Serologic Evidence of Zoonotic Alphaviruses in Humans from an Indigenous Community in the Peruvian Amazon

Jocelyn G. Pérez University of Liverpool, Liverpool, United Kingdom;

Search for other papers by Jocelyn G. Pérez in
Current site
Google Scholar
PubMed
Close
,
Jean-Paul Carrera Gorgas Memorial Institute of Health Studies, Panama City, Panama;

Search for other papers by Jean-Paul Carrera in
Current site
Google Scholar
PubMed
Close
,
Emmanuel Serrano Universitat Autònoma de Barcelona, Barcelona, Spain;
Universitá di Torino, Torino, Italy;

Search for other papers by Emmanuel Serrano in
Current site
Google Scholar
PubMed
Close
,
Yaneth Pittí Gorgas Memorial Institute of Health Studies, Panama City, Panama;

Search for other papers by Yaneth Pittí in
Current site
Google Scholar
PubMed
Close
,
Jorge L. Maguiña Universidad Peruana Cayetano Heredia, Lima, Peru;

Search for other papers by Jorge L. Maguiña in
Current site
Google Scholar
PubMed
Close
,
Gregorio Mentaberre Universitat Autònoma de Barcelona, Barcelona, Spain;
Universitat de Lleida, Lleida, Spain

Search for other papers by Gregorio Mentaberre in
Current site
Google Scholar
PubMed
Close
,
Andrés G. Lescano Universidad Peruana Cayetano Heredia, Lima, Peru;

Search for other papers by Andrés G. Lescano in
Current site
Google Scholar
PubMed
Close
,
Anayansi Valderrama Gorgas Memorial Institute of Health Studies, Panama City, Panama;

Search for other papers by Anayansi Valderrama in
Current site
Google Scholar
PubMed
Close
, and
Pedro Mayor Universitat Autònoma de Barcelona, Barcelona, Spain;

Search for other papers by Pedro Mayor in
Current site
Google Scholar
PubMed
Close
Restricted access

Alphaviruses (Togaviridae, Alphavirus) are arthropod-borne single-stranded RNA pathogens that cause febrile and neurologic disease in much of Latin America. However, many features of Alphavirus epidemiology remain unknown. In 2011, we undertook a cross-sectional study in Nueva Esperanza, an indigenous community in the Peruvian Amazon. Here, we present the first serologic evidence of Mayaro (MAYV), Venezuelan equine encephalitis (VEE) complex alphavirus, Una (UNAV), and Madariaga (MADV) viruses reported in humans (24%, 16%, 13%, and 1.5%, respectively) from an Amazonian indigenous community in Peru. Hunting activity and cohabiting with hunters were the main risk factors for Mayaro seroconversion, but only hunting was associated with UNAV seropositivity. Our results suggest that alphavirus infection in this region is common, but we highlight the high UNAV seroprevalence found and corroborate the low MADV prevalence reported in this region. Furthermore, MAYV-neutralizing antibodies were also detected in stored samples from wild animals (18%) hunted by Nueva Esperanza inhabitants and another mestizo community located close to Iquitos. Further serological surveys of VEE complex alphaviruses, UNAV, and MADV in wild animals and assessing the ability of the MAYV seropositive species to transmit the virus will be relevant.

    • Supplemental Materials (MS Word 60 KB)

Author Notes

Address correspondence to Jocelyn G. Pérez, University of Liverpool, 8 West Derby St., Liverpool L69 7BE, United Kingdom. E-mail: jgpl16@liverpool.ac.uk

Financial support: This research was supported by a grant from SENACYT FID 16-201 to J. P. C. and A. V., Secretaría Nacional de Ciencia y Tecnología from Panama; by the grant for neglected diseases studies in Panama 1.11.1.3.703.01.55.120 from the Ministry of Economy and Finance of Panama to J. P. C. and A. V.; and by ERANet17/HLH-0271. Scott Weaver also supported this study through the World Reference Center for Emerging Viruses and Arboviruses, NIH grant R24AI120942. Dr. Lescano is sponsored by the training grant D43 TW007393 awarded by the Fogarty International Center of the US National Institutes of Health. J. L. M. is a doctoral candidate studying an Epidemiological Research Doctorate at Universidad Peruana Cayetano Heredia under FONDECYT/CIENCIACTIVA scholarship EF033-235-2015 and also supported by training grant D43 TW007393. A. V. is a member of the Sistema Nacional de Investigación de Panamá (SNI), SENACYT. E. S. was supported by the Spanish Ministerio de Ciencia Innovación y Universidades (MICINN) through a Ramon y Cajal agreement (RYC-2016-21120).

