ABSTRACT

Objectives.

To assess the distribution of Mayaro virus (MAYV) in Latin America and the Caribbean and evaluate existing country-level MAYV surveillance mechanisms.

Methods.

Research was conducted from May 2018 through May 2019 to collect data from academic literature on Mayaro fever in Latin America and the Caribbean. PubMed, ClinicalKey, Scopus, Nature, SciELO, LILACS, and Google Scholar were searched for peer-reviewed journal articles, and data from health authorities, including the Pan American Health Organization (PAHO) and ministries of health, was also sought. MAYV-related publications published from 1954 through 2019 were screened. Publications that added to the overall understanding of MAYV, including its geographical and epidemiological distribution, were included in this report.

Results.

A total of 901 MAYV cases have been reported in humans in countries in Latin America and the Caribbean. Since its discovery in 1954 in Trinidad and Tobago, MAYV has been isolated from individuals living in Argentina, Bolivia, Brazil, Ecuador, French Guiana, Haiti, Mexico, Panama, Peru, and Venezuela. Of those 901 cases, 42 of them were reported exclusively by health authorities. In contrast, 843 confirmed and presumptive autochthonous cases and an additional 16 imported cases were identified in academic literature. No country-level surveillance mechanisms for MAYV were recorded in academic literature or by health authorities.

Conclusions.

This report demonstrates that MAYV surveillance efforts are limited in comparison to the virus’s presence in Latin America and the Caribbean, highlighting the importance of enhancing arboviral surveillance systems in the affected countries.

Keywords
Disease outbreaks; arboviruses; infection; Latin America; West Indies

RESUMEN

Objetivos.

Evaluar la distribución del virus Mayaro (MAYV) en América Latina y el Caribe y los mecanismos de vigilancia de nivel nacional.

Métodos.

Entre mayo de 2018 y mayo de 2019 se llevó a cabo una revisión bibliográfica sobre la fiebre de Mayaro en América Latina y el Caribe en las bases de datos PubMed, ClinicalKey, Scopus, Nature, SciELO, LILACS y Google Académico para identificar artículos en revistas arbitradas; también se revisó información suministrada por las autoridades sanitarias, entre ellas la Organización Panamericana de la Salud y los ministerios de salud. Se revisaron artículos relacionados con MAYV publicados entre 1954 y 2019. En este informe se incluyeron artículos que contribuyeran a la comprensión general sobre el MAYV, incluida su distribución geográfica y su epidemiología.

Resultados.

Se han reportado 901 casos de MAYV en seres humanos en 11 países de América Latina y el Caribe. Desde su descubrimiento en 1954 en Trinidad y Tobago, MAYV ha sido aislado de personas en Argentina, Bolivia, Brasil, Ecuador, Guayana Francesa, Haití, México, Panamá, Perú y Venezuela. De estos 901 casos, 42 fueron reportados exclusivamente por las autoridades sanitarias. A la vez, en la bibliografía se identificaron 844 casos autóctonos confirmados o presuntivos y 15 casos importados. A través de la bibliografía o las autoridades sanitarias no se identificaron mecanismos de vigilancia de nivel nacional para el MAYV.

Conclusiones.

En América Latina y el Caribe la vigilancia del MAYV es limitada en comparación con la presencia del virus en la región; es necesario mejorar los sistemas de vigilancia de arbovirus en los países afectados.

Palabras clave
Brotes de enfermedades; arbovirus; infección; América Latina; Indias Occidentales

RESUMO

Objetivo.

Analisar a distribuição do vírus Mayaro (MAYV) na América Latina e Caribe e avaliar os mecanismos nacionais de vigilância.

Métodos.

Dados da literatura acadêmica sobre a febre Mayaro na América Latina e Caribe foram coletados de maio de 2018 a maio de 2019. Foram pesquisadas as bases de dados PubMed, ClinicalKey, Scopus, Nature, SciELO, LILACS e Google Acadêmico para identificar artigos em revistas revisadas por pares; também foram examinados dados de autoridades sanitárias, incluindo a Organização Pan-Americana da Saúde (OPAS), e dos ministérios de saúde. Artigos relacionados com MAYV publicados de 1954 a 2019 foram revisados. Este relatório incluiu artigos que contribuíssem para o entendimento geral do MAYV, com informações sobre distribuição geográfica e epidemiologia.

Resultados.

Foram registrados 901 casos de MAYV em humanos em 11 países da América Latina e do Caribe. Desde a sua descoberta em 1954 em Trinidad e Tobago, o MAYV foi isolado em indivíduos na Argentina, Bolívia, Brasil, Equador, Guiana Francesa, Haiti, México, Panamá, Peru e Venezuela. Desses 901 casos, 42 foram comunicados exclusivamente pelas autoridades sanitárias. Por sua vez, 844 casos autóctones confirmados ou suspeitos e 15 casos importados foram descritos na literatura. Nenhum mecanismo nacional de vigilância do MAYV foi identificado na literatura ou pelas autoridades sanitárias.

Conclusões.

Na América Latina e Caribe, a vigilância do MAYV é limitada em contraste com a presença do vírus na região; é importante melhorar os sistemas de vigilância desse arbovírus nos países afetados.

Palavras-chave
Surtos de doenças; arbovírus; infecção; América Latina; Índias Ocidentais

Arboviral diseases share many common characteristics, making them difficult to discern from one another. However, due to changes in anthropogenic factors and viral mutations, arboviruses have the potential to emerge or reemerge throughout the Americas. In order to properly allocate resources and develop interventions to prevent the spread of arboviruses, it is important to make the diseases discernible from one another.

Mayaro virus (MAYV) is a positive-sense, enveloped, singlestranded RNA alphavirus classified in the Semliki Complex. MAYV is the etiological agent of Mayaro fever (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.). The Semliki Complex is made up of eight viruses of importance in the medical and veterinary fields: Bebaru, Chikungunya, Getah, Mayaro, O’nyong-nyong, Ross River, Semliki Forest, and Una (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.). Due to the fact that these eight viruses belong to the same serological complex, it is difficult to achieve an accurate diagnosis of the viruses outside of well-equipped laboratory settings (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.). Further, the virus is closely related to and cocirculates with Venezuelan equine encephalitis and Chikungunya viruses (²2. Smith JL PC, Cisney ED, et al. Human antibody responses to emerging Mayaro virus and cocirculating alphavirus infections examined by using structural proteins from nine New and Old World lineages. mSphere. 2018;3(2):e00003-18.).

MAYV is maintained in an enzootic cycle through continuous evolutions of transmission between diurnal mosquitoes from the forest canopy to nonhuman primates, rodents, marsupials, and birds (³3. Mackay IM, Arden KE. Mayaro virus: a forest virus primed for a trip to the city? Microbes Infect. 2016;18(12):724-34., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). Similar to the yellow fever virus life cycle, the transmission of MAYV to humans is believed to occur in the rural cycle, in which mosquitoes spread the virus to humans who live near to or make frequent use of forest habitats (⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). To date, human cases of Mayaro fever have mostly occurred due to accidental spillover from the sylvatic cycle (³3. Mackay IM, Arden KE. Mayaro virus: a forest virus primed for a trip to the city? Microbes Infect. 2016;18(12):724-34.).

