Silent emergence of Mayaro and Oropouche viruses in humans in Central Brazil

Abstract

Oropouche (OROV) virus and Mayaro (MAYV) virus belong to the Bunyaviridae family and Togaviridae family, respectively. These are dengue-like viruses, responsible for acute febrile diseases, mainly in the Pan-Amazon region. However, the clinical spectrum of disease ranges from subclinical cases to severe disease (Figueiredo, 2007Figueiredo L.T.M. Emergent arboviruses in Brazil.Rev Soc Bras Med Trop. 2007; 40: 224-229Crossref PubMed Google Scholar, Pinheiro et al., 1981Pinheiro F.P. Freitas R.B. Travassos da Rosa J.F. Gabbay Y.B. Mello W.A. LeDuc J.W. An Outbreak of Mayaro Virus Disease in Belterra, Brazil.Am J Trop Med Hyg. 1981; 30: 674-681Crossref PubMed Scopus (100) Google Scholar, Bastos et al., 2012Bastos M.S. Figueiredo L.T.M. Naveca F.G. Monte R.L. Lessa N. Figueiredo R.M.P. et al.Identification of Oropouche Orthobunyavirus in the Cerebrospinal Fluid of Three Patients in the Amazonas, Brazil.Am J Trop Med Hyg. 2012; 86: 732-735Crossref PubMed Scopus (51) Google Scholar). In addition, these viruses have the potential to expand to other sites due to the wide variety of vectors, including Haemagogus and Aedes mosquitoes for MAYV (Long et al., 2011Long K.C. Ziegler S.A. Thangamani S. Hausser N.L. Kochel T.J. Higgs S. et al.Experimental transmission of Mayaro virus by Aedes aegypti.Am J Trop Med Hyg. 2011; 85: 750-757Crossref PubMed Scopus (138) Google Scholar), and Culicoides paraensis and Ochlerotatus serratus for OROV (Pinheiro et al., 1962Pinheiro F.P. Pinheiro M. Bensabath G. Causey O.R. Shope R.E. Epidemia de vírus Oropouche em Belém.Rev Serv Esp Saúde Públ. 1962; 12: 15-23Google Scholar). Considering the potential epidemiological importance of these viruses, the authors performed a seroepidemiological study looking for the presence of anti-MAYV/OROV antibodies in patients from Goiânia, Central Brazil. The research was conducted due to the scarcity of data on the prevalence and circulation of these viruses in this region of the country, and in the case of OROV, due to the total absence of viral circulation findings in humans. A total of 647 blood samples collected from patients suspected of dengue during the period 2011–2013 were tested. Among these, 130 samples were dengue virus (DENV)-negative, collected at ≥5 days of illness. An enzyme immunoassay on infected cultured cells (EIA-ICC) was used to identify IgM/IgG for MAYV and OROV (Figueiredo et al., 1989Figueiredo L.T. Nogueira R.M. Cavalcanti S.M. Schatzmayr H. da Rosa A.T. Study of two different enzyme immunoassays for the detection of Mayaro virus antibodies.Mem Inst Oswaldo Cruz. 1989; 84: 303-307Crossref PubMed Google Scholar, Figueiredo and Shope, 1987Figueiredo L.T. Shope R.E. An enzyme immunoassay for dengue antibody using infected cultured mosquito cells as antigen.J Virol Methods. 1987; 17: 191-198Crossref PubMed Scopus (17) Google Scholar). IgM for MAYV was observed in six (4.6%) samples from patients who ranged in age from 9 to 65 years (mean 40.6 ± 20 years). Meanwhile, six (4.6%) samples obtained from patients who ranged in age from 17 to 41 years (mean 29.5 ± 7 years) had IgM for OROV. The majority of reactive samples were from female participants (approximately 60%). Interestingly, it was found that one of the IgM samples for MAYV was IgG-positive for OROV. There was simultaneous detection of IgM/IgG for OROV in three samples, probably indicating seroconversion. In addition, RT-PCR was performed on samples collected at ≤5 days of illness (Bronzoni et al., 2005Bronzoni R.V.M. Baleotti F.G. Nogueira R.M.R. Nunes M. Figueiredo L.T.M. Duplex reverse transcription-PCR followed by Nested PCR assays for detection and identification of Brazilian Alphaviruses and Flaviviruses.J Clin Microbiol. 