Authors’ addresses: Jocelyn G. Pérez, University of Liverpool, Liverpool, United Kingdom, E-mail: jgpl16@liverpool.ac.uk. Jean-Paul Carrera, Yaneth Pittí, and Anayansi Valderrama, Gorgas Memorial Institute of Health Studies, Panama City, Panama, E-mails: jpcarrera@gorgas.gob.pa, ypitti@gorgas.gob.pa, and avalderrama@gorgas.gob.pa. Emmanuel Serrano, Universitat Autònoma de Barcelona, Barcelona, Spain and Universitá di Torino, Torino, Italy, E-mail: emmanuel.serrano@uab.cat. Jorge L. Maguiña and Andres G. Lescano, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: jorge.luis.maguina@upch.pe and willy.lescano@upch.pe. Gregorio Mentaberre, Universitat Autònoma de Barcelona, Barcelona, Spain and Universitat de Lleida, Lleida, Spain, E-mail: gregorio.mentaberre@uab.cat. Pedro Mayor, Universitat Autònoma de Barcelona, Barcelona, Spain, E-mail: mayorpedro@hotmail.com.

  • 1.

    Halsey ES, Siles C, Guevara C, Vilcarromero S, Jhonston EJ, Ramal C, Aguilar PV, Ampuero JS, 2013. Mayaro virus infection, Amazon basin region, Peru, 2010–2013. Emerg Infect Dis 19: 18391842.

    • Search Google Scholar
    • Export Citation
  • 2.

    Forshey BM et al. 2010. Arboviral etiologies of acute febrile illnesses in western South America, 2000–2007. PLoS Negl Trop Dis 4: e787.

  • 3.

    Neumayr A, Gabriel M, Fritz J, Gunther S, Hatz C, Schmidt-Chanasit J, Blum J, 2012. Mayaro virus infection in traveler returning from Amazon basin, northern Peru. Emerg Infect Dis 18: 695696.

    • Search Google Scholar
    • Export Citation
  • 4.

    Morrison AC et al. 2008. Venezuelan equine encephalitis virus in Iquitos, Peru: urban transmission of a sylvatic strain. PLoS Negl Trop Dis 2: e349.

    • Search Google Scholar
    • Export Citation
  • 5.

    Vilcarromero S et al. 2010. Venezuelan equine encephalitis and 2 human deaths, Peru. Emerg Infect Dis 16: 553556.

  • 6.

    Aguilar PV et al. 2007. Endemic eastern equine encephalitis in the Amazon region of Peru. Am J Trop Med Hyg 76: 293298.

  • 7.

    Luciani K, Abadía I, Martínez-Torres AO, Cisneros J, Guerra I, García M, Estripeaut D, Carrera JP, 2015. Case report: Madariaga virus infection associated with a case of acute disseminated encephalomyelitis. Am J Trop Med Hyg 92: 11301132.

    • Search Google Scholar
    • Export Citation
  • 8.

    Carrera JP et al. 2013. Eastern equine encephalitis in Latin America. N Engl J Med 369: 732744.

  • 9.

    Lednicky JA, White SK, Mavian CN, El Badry MA, Telisma T, Salemi M, Okech BA, Beau De Rochars VM, Morris JG Jr., 2019. Emergence of Madariaga virus as a cause of acute febrile illness in children, Haiti, 2015–2016. PLoS Negl Trop Dis 13: e0006972.

    • Search Google Scholar
    • Export Citation
  • 10.

    Blohm GM, Lednicky JA, White SK, Mavian CN, Márquez MC, González-García KP, Salemi M, Morris JG Jr., Paniz-Mondolfi AE, 2018. Madariaga virus: identification of a lineage III strain in a Venezuelan child with acute undifferentiated febrile illness, in the setting of a possible equine epizootic. Clin Infect Dis 67: 619621.

    • Search Google Scholar
    • Export Citation
  • 11.

    Turell MJ et al. 2005. Isolation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon basin region of Peru. J Med Entomol 42: 891898.

    • Search Google Scholar
    • Export Citation
  • 12.

    Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS, 2003. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo 45: 109110.

    • Search Google Scholar
    • Export Citation
  • 13.

    Palma-Pinedo H, Reyes-Vega MF, 2018. Barriers identified by the health staff for the screening of human immunodeficiency virus in indigenous populations of the peruvian amazon [article in Spanish]. Rev Peru Med Exp Salud Publica 35: 610619.

    • Search Google Scholar
    • Export Citation
  • 14.

    Izurieta RO, Macaluso M, Watts DM, Tesh RB, Guerra B, Cruz LM, Galwankar S, Vermund SH, 2011. Hunting in the rainforest and Mayaro virus infection: an emerging Alphavirus in Ecuador. J Glob Infect Dis 3: 317323.

    • Search Google Scholar
    • Export Citation
  • 15.

    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 Vaccine Immunol 18: 14861491.

    • Search Google Scholar
    • Export Citation
  • 16.

    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.

    • Search Google Scholar
    • Export Citation
  • 17.