Transmission of MAYV to humans primarily occurs by the bite of female mosquitoes from the Haemagogus genus in the dipteran family Culicidae, which are not known to be anthropophilic (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). In order to assess whether an urban cycle of MAYV could be initiated and sustained, laboratory experiments were conducted to assess the vector competence of anthropophilic mosquitoes (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁵5. Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, et al. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011;85(4):750-7.). Studies showed that MAYV can infect Aedes albopictus, but Aedes aegypti demonstrated limited opportunity for MAYV transmission to humans (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁵5. Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, et al. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011;85(4):750-7.); however, the vector competence of the species was demonstrated and suggests the potential for urban transmission (⁵5. Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, et al. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011;85(4):750-7.). MAYV-infected Ae. Aegypti and Culex quinquefasciatus have also been found in the city of Cuiabá, in the state of Mato Grosso, Brazil (⁶6. Serra OP, Cardoso BF, Ribeiro AL, Santos FA, Slhessarenko RD. Mayaro virus and dengue virus 1 and 4 natural infection in culicids from Cuiabá, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz. 2016;111(1):20-9.). MAYV was first isolated from Mansonia venezuelensis collected from the Rio Grande Forest in Trinidad and Tobago (⁵5. Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, et al. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011;85(4):750-7.). A small number of Psorophora ferox/albipes, Ae. (Ochlerotatus) serratus, Sabethes spp., Culex spp., and Haemagogus janthinomys have also contained isolates of the virus (⁵5. Long KC, Ziegler SA, Thangamani S, Hausser NL, Kochel TJ, Higgs S, et al. Experimental transmission of Mayaro virus by Aedes aegypti. Am J Trop Med Hyg. 2011;85(4):750-7.).

Further evidence of the virus’s potential to emerge in new areas was provided when sheep, caiman, and equids were sampled from 16 cattle ranches across the Pantanal region of Brazil from October 2009 through January 2011 (⁷7. Pauvolid-Corrêa A, Juliano RS, Campos Z, Velez J, Nogueira RM, Komar N. Neutralising antibodies for Mayaro virus in Pantanal, Brazil. Mem Inst Oswaldo Cruz. 2015;110(1):125-33.). Results from the study showed that 10 of the 748 equids were seropositive for MAYV, demonstrating the first evidence of MAYV circulation in the southern Pantanal. Since equids tested negative for MAYV in previous investigations, the authors of the study suggested that MAYV circulation in the Pantanal might be a recent occurrence. More research is needed to identify amplifier hosts and vectors, and to understand the ecology of the transmission of the virus (⁷7. Pauvolid-Corrêa A, Juliano RS, Campos Z, Velez J, Nogueira RM, Komar N. Neutralising antibodies for Mayaro virus in Pantanal, Brazil. Mem Inst Oswaldo Cruz. 2015;110(1):125-33.).

Clinical symptom of Mayaro fever tend to be nonspecific and include high-grade fever, debilitating arthralgia, headache, retro-orbital pain, myalgia, vomiting, diarrhea, and maculopapular rash (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9.). Similar to Chikungunya, MAYV infection can also lead to the development of long-term arthralgia (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9.). To date, no studies have shown whether individuals infected with MAYV can present as asymptomatic.

Due to the generic nature of the symptoms of alphaviruses, misdiagnosis can occur. Diagnosis of MAYV relies on clinical diagnosis, which may contribute to the misclassification of MAYV cases for dengue, Zika, Chikungunya, or other arboviruses (³3. Mackay IM, Arden KE. Mayaro virus: a forest virus primed for a trip to the city? Microbes Infect. 2016;18(12):724-34., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). The diagnostic procedures for MAYV include serological detection through the detection of antibodies in the host serum; molecular detection through reverse transcription polymerase chain reaction (RT-PCR); and viral isolation in a cell culture (⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). The reference standard for MAYV diagnosis is viral isolation (⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). Enzyme-immune assays, hemagglutination inhibition, immunofluorescence, or neutralization methods are useful serological methods for the detection of antibodies (⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). Diagnostic misdiagnoses can occur among viruses of the Alphavirus genus due to cross-reactivity among viruses with common antigenic sites (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.). Further, the short viremic period of MAYV may make it difficult to accurately isolate the virus from blood (⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.). As a result, the exact number of MAYV cases is difficult to determine in both clinical and serological detection outside of well-equipped laboratories (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.).

Disease prevention relies on vector control and personal protection measures (¹⁰10. Sakkas H BP, Franks A, Papadopoulou C. Oropouche fever: A review. Viruses. 2018;10(4).). Case management of MAYV relies solely on the treatment of symptoms with analgesics. Efforts to develop other control methods have been recorded. For example, the antiviral effects of thienopyridine derivatives have been evaluated and found to affect the late early and late stages of MAYV replication (¹¹11. Amorim R, de Meneses MDF, Borges JC, da Silva Pinheiro LC, Caldas LA, Cirne-Santos CC, et al. Thieno[2,3-b]pyridine derivatives: a new class of antiviral drugs against Mayaro virus. Arch Virol. 2017;162(6):1577-87.). One study demonstrated that these substances could potentially act as a new class of antiviral drugs due to their bioavailability and low cytotoxicity (¹¹11. Amorim R, de Meneses MDF, Borges JC, da Silva Pinheiro LC, Caldas LA, Cirne-Santos CC, et al. Thieno[2,3-b]pyridine derivatives: a new class of antiviral drugs against Mayaro virus. Arch Virol. 2017;162(6):1577-87.). A live-attenuated vaccine against MAYV has also been developed. The vaccine was found to protect against lethal challenge in murine models, was highly immunogenic, and noninfectious to mosquitoes, but still required further preclinical development (¹²12. Weise WJ, Hermance ME, Forrester N, Adams AP, Langsjoen R, Gorchakov R, et al. A novel live-attenuated vaccine candidate for mayaro Fever. PLoS Negl Trop Dis. 2014;8(8):e2969.). A synthetic DNA envelope vaccine has also been evaluated in mice (¹³13. Choi H, Kudchodkar SB, Reuschel EL, Asija K, Borole P, Ho M, et al. Protective immunity by an engineered DNA vaccine for Mayaro virus. PLoS Negl Trop Dis. 2019;13(2):e0007042.). T cell immunity and antibody immune responses were induced by the vaccine, and mice challenged with live MAYV after receiving the vaccine were protected against the disease (¹³13. Choi H, Kudchodkar SB, Reuschel EL, Asija K, Borole P, Ho M, et al. Protective immunity by an engineered DNA vaccine for Mayaro virus. PLoS Negl Trop Dis. 2019;13(2):e0007042.). Despite these developments, licensed vaccinations and antiretroviral therapy are not currently available for MAYV (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22.).