2005; 43: 696-702Crossref PubMed Scopus (133) Google Scholar); however, genetic material was not found, possibly because of a short viremic period. Regarding the sensitivity of the serological tests, EIA-ICC has a lower sensitivity when compared to IgM antibody capture ELISA, which may have contributed to the possibility of false-negative results with reduced IgM anti-MAYV/OROV in these samples (Figueiredo et al., 1989Figueiredo L.T. Nogueira R.M. Cavalcanti S.M. Schatzmayr H. da Rosa A.T. Study of two different enzyme immunoassays for the detection of Mayaro virus antibodies.Mem Inst Oswaldo Cruz. 1989; 84: 303-307Crossref PubMed Google Scholar, Brunini et al., 2017Brunini S. França D.D.S. Silva J.B. Silva L.N. Silva F.P.A. Spadoni M. Rezza G. High frequency of Mayaro virus IgM among febrile patients, Central Brazil.Emerg Infect Dis. 2017; 23: 1025-1026Crossref PubMed Scopus (37) Google Scholar). The main clinical data for the patients are shown in Table 1.Table 1Clinical data of acute febrile patients positive for IgM against Mayaro virus (MAYV) and Oropouche virus (OROV)—Goiânia, Goiás State, Brazil.Sign or symptomNumber of patients (%)IgM MAYV (n = 5)aThis information was not gathered for the sixth patient IgM reactive against MAYV. All patients recovered and were cured.IgM OROV (n = 6)Prostration5 (100)5 (83.3)Eye pain5 (100)5 (83.3)Myalgia4 (80)5 (83.3)Arthralgia4 (80)5 (83.3)Headache4 (80)4 (66.6)Abdominal pain4 (80)3 (50)Rash3 (60)3 (50)Diarrhea3 (60)1 (16.6)Dizziness2 (40)3 (50)Itching2 (40)2 (33.3)Nausea2 (40)1 (16.6)Vomiting2 (40)1 (16.6)Palpebral edema1 (20)0Neurological1 (20)0Severe abdominal pain1 (20)2 (33.3)Jaundice01 (16.6)Respiratory distress01 (16.6)a This information was not gathered for the sixth patient IgM reactive against MAYV. All patients recovered and were cured. Open table in a new tab To date, there has only been evidence of OROV circulation in non-human primates in the region (Gibrail et al., 2016Gibrail M.M. Fiaccadori F.S. Souza M. Almeida T.N.V. Chiang J.O. Martins L.C. et al.Detection of antibodies to Oropouche virus in non-human primates in Goiânia City, Goiás.Rev Soc Bras Med Trop. 2016; 49: 357-360Crossref PubMed Scopus (13) Google Scholar). Regional studies have described the occurrence of OROV in non-human primates captured in urban conservation parks in 2011 to 2013, and MAYV infected humans (2014–2015) in rural areas near the city of Goiânia (Brunini et al., 2017Brunini S. França D.D.S. Silva J.B. Silva L.N. Silva F.P.A. Spadoni M. Rezza G. High frequency of Mayaro virus IgM among febrile patients, Central Brazil.Emerg Infect Dis. 2017; 23: 1025-1026Crossref PubMed Scopus (37) Google Scholar, Gibrail et al., 2016Gibrail M.M. Fiaccadori F.S. Souza M. Almeida T.N.V. Chiang J.O. Martins L.C. et al.Detection of antibodies to Oropouche virus in non-human primates in Goiânia City, Goiás.Rev Soc Bras Med Trop. 2016; 49: 357-360Crossref PubMed Scopus (13) Google Scholar). The febrile patients reported in this study were identified during the same time period, confirming the occurrence of MAYV infections in patients from an urban region of Central Brazil, as well as the circulation of OROV due to the presence of mosquito vectors. These results suggest that in addition to Mayaro fever in urban areas, Oropouche fever should be considered in the differential diagnosis of DENV-like infections in endemic areas.