    Lennette EH, Lennette DA, Lennette ET, 1995. Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections. Washington, DC: American Public Health Association.

    • Search Google Scholar
    • Export Citation
  • 18.

    Therneau T, Atkinson B, 2018. Rpart: Recursive Partitioning and Regression Trees. Available at: https://CRAN.R-project.org/package=rpart. R Package Version 4. 1–13.

  • 19.

    R Core team, 2019. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.

  • 20.

    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: 721740.

    • Search Google Scholar
    • Export Citation
  • 21.

    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: 10141025.

    • Search Google Scholar
    • Export Citation
  • 22.

    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.

    • Search Google Scholar
    • Export Citation
  • 23.

    Hoch AL, Peterson NE, LeDuc JW, Pinheiro FP, 1981. An outbreak of Mayaro virus disease in Belterra, Brazil. III. entomological and ecological studies. Am J Trop Med Hyg 30: 689698.

    • Search Google Scholar
    • Export Citation
  • 24.

    Auguste AJ et al. 2015. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerg Infect Dis 21: 17421750.

    • Search Google Scholar
    • Export Citation
  • 25.

    Schaeffer M, Gajdusek DC, Lema AB, Eichenwald H, 1959. Epidemic jungle fevers among Okinawan colonists in the Bolivian rain forest I. Epidemiology. Am J Trop Med Hyg 8: 372396.

    • Search Google Scholar
    • Export Citation
  • 26.

    LeDuc JW, Pinheiro FP, Travassos da Rosa AP, 1981. An outbreak of Mayaro virus disease in Belterra, Brazil. II. Epidemiology. Am J Trop Med Hyg 30: 682688.

    • Search Google Scholar
    • Export Citation
  • 27.

    Black FL et al. 1974. Evidence for persistence of infectious agents in isolated human populations. Am J Epidemiol 100: 230250.

  • 28.

    Talarmin A et al. 1998. Mayaro virus fever in French Guiana: isolation, identification, and seroprevalence. Am J Trop Med Hyg 59: 452456.

  • 29.

    Hotez PJ, Murray KO, 2017. Dengue, West Nile virus, Chikungunya, Zika-and now Mayaro? PLoS Negl Trop Dis 11: e0005462.

  • 30.

    Calisher CH, Gutierrez E, Maness KS, Lord RD, 1974. Isolation of Mayaro virus from a migrating bird captured in Louisiana in 1967. Bull Pan Am Health Organ 8: 243248.

    • Search Google Scholar
    • Export Citation
  • 31.

    de Thoisy B, Gardon J, Salas RA, Morvan J, Kazanji M, 2003. Mayaro virus in wild mammals, French Guiana. Emerg Infect Dis 9: 13261329.

  • 32.

    Batista PM, Andreotti R, Chiang JO, Ferreira MS, Vasconcelos PF, 2012. Seroepidemiological monitoring in sentinel animals and vectors as part of arbovirus surveillance in the state of Mato Grosso do Sul, Brazil. Rev Soc Bras Med Trop 45: 168173.

    • Search Google Scholar
    • Export Citation
  • 33.

    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
  • 34.

    Ramírez JE, Yanoviak SP, Lounibos LP, Weaver SC, 2007. Distribución vertical de Haemagogus janthinomys (dyar) (Diptera: Culicidae) en bosques de la AmazonÌa Peruana. Rev Peru Med Exp Salud publica 24: 4045.

    • Search Google Scholar
    • Export Citation
  • 35.

    Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, Tesh RB, 2011. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg 85: 750757.

    • Search Google Scholar
    • Export Citation
  • 36.

    Turell MJ, Sardelis MR, Jones JW, Watts DM, Fernandez R, Carbajal F, Pecor JE, Klein TA, 2008. Seasonal distribution, biology, and human attraction patterns of mosquitoes (Diptera: Culicidae) in a rural village and adjacent forested site near Iquitos, Peru. J Med Entomol 45: 11651172.

    • Search Google Scholar
    • Export Citation
  • 37.

    Brustolin M, Pujhari S, Henderson CA, Rasgon JL, 2018. Anopheles mosquitoes may drive invasion and transmission of Mayaro virus across geographically diverse regions. PLoS Negl Trop Dis 12: e0006895.

    • Search Google Scholar
    • Export Citation
  • 38.

    Cardozo F et al. 2018. Alphaviruses: serological evidence of human infection in Paraguay (2012–2013). Vector-Borne Zoonotic Dis 18:5, 266272.

    • Search Google Scholar
    • Export Citation
  • 39.

    Martins KA et al. 2019. Neutralizing antibodies from convalescent Chikungunya virus patients can cross-neutralize Mayaro and Una viruses. Am J Trop Med Hyg 100: 15411544.

    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 119 127 26
Full Text Views 2655 503 2
PDF Downloads 435 103 1
 
Membership Banner
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save