The objectives of this report were to assess the presence of MAYV in Latin America and the Caribbean while simultaneously evaluating country-level MAYV surveillance efforts in Latin American and Caribbean countries.

MATERIALS AND METHODS

In order to assess the presence of Mayaro fever in Latin America and the Caribbean, databases that included PubMed, ClinicalKey, Scopus, Nature, SciELO, LILACS, and Google Scholar were searched periodically from May 2018 through May 2019. Materials in French, Spanish, Portuguese, and English were reviewed. The terms used and adapted to each database were “Mayaro fever,” “Mayaro virus,” “MAYV,” “Mayaro,” “Mayaro AND alphavirus,” “Mayaro AND Semliki Complex,” and “Mayaro AND epidemiology.” In PubMed, 90 articles were identified for the search term “Mayaro fever,” 221 articles for “Mayaro virus,” 79 articles for “MAYV,” 227 articles for “Mayaro,” 158 articles for “Mayaro AND alphavirus,” 9 articles for “Mayaro AND Semliki Complex,” and 71 articles for “Mayaro AND epidemiology.” (The other databases did not generate new, unique journal-article hits that were not in PubMed. Therefore, from this point forward, this report will discuss the journal-article hits only from PubMed.)

In addition, health authorities were consulted to obtain outbreak data. Also, the archives of the Pan American Health Organization were examined, and epidemiological bulletins were investigated on the ministry of health websites of countries with a reported presence of Mayaro (Argentina, Bolivia, Brazil, Ecuador, French Guiana, Haiti, Mexico, Panama, Peru, Suriname, Trinidad and Tobago, and Venezuela). Lastly, references listed in academic articles and health authority reports were manually examined to further identify MAYV data for this report.

We included in our analysis journal articles and other publications that were published between 1954 and 2019 and that provided a historical overview of Mayaro, hosts, transmission mechanisms of the virus, clinical manifestation, geographical distribution and epidemiology of the disease, diagnostic methods, case management, surveillance efforts, known risk factors, and prevention and control techniques. Studies were excluded from the report if they were unable to add to the overall understanding of MAYV in Latin America and the Caribbean, including studies that were too broad or too heavily focused on the microbiological and virological components of MAYV or did not contribute data to the analysis.

RESULTS

Periodic searches were carried out between May 2018 and May 2019 to assess the distribution of Mayaro fever in Latin America and the Caribbean. The study flow diagram, including with the PubMed searching, is given in Figure 1.

In this special report, 50 publications were included in the analysis and 41 were excluded. Of those 50 included publications, 49 of them were journal articles and the other was a health authority alert issued by the Pan American Health Organization (PAHO) in May of 2019.

As shown in Figure 2 and Table 1, MAYV cases have been found in Latin America and the Caribbean, with the highest number of cases occurring in Brazil and Peru. Of the 901 reported cases of MAYV, approximately 843 confirmed and presumptive autochthonous cases and 16 imported cases were identified in academic literature, and the remaining 42 cases were reported exclusively by a health authority (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22., ⁸8. Azevedo RSS SE, Carvalho VL, et al. Mayaro fever virus, Brazilian Amazon. Emerging Infectious Diseases. 2009;15(11):1830-2., ¹⁴14. Auguste AJ LJ, Forrester NL, et al. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases. 2015;21(10):1742-50.

15. SCHMIDT JR, GAJDUSEK DC, SCHAFFER M, GORRIE RH. Epidemic jungle fever among Okinawan colonists in the Bolivian rain forest. II. Isolation and characterization of Uruma virus, a newly recognized human pathogen. Am J Trop Med Hyg. 1959;8(4):479-87.

16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.

17. LeDuc JW, Pinheiro FP, Travassos da Rosa AP. An outbreak of Mayaro virus disease in Belterra, Brazil. II. Epidemiology. Am J Trop Med Hyg. 1981;30(3):682-8.

18. Terzian AC, Auguste AJ, Vedovello D, Ferreira MU, da Silva-Nunes M, Sperança MA, et al. Isolation and characterization of Mayaro virus from a human in Acre, Brazil. Am J Trop Med Hyg. 2015;92(2):401-4.

19. Munoz M NJ. Virus Mayaro: Un arbovirus reemergente en Vene-zuela y Latinoamerica. Biomedica. 2012;32:286-302.

20. Pinheiro FP, Bensabath G, Rosa APAT, Lainson R, Shaw JJ, Ward R, et al. Public health hazards among workers along the trans-Amazon highway. Journal of Occupational Medicine. 1977;19:490-7.

21. Tavares-Neto J, Freitas-Carvalho J, Teixeira Nunes MR, Rocha G, Guerreiro Rodrigues S, Damasceno E, et al. Pesquisa de anticorpos contra arbovirus e o virus vacinal da febre amarela em uma amostra da populacao de Rio Branco, antes a tres meses apos a vacina 17D. Revista da Sociedada Brasileira de Medicina Tropical. 2004;37:1-6.

22. Cruz ACR, Correa dos Prazeres AdS, Colares Gama E, Furtado da Lima M, Silva Azevedo RdS, Neves Casseb LM, et al. Vigilancia sorologica para arbovirus em Juruti, Para, Brasil. Cad Saude Publica. 2009;25(11):2517-23.

23. Zuchi N, Borges da Silva Heinen L, Mendes dos Santos MA, Pereira FC, Dezengrini Slhessarenko R. Molecular detection of Mayaro virus during a dengue outbreak in the state of Mato Grosso, Central-West Brazil. Mem Inst Oswaldo Cruz. 2014;109(6):820-3.

24. Nunes MR, Barbosa TF, Casseb LM, Nunes Neto JP, Segura NeO, Monteiro HA, et al. [Arbovirus eco-epidemiology in the area affected by the Cuiabá-Santarém Highway (BR-163), Pará State, Brazil]. Cad Saude Publica. 2009;25(12):2583-602.

25. Talarmin A CL, Kazanji M, et al. Mayaro virus fever in French Guiana: Isolation, identification, and seroprevalence. American Journal of Tropical Medical Hygiene. 1998;59(3):452-6.

26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.

27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.

28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73.

29. Halsey ES, Siles C, Guevara C, Vilcarromero S, Jhonston EJ, Ramal C, et al. Mayaro virus infection, Amazon Basin region, Peru, 2010-2013. Emerg Infect Dis. 2013;19(11):1839-42.

30. Torres JR, Russell KL, Vasquez C, Barrera R, Tesh RB, Salas R, et al. Family cluster of Mayaro fever, Venezuela. Emerg Infect Dis. 2004;10(7):1304-6.

31. Travassos da Rosa JF MdSW, Pinheiro FP, et al. Oropouche virus: Clinical, epidemiological, and molecular aspects of a neglected Orthobunyavirus. American Journal of Tropical Medical Hygiene. 2017;96(5):1019-30.

32. Coimbra TL, Santos CL, Suzuki A, Petrella SM, Bisordi I, Nagamori AH, et al. Mayaro virus: imported cases of human infection in São Paulo State, Brazil. Rev Inst Med Trop Sao Paulo. 2007;49(4):221-4.

