Pantanal, central-west Brazil. Mem Inst Oswaldo Cruz 105: 829–833.
Rodrigues SG, Oliva, O P, Francisco AAA, Martins LC, Chiang JO, Henriques DF, Pinto da Silva EV, Daniela SGR, Assis do, SCP, 2010. Epidemiology of Saint Louis encephalitis virus in the Brazilian Amazon region and in the State of Mato Grosso do Sul, Brazil: elevated prevalence of antibodies in horses. Rev Pan-Amazônica Saúde 1: 81–86.
Komar N, Clark GG, 2006. West Nile virus activity in Latin America and the Caribbean. Rev Panam Salud Publica 19: 112–117.
Tesh RB, Travassos da Rosa APA, Guzman H, Araujo TP, Xiao SY, 2002. Immunization with heterologous flaviviruses protective against fatal West Nile encephalitis. Emerg Infect Dis 8: 245–251.
Fleiss JL, 1986. Letters to the editor: confidence intervals vs significance tests: quantitative interpretation. Am J Public Health 76: 587.
Foxman B, Frerichs RR, 1986. Letters to the editor: response from Drs. Foxman and Frerichs. Am J Public Health 76: 587.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 59 | 59 | 11 |
Full Text Views | 1530 | 277 | 1 |
PDF Downloads | 292 | 52 | 0 |