33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.

34. Pinto De Figueiredo RM, Dutary Thatcher B, Lira de Lima M, Carvalho Almeida T, Duarte Alecrim W, Vinitius de Farias Guerra M. Doenças exantemáticas e primeira epidemia de dengue ocorrida em Manaus, Amazonas, no período de 1998-1999. Revista da Sociedade Brasileira de Medicina Tropical. 2004;37(6):476-9.

35. Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo. 2003;45(2):109-10.

36. Estudio Interinstitucional Desarrollado Por Las Instituciones Del Ministerio de Salud Del Perú, en colaboración con el Instituto de Investigación de Enfermedades Tropicales de la Marina de los Estados Unidos, La Universidad Nacional Mayor de San Marcos, & La Universidad Peruana Cayetano Heredia. Perfil etiológico del síndrome febril en áreas de alto riesgo de transmisión de enfermedades infecciosas de impacto en salud pública en el Perú, 2000-2001. 2005.-³⁷37. Anderson CR, Downs WG, Wattley GH, Ahin NW, Reese AA. Mayaro virus: a new human disease agent. II. Isolation from blood of patients in Trinidad, B.W.I. Am J Trop Med Hyg. 1957;6(6):1012-6.). Epidemiological bulletins from the ministries of health in Argentina, Bolivia, Brazil, Ecuador, French Guiana, Haiti, Mexico, Panama, Peru, Suriname, Trinidad and Tobago, and Venezuela made no mention of the presence of Mayaro.

Table 2 includes a descriptive overview of reported confirmed and presumptive cases of Mayaro, as well as the publications in which these cases were identified. The table provides information on the number of cases reported in an article, the lead author of the article in which the case(s) were reported, the country the case(s) originated in, the year the case(s) occurred, and the diagnostic procedure used to confirm the case(s).

The lack of standardization in Mayaro case definitions and laboratory diagnostics weaken the robustness of reported case data; however, the data was incorporated in this report due to the limited availability of MAYV case data to create the first epidemiological database for Mayaro. To date, epidemiological data on Mayaro continues to be descriptive in nature. Given the lack of accurate and consistent case information, incidence rate calculations were not attempted. Rather, an overview of the number of reported cases and/or epidemics of MAYV was given. Data on MAYV mortality was extremely limited. Of the 901 reported MAYV cases, only one fatality was recorded in academic literature (²⁷27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.). Lastly, MAYV attack rates were not available in the existing literature.

Argentina

Three cases of Una virus (UNAV), a subtype of Mayaro, were discovered in the sera of three individuals from central Argentina in 2001 (³⁵35. Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo. 2003;45(2):109-10.). Due to the low titers of neutralizing antibodies detected, it was difficult to ascertain when the individuals became infected with UNAV; nonetheless, the circulation of UNAV in Argentina was demonstrated (³⁵35. Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo. 2003;45(2):109-10.).

Bolivia

A total of 60 cases were identified from 1955 through 2007 in Bolivia. In the first instance, Uruma virus, now considered to be a strain of Mayaro, was isolated from the blood of two febrile Okinawan colonists in 1955 (¹⁵15. SCHMIDT JR, GAJDUSEK DC, SCHAFFER M, GORRIE RH. Epidemic jungle fever among Okinawan colonists in the Bolivian rain forest. II. Isolation and characterization of Uruma virus, a newly recognized human pathogen. Am J Trop Med Hyg. 1959;8(4):479-87.). Another article reported that 12 cases of MAYV were found in 2007, but no further information was provided about the cases (¹⁴14. Auguste AJ LJ, Forrester NL, et al. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases. 2015;21(10):1742-50.). The remaining 46 MAYV cases in Bolivia were identified from 2000 to 2007 in a study done in three departments of the country (¹⁶16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.).

Brazil

The country with the highest number of recorded MAYV cases in the Americas is Brazil. Of a total of 495 cases, 199 of them were identified in the state of Goiás, and 194 took place in the state of Pará. Cases were also identified in the states of Acre, Amazonas, and Mato Grosso and the city of São Paulo. The virus is considered to be endemic in the northern, western, and central portions of the country (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4.).

Ecuador

The first case of MAYV in Ecuador was identified during a study that took place from 2000 to 2007 (¹⁶16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.). The patient lived in the city of Guayaquil, in the province of Guayas (¹⁶16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.). In May of 2019 an epidemiological bulletin released by PAHO reported that an additional five cases of Mayaro were detected in Ecuador (³⁸38. Epidemiological Alert: Mayaro Fever: Pan American Health Organization; 2019 [Available from: https://www.paho.org/hq/index.php?option=com_docman&view=download&category_slug=mayaro-fever-2323&alias=48374-1-may-201 9-mayaro-fever-epidemiological-alert&Itemid=270⟨=en.
https://www.paho.org/hq/index.php?option... ). These cases were identified in samples that tested negative for leptospirosis, dengue, Chikungunya, and Zika (³⁸38. Epidemiological Alert: Mayaro Fever: Pan American Health Organization; 2019 [Available from: https://www.paho.org/hq/index.php?option=com_docman&view=download&category_slug=mayaro-fever-2323&alias=48374-1-may-201 9-mayaro-fever-epidemiological-alert&Itemid=270⟨=en.
https://www.paho.org/hq/index.php?option... ) and that had originated from individuals in the cities of Guayaquil, Babahoyo, Portoviejo, and Santo Domingo (³⁸38. Epidemiological Alert: Mayaro Fever: Pan American Health Organization; 2019 [Available from: https://www.paho.org/hq/index.php?option=com_docman&view=download&category_slug=mayaro-fever-2323&alias=48374-1-may-201 9-mayaro-fever-epidemiological-alert&Itemid=270⟨=en.
https://www.paho.org/hq/index.php?option... ).

French Guiana

The first case of MAYV in French Guiana was identified in 1996 (²⁵25. Talarmin A CL, Kazanji M, et al. Mayaro virus fever in French Guiana: Isolation, identification, and seroprevalence. American Journal of Tropical Medical Hygiene. 1998;59(3):452-6.). The patient was a female who had been living in French Guiana for several months and had presented with symptoms for two days (²⁵25. Talarmin A CL, Kazanji M, et al. Mayaro virus fever in French Guiana: Isolation, identification, and seroprevalence. American Journal of Tropical Medical Hygiene. 1998;59(3):452-6.).

Haiti

Only one case of MAYV has been recorded in Haiti. In 2015, an eight-year-old boy from a rural/semirural area of the Ouest department presented febrile symptoms and tested positive for MAYV (²⁶26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.). This case demonstrates an instance where the ecological settings that precipitated the emergence of this case differed from the sylvan Amazon regions where MAYV infections have generally occurred (²⁶26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.).

Mexico

A total of two cases of MAYV have been found in Mexico. These cases were identified in 2001, when 35 patients at the Mexican Institute of Social Security in the state of Veracruz underwent testing for MAYV (²⁷27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.). Two of the patients tested positive for the virus and displayed symptoms characteristic of hemorrhagic cases (²⁷27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.). Of the two cases, one patient died (²⁷27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.). This has been the only recorded case of fatality due to MAYV (²⁷27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.).

Panama

One case of MAYV was detected in a study carried out from 1966 through 1967 (³³33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.). In this instance, a citizen of the United States of America who was conducting studies assessing the feasibility of routes for a new, sea-level canal in Panama or Colombia demonstrated a significant rise in viral MAYV antibodies (³³33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.). Unfortunately, due to study group cross-over, it was unclear whether the virus was acquired in Panama or Colombia (³³33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.).

Peru

Peru had the second-largest number of reported cases. A total of 230 cases were identified, with the highest number reported in the region of Loreto. Mayaro was also recorded in the regions of Madre de Dios, Junín, Cusco, Huánuco, Ucayali, San Martín, Tumbes, and Ayacucho.

Trinidad and Tobago

Trinidad and Tobago was the location where MAYV was first isolated, from blood samples from one urban-dwelling female and four male forest workers (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ³⁷37. Anderson CR, Downs WG, Wattley GH, Ahin NW, Reese AA. Mayaro virus: a new human disease agent. II. Isolation from blood of patients in Trinidad, B.W.I. Am J Trop Med Hyg. 1957;6(6):1012-6.). Since the virus was first discovered in the county of Mayaro, it was subsequently named for that area.

Venezuela

There have only been two recorded instances of MAYV infection in Venezuela. In 2000, MAYV was identified in a family of four in the Barlovento subregion of the state of Miranda (³⁰30. Torres JR, Russell KL, Vasquez C, Barrera R, Tesh RB, Salas R, et al. Family cluster of Mayaro fever, Venezuela. Emerg Infect Dis. 2004;10(7):1304-6.). The second instance of MAYV was in the village of La Estación, where 77 cases were reported, of which 19 of them were confirmed as being seropositive (¹⁴14. Auguste AJ LJ, Forrester NL, et al. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases. 2015;21(10):1742-50.).

Imported cases

A total of 15 imported cases of Mayaro have been reported in the academic literature (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9., ²⁸28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73., ³⁹39. Llagonne-Barets M IV, Leparc-Goffart I, Prat C, Perpoint T, Andre P, Ramiere C. A case of Mayaro virus infection imported from French Guiana. Journal of Clinical Virology. 2016;77(66-68):66.

40. Tappe D, Pérez-Girón JV, Just-Nübling G, Schuster G, Gómez-Medina S, Günther S, et al. Sustained Elevated Cytokine Levels during Recovery Phase of Mayaro Virus Infection. Emerg Infect Dis. 2016;22(4):750-2.

41. Hassing RJ, Leparc-Goffart I, Blank SN, Thevarayan S, Tolou H, van Doornum G, et al. Imported Mayaro virus infection in the Netherlands. J Infect. 2010;61(4):343-5.

42. Friedrich-Jânicke B, Emmerich P, Tappe D, Günther S, Cadar D, Schmidt-Chanasit J. Genome analysis of Mayaro virus imported to Germany from French Guiana. Emerg Infect Dis. 2014;20(7):1255-7.

43. Neumayr A, Gabriel M, Fritz J, Günther S, Hatz C, Schmidt-Chanasit J, et al. Mayaro virus infection in traveler returning from Amazon Basin, northern Peru. Emerg Infect Dis. 2012;18(4):695-6.

44. Theilacker C, Held J, Allering L, Emmerich P, Schmidt-Chanasit J, Kern WV, et al. Prolonged polyarthralgia in a German traveller with Mayaro virus infection without inflammatory correlates. BMC Infect Dis. 2013;13:369.-⁴⁵45. Receveur MC, Grandadam M, Pistone T, Malvy D. Infection with Mayaro virus in a French traveller returning from the Amazon region, Brazil, January, 2010. Euro Surveill. 2010;15(18).). These cases impacted individuals from Canada, France, Germany, the Netherlands, Switzerland, and unidentified parts of North America. The patients had acquired MAYV during travel in Bolivia, Brazil, Ecuador, French Guiana, Peru, and Suriname (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9., ²⁸28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73., ³⁹39. Llagonne-Barets M IV, Leparc-Goffart I, Prat C, Perpoint T, Andre P, Ramiere C. A case of Mayaro virus infection imported from French Guiana. Journal of Clinical Virology. 2016;77(66-68):66.

40. Tappe D, Pérez-Girón JV, Just-Nübling G, Schuster G, Gómez-Medina S, Günther S, et al. Sustained Elevated Cytokine Levels during Recovery Phase of Mayaro Virus Infection. Emerg Infect Dis. 2016;22(4):750-2.

41. Hassing RJ, Leparc-Goffart I, Blank SN, Thevarayan S, Tolou H, van Doornum G, et al. Imported Mayaro virus infection in the Netherlands. J Infect. 2010;61(4):343-5.

42. Friedrich-Jânicke B, Emmerich P, Tappe D, Günther S, Cadar D, Schmidt-Chanasit J. Genome analysis of Mayaro virus imported to Germany from French Guiana. Emerg Infect Dis. 2014;20(7):1255-7.

43. Neumayr A, Gabriel M, Fritz J, Günther S, Hatz C, Schmidt-Chanasit J, et al. Mayaro virus infection in traveler returning from Amazon Basin, northern Peru. Emerg Infect Dis. 2012;18(4):695-6.

44. Theilacker C, Held J, Allering L, Emmerich P, Schmidt-Chanasit J, Kern WV, et al. Prolonged polyarthralgia in a German traveller with Mayaro virus infection without inflammatory correlates. BMC Infect Dis. 2013;13:369.-⁴⁵45. Receveur MC, Grandadam M, Pistone T, Malvy D. Infection with Mayaro virus in a French traveller returning from the Amazon region, Brazil, January, 2010. Euro Surveill. 2010;15(18).).

Mayaro virus surveillance efforts

To date, no standardized case definitions or laboratory diagnosis algorithms have been recorded for Mayaro fever at the regional or country levels in Latin America and the Caribbean. Similarly, information on country-level MAYV surveillance efforts in Latin America and the Caribbean were not available in academic literature or from health authorities. However, many of the cases reported in academic literature came about from the differential diagnosis of sera that were negative for other, more well-known arboviral diseases (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ¹⁸18. Terzian AC, Auguste AJ, Vedovello D, Ferreira MU, da Silva-Nunes M, Sperança MA, et al. Isolation and characterization of Mayaro virus from a human in Acre, Brazil. Am J Trop Med Hyg. 2015;92(2):401-4., ²¹21. Tavares-Neto J, Freitas-Carvalho J, Teixeira Nunes MR, Rocha G, Guerreiro Rodrigues S, Damasceno E, et al. Pesquisa de anticorpos contra arbovirus e o virus vacinal da febre amarela em uma amostra da populacao de Rio Branco, antes a tres meses apos a vacina 17D. Revista da Sociedada Brasileira de Medicina Tropical. 2004;37:1-6.

22. Cruz ACR, Correa dos Prazeres AdS, Colares Gama E, Furtado da Lima M, Silva Azevedo RdS, Neves Casseb LM, et al. Vigilancia sorologica para arbovirus em Juruti, Para, Brasil. Cad Saude Publica. 2009;25(11):2517-23.-²³23. Zuchi N, Borges da Silva Heinen L, Mendes dos Santos MA, Pereira FC, Dezengrini Slhessarenko R. Molecular detection of Mayaro virus during a dengue outbreak in the state of Mato Grosso, Central-West Brazil. Mem Inst Oswaldo Cruz. 2014;109(6):820-3., ²⁶26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2., ³⁴34. Pinto De Figueiredo RM, Dutary Thatcher B, Lira de Lima M, Carvalho Almeida T, Duarte Alecrim W, Vinitius de Farias Guerra M. Doenças exantemáticas e primeira epidemia de dengue ocorrida em Manaus, Amazonas, no período de 1998-1999. Revista da Sociedade Brasileira de Medicina Tropical. 2004;37(6):476-9., ³⁹39. Llagonne-Barets M IV, Leparc-Goffart I, Prat C, Perpoint T, Andre P, Ramiere C. A case of Mayaro virus infection imported from French Guiana. Journal of Clinical Virology. 2016;77(66-68):66., ⁴²42. Friedrich-Jânicke B, Emmerich P, Tappe D, Günther S, Cadar D, Schmidt-Chanasit J. Genome analysis of Mayaro virus imported to Germany from French Guiana. Emerg Infect Dis. 2014;20(7):1255-7., ⁴⁶46. Vieira CJ, Silva DJ, Barreto ES, Siqueira CE, Colombo TE, Ozanic K, et al. Detection of Mayaro virus infections during a dengue outbreak in Mato Grosso, Brazil. Acta Trop. 2015;147:12-6.

47. Estofolete CF, Tasso Oliveira Mota M, Vedovello D, Vinha Nunes de Gongora D, Maia IL, Lacerda Nogueira M. Mayaro fever in an HIV-infected patient suspected of having Chikungunya fever. 2016;49(5):648-52.-⁴⁸48. Brunini S, França DDS, Silva JB, Silva LN, Silva FPA, Spadoni M, et al. High Frequency of Mayaro Virus IgM among Febrile Patients, Central Brazil. Emerg Infect Dis. 2017;23(6):1025-6.).

DISCUSSION

MAYV was first isolated in 1954 in Trinidad and Tobago and has since been reported in Central and South America, circulating through high-density tropical forests (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22., ⁸8. Azevedo RSS SE, Carvalho VL, et al. Mayaro fever virus, Brazilian Amazon. Emerging Infectious Diseases. 2009;15(11):1830-2., ¹⁴14. Auguste AJ LJ, Forrester NL, et al. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases. 2015;21(10):1742-50.

15. SCHMIDT JR, GAJDUSEK DC, SCHAFFER M, GORRIE RH. Epidemic jungle fever among Okinawan colonists in the Bolivian rain forest. II. Isolation and characterization of Uruma virus, a newly recognized human pathogen. Am J Trop Med Hyg. 1959;8(4):479-87.

16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.

17. LeDuc JW, Pinheiro FP, Travassos da Rosa AP. An outbreak of Mayaro virus disease in Belterra, Brazil. II. Epidemiology. Am J Trop Med Hyg. 1981;30(3):682-8.

18. Terzian AC, Auguste AJ, Vedovello D, Ferreira MU, da Silva-Nunes M, Sperança MA, et al. Isolation and characterization of Mayaro virus from a human in Acre, Brazil. Am J Trop Med Hyg. 2015;92(2):401-4.

19. Munoz M NJ. Virus Mayaro: Un arbovirus reemergente en Vene-zuela y Latinoamerica. Biomedica. 2012;32:286-302.

20. Pinheiro FP, Bensabath G, Rosa APAT, Lainson R, Shaw JJ, Ward R, et al. Public health hazards among workers along the trans-Amazon highway. Journal of Occupational Medicine. 1977;19:490-7.

21. Tavares-Neto J, Freitas-Carvalho J, Teixeira Nunes MR, Rocha G, Guerreiro Rodrigues S, Damasceno E, et al. Pesquisa de anticorpos contra arbovirus e o virus vacinal da febre amarela em uma amostra da populacao de Rio Branco, antes a tres meses apos a vacina 17D. Revista da Sociedada Brasileira de Medicina Tropical. 2004;37:1-6.

22. Cruz ACR, Correa dos Prazeres AdS, Colares Gama E, Furtado da Lima M, Silva Azevedo RdS, Neves Casseb LM, et al. Vigilancia sorologica para arbovirus em Juruti, Para, Brasil. Cad Saude Publica. 2009;25(11):2517-23.

23. Zuchi N, Borges da Silva Heinen L, Mendes dos Santos MA, Pereira FC, Dezengrini Slhessarenko R. Molecular detection of Mayaro virus during a dengue outbreak in the state of Mato Grosso, Central-West Brazil. Mem Inst Oswaldo Cruz. 2014;109(6):820-3.

24. Nunes MR, Barbosa TF, Casseb LM, Nunes Neto JP, Segura NeO, Monteiro HA, et al. [Arbovirus eco-epidemiology in the area affected by the Cuiabá-Santarém Highway (BR-163), Pará State, Brazil]. Cad Saude Publica. 2009;25(12):2583-602.

25. Talarmin A CL, Kazanji M, et al. Mayaro virus fever in French Guiana: Isolation, identification, and seroprevalence. American Journal of Tropical Medical Hygiene. 1998;59(3):452-6.

26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.

27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.

28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73.

29. Halsey ES, Siles C, Guevara C, Vilcarromero S, Jhonston EJ, Ramal C, et al. Mayaro virus infection, Amazon Basin region, Peru, 2010-2013. Emerg Infect Dis. 2013;19(11):1839-42.

30. Torres JR, Russell KL, Vasquez C, Barrera R, Tesh RB, Salas R, et al. Family cluster of Mayaro fever, Venezuela. Emerg Infect Dis. 2004;10(7):1304-6.

31. Travassos da Rosa JF MdSW, Pinheiro FP, et al. Oropouche virus: Clinical, epidemiological, and molecular aspects of a neglected Orthobunyavirus. American Journal of Tropical Medical Hygiene. 2017;96(5):1019-30.

32. Coimbra TL, Santos CL, Suzuki A, Petrella SM, Bisordi I, Nagamori AH, et al. Mayaro virus: imported cases of human infection in São Paulo State, Brazil. Rev Inst Med Trop Sao Paulo. 2007;49(4):221-4.

33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.

34. Pinto De Figueiredo RM, Dutary Thatcher B, Lira de Lima M, Carvalho Almeida T, Duarte Alecrim W, Vinitius de Farias Guerra M. Doenças exantemáticas e primeira epidemia de dengue ocorrida em Manaus, Amazonas, no período de 1998-1999. Revista da Sociedade Brasileira de Medicina Tropical. 2004;37(6):476-9.

35. Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo. 2003;45(2):109-10.

36. Estudio Interinstitucional Desarrollado Por Las Instituciones Del Ministerio de Salud Del Perú, en colaboración con el Instituto de Investigación de Enfermedades Tropicales de la Marina de los Estados Unidos, La Universidad Nacional Mayor de San Marcos, & La Universidad Peruana Cayetano Heredia. Perfil etiológico del síndrome febril en áreas de alto riesgo de transmisión de enfermedades infecciosas de impacto en salud pública en el Perú, 2000-2001. 2005.-³⁷37. Anderson CR, Downs WG, Wattley GH, Ahin NW, Reese AA. Mayaro virus: a new human disease agent. II. Isolation from blood of patients in Trinidad, B.W.I. Am J Trop Med Hyg. 1957;6(6):1012-6.). A total of 901 MAYV cases have been reported in 10 Latin American countries and 1 Caribbean country. Of these 901 cases, 843 autochthonous and 16 imported cases were reported in academic literature, and the remaining 42 cases were exclusively reported by health authorities (¹1. Alves Esposito DL LdFB. Will Mayaro virus be responsible for the next outbreak of an arthopod-borne virus in Brazil. The Brazilian Journal of Infectious Diseases. 2017;21(5):540-4., ⁴4. Mota MTdO, Ribeiro MR, Vedovello D, Nogueira ML. Mayaro virus: A neglected arbovirus of the Americas. Future Virology. 2015;10(9):1109-22., ⁸8. Azevedo RSS SE, Carvalho VL, et al. Mayaro fever virus, Brazilian Amazon. Emerging Infectious Diseases. 2009;15(11):1830-2., ¹⁴14. Auguste AJ LJ, Forrester NL, et al. Evolutionary and ecological characterization of Mayaro virus strains isolated during an outbreak, Venezuela, 2010. Emerging Infectious Diseases. 2015;21(10):1742-50.

15. SCHMIDT JR, GAJDUSEK DC, SCHAFFER M, GORRIE RH. Epidemic jungle fever among Okinawan colonists in the Bolivian rain forest. II. Isolation and characterization of Uruma virus, a newly recognized human pathogen. Am J Trop Med Hyg. 1959;8(4):479-87.

16. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, et al. Arboviral etiologies of acute febrile illnesses in Western South America, 2000-2007. PLoS Negl Trop Dis. 2010;4(8):e787.

17. LeDuc JW, Pinheiro FP, Travassos da Rosa AP. An outbreak of Mayaro virus disease in Belterra, Brazil. II. Epidemiology. Am J Trop Med Hyg. 1981;30(3):682-8.

18. Terzian AC, Auguste AJ, Vedovello D, Ferreira MU, da Silva-Nunes M, Sperança MA, et al. Isolation and characterization of Mayaro virus from a human in Acre, Brazil. Am J Trop Med Hyg. 2015;92(2):401-4.

19. Munoz M NJ. Virus Mayaro: Un arbovirus reemergente en Vene-zuela y Latinoamerica. Biomedica. 2012;32:286-302.

20. Pinheiro FP, Bensabath G, Rosa APAT, Lainson R, Shaw JJ, Ward R, et al. Public health hazards among workers along the trans-Amazon highway. Journal of Occupational Medicine. 1977;19:490-7.

21. Tavares-Neto J, Freitas-Carvalho J, Teixeira Nunes MR, Rocha G, Guerreiro Rodrigues S, Damasceno E, et al. Pesquisa de anticorpos contra arbovirus e o virus vacinal da febre amarela em uma amostra da populacao de Rio Branco, antes a tres meses apos a vacina 17D. Revista da Sociedada Brasileira de Medicina Tropical. 2004;37:1-6.

22. Cruz ACR, Correa dos Prazeres AdS, Colares Gama E, Furtado da Lima M, Silva Azevedo RdS, Neves Casseb LM, et al. Vigilancia sorologica para arbovirus em Juruti, Para, Brasil. Cad Saude Publica. 2009;25(11):2517-23.

23. Zuchi N, Borges da Silva Heinen L, Mendes dos Santos MA, Pereira FC, Dezengrini Slhessarenko R. Molecular detection of Mayaro virus during a dengue outbreak in the state of Mato Grosso, Central-West Brazil. Mem Inst Oswaldo Cruz. 2014;109(6):820-3.

24. Nunes MR, Barbosa TF, Casseb LM, Nunes Neto JP, Segura NeO, Monteiro HA, et al. [Arbovirus eco-epidemiology in the area affected by the Cuiabá-Santarém Highway (BR-163), Pará State, Brazil]. Cad Saude Publica. 2009;25(12):2583-602.

25. Talarmin A CL, Kazanji M, et al. Mayaro virus fever in French Guiana: Isolation, identification, and seroprevalence. American Journal of Tropical Medical Hygiene. 1998;59(3):452-6.

26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.

27. Navarrete-Espinosa J G-DH. Arbovirus causales de fiebre hemorrágica en pacientes del Instituo Mexicano del Seguro Social. Revista Medica Del Instituto Mexicano Del Seguro Social. 2006;44(4):347-53.

28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73.

29. Halsey ES, Siles C, Guevara C, Vilcarromero S, Jhonston EJ, Ramal C, et al. Mayaro virus infection, Amazon Basin region, Peru, 2010-2013. Emerg Infect Dis. 2013;19(11):1839-42.

30. Torres JR, Russell KL, Vasquez C, Barrera R, Tesh RB, Salas R, et al. Family cluster of Mayaro fever, Venezuela. Emerg Infect Dis. 2004;10(7):1304-6.

31. Travassos da Rosa JF MdSW, Pinheiro FP, et al. Oropouche virus: Clinical, epidemiological, and molecular aspects of a neglected Orthobunyavirus. American Journal of Tropical Medical Hygiene. 2017;96(5):1019-30.

32. Coimbra TL, Santos CL, Suzuki A, Petrella SM, Bisordi I, Nagamori AH, et al. Mayaro virus: imported cases of human infection in São Paulo State, Brazil. Rev Inst Med Trop Sao Paulo. 2007;49(4):221-4.

33. Srihongse S, Stacy HG, Gauld JR. A survey to assess potential human disease hazards along proposed sea level canal routes in Panama and Colombia. IV. Arbovirus surveillance in man. Military Medicine Journal. 1973;138:422-6.

34. Pinto De Figueiredo RM, Dutary Thatcher B, Lira de Lima M, Carvalho Almeida T, Duarte Alecrim W, Vinitius de Farias Guerra M. Doenças exantemáticas e primeira epidemia de dengue ocorrida em Manaus, Amazonas, no período de 1998-1999. Revista da Sociedade Brasileira de Medicina Tropical. 2004;37(6):476-9.

35. Diaz LA, Spinsanti LI, Almiron WR, Contigiani MS. UNA virus: first report of human infection in Argentina. Rev Inst Med Trop Sao Paulo. 2003;45(2):109-10.

36. Estudio Interinstitucional Desarrollado Por Las Instituciones Del Ministerio de Salud Del Perú, en colaboración con el Instituto de Investigación de Enfermedades Tropicales de la Marina de los Estados Unidos, La Universidad Nacional Mayor de San Marcos, & La Universidad Peruana Cayetano Heredia. Perfil etiológico del síndrome febril en áreas de alto riesgo de transmisión de enfermedades infecciosas de impacto en salud pública en el Perú, 2000-2001. 2005.-³⁷37. Anderson CR, Downs WG, Wattley GH, Ahin NW, Reese AA. Mayaro virus: a new human disease agent. II. Isolation from blood of patients in Trinidad, B.W.I. Am J Trop Med Hyg. 1957;6(6):1012-6.). Given the extent of arboviral diseases in Latin America and the Caribbean, MAYV may pose a similar public health threat in the area.

As with other arboviral diseases, such as yellow fever, that have an urban cycle through Ae. aegypti, the MAYV case in Haiti highlights the need for vector competency research and demonstrates the potential for the MAYV transmission cycle to shift into an urban cycle. Urbanization of MAYV could establish new outbreaks of greater number throughout Latin America and the Caribbean and result in a wider distribution of MAYV, including circulation in North America and Europe (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9., ²⁶26. Lednicky J BDRV, Elbadry M, et al. Mayaro virus in child with acute febrile illness, Haiti, 2015. Emerging Infectious Diseases. 2016;22(11):2000-2.). Changes in the natural environment and the resulting impacts on interactions between host and vector populations could also expand the geographic distribution of MAYV in Latin America and the Caribbean (⁴⁹49. Vasconcelos PF, Travassos da Rosa AP, Rodrigues SG, Travassos da Rosa ES, Dégallier N, Travassos da Rosa JF. Inadequate management of natural ecosystem in the Brazilian Amazon region results in the emergence and reemergence of arboviruses. Cad Saude Publica. 2001;17 Suppl:155-64.). These changes could include the globalization of human and animal transportation, climate change, deforestation, human colonization, urbanization, mining, and infrastructure construction (dams and highways) (¹⁰10. Sakkas H BP, Franks A, Papadopoulou C. Oropouche fever: A review. Viruses. 2018;10(4)., ²⁸28. Tesh RB WD, Russell KL, et al. Mayaro virus disease: An emerging mosquito-borne zoonosis in tropical South America. Clinical Infectious Diseases. 1999;28(1):67-73., ⁴⁹49. Vasconcelos PF, Travassos da Rosa AP, Rodrigues SG, Travassos da Rosa ES, Dégallier N, Travassos da Rosa JF. Inadequate management of natural ecosystem in the Brazilian Amazon region results in the emergence and reemergence of arboviruses. Cad Saude Publica. 2001;17 Suppl:155-64.). Increased air travel and globalization is expected to boost the number of imported cases of MAYV (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9., ⁴⁴44. Theilacker C, Held J, Allering L, Emmerich P, Schmidt-Chanasit J, Kern WV, et al. Prolonged polyarthralgia in a German traveller with Mayaro virus infection without inflammatory correlates. BMC Infect Dis. 2013;13:369.). As such, MAYV demonstrates the potential to emerge in new areas and reemerge in existing areas and become a significant public health issue in the Western Hemisphere (¹⁰10. Sakkas H BP, Franks A, Papadopoulou C. Oropouche fever: A review. Viruses. 2018;10(4).). Findings from our research coincide with previous research.

Cases of MAYV may be going undetected due to a lack of awareness among the medical community. For example, since diagnostic testing is not widely available and little is known of MAYV outside of endemic areas, imported cases may be getting clinically misdiagnosed as dengue. Within Latin America and the Caribbean, coinfection with other arboviral diseases may also misguide the diagnosis of MAYV, further demonstrating that the number of reported cases of MAYV only represent a portion of those that have occurred (⁹9. Slegers CA, Keuter M, Günther S, Schmidt-Chanasit J, van der Ven AJ, de Mast Q. Persisting arthralgia due to Mayaro virus infection in a traveler from Brazil: is there a risk for attendants to the 2014 FIFA World Cup? J Clin Virol. 2014;60(3):317-9.). It is also important to note that many of the cases of MAYV that were identified in academic literature were only detected because of extensive testing for arboviral viruses such as dengue and Chikungunya, further pointing to the need for differential testing for arboviral diseases. Lastly, since clinical symptoms of MAYV are generic, treatment may not be sought after and cases could go undetected. This would present a large obstacle to timely outbreak detection.

Data constraints must be considered when evaluating the outcomes of this research. The first limitation to this research includes the potential overestimation of the total number of presumptive MAYV cases found in academic literature due to serological cross-reaction between alphaviruses. Cross-reaction could also be a concern since diagnostic techniques were not uniform throughout the studies we included. Finally, many cases of MAYV may be unaccounted for both due to similarities between the clinical symptoms of MAYV and other arboviral diseases and coinfection.

Findings from this research demonstrate that MAYV surveillance efforts are limited in comparison to the virus’s epidemic potential, highlighting the importance of enhancing arboviral surveillance systems to include the differential diagnosis of MAYV. Given that the number of known cases of MAYV were primarily drawn from academic literature, country-level surveillance systems need to be strengthened to improve the data collection capabilities of health authorities.

Specific recommendations for MAYV surveillance include standardized lab capacities, the proactive seeking of cases, and the creation of standardized case definitions and laboratory diagnosis algorithms. While these recommendations are generally applicable to other arboviral diseases, the application of these recommendations specifically for MAYV will allow epidemics to be identified before they become problematic and also help the data collected to serve as a bridge between research and public health practice. Capacities and differential diagnosis algorithms need to be strengthened to ensure that labs are able to accurately distinguish among arboviral viruses. It is also important that labs be considered an integral data source for surveillance systems. Other recommendations include strengthening entomological surveillance and creating a global arboviral database. Public health practitioners and clinicians should also be made aware of the other arboviral diseases that exist, to be better able to discern the differences between them. Lastly, increased research interest will allow for the ongoing exploration of potentially epidemic diseases, such as Mayaro fever.

Author contributions.

Dr. Ana Riviere-Cinnamond conceived the original idea for the special report, and Niloofar Ganjian collected the data, analyzed the data, interpreted the results, and wrote the paper. Both authors reviewed and approved the final version.

Acknowledgments.

The publication would not have been possible without the intellectual contributions and expert advice provided throughout the process of compiling this special report. The authors would especially like to thank Dr. Sylvain Aldighieri, Dr. Enrique Perez-Gutierrez, Dr. Jairo Andres Mendez Rico, Dr. Juliana Leite, Jisoo Kim, Tshewang Choden Dorji, and Alexandra Gomes.

Funding.

None declared.

Disclaimer.

The authors hold sole responsibility for the views expressed in the manuscript, which may not necessarily reflect the opinion or policy of the RPSP/PAJPH and/or PAHO.

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