Cryptic circulation of chikungunya virus in São Jose do Rio Preto, Brazil, 2015–2019

by Nathalia Zini, Matheus Henrique Tavares Ávila, Natalia Morbi Cezarotti, Maisa Carla Pereira Parra, Cecília Artico Banho, Livia Sacchetto, Andreia Francesli Negri, Emerson Araújo, Cintia Bittar, Bruno Henrique Gonçalves de Aguiar Milhin, Victor Miranda Hernandes, Karina Rocha Dutra, Leonardo Agopian Trigo, Leonardo Cecílio da Rocha, Rafael Alves da Silva, Gislaine Celestino Dutra da Silva, Tamires Fernanda Pereira dos Santos, Beatriz de Carvalho Marques, Andresa Lopes dos Santos, Marcos Tayar Augusto, Natalia Franco Bueno Mistrão, Milene Rocha Ribeiro, Tauyne Menegaldo Pinheiro, Thayza Maria Izabel Lopes dos Santos, Clarita Maria Secco Avilla, Victoria Bernardi, Caroline Freitas, Flora de Andrade Gandolfi, Hélio Correa Ferraz Júnior, Gabriela Camilotti Perim, Mirella Cezare Gomes, Pedro Henrique Carrilho Garcia, Rodrigo Sborghi Rocha, Tayna Manfrin Galvão, Eliane Aparecida Fávaro, Samuel Noah Scamardi, Karen Sanmartin Rogovski, Renan Luiz Peixoto, Luiza Benfatti, Leonardo Teixeira Cruz, Paula Patricia de Freitas Chama, Mânlio Tasso Oliveira, Aripuanã Sakurada Aranha Watanabe, Ana Carolina Bernardes Terzian, Alice de Freitas Versiani, Margareth Regina Dibo, Francisco Chiaravalotti-Neto, Scott Cameron Weaver, Cassia Fernanda Estofolete, Nikos Vasilakis, Mauricio Lacerda Nogueira

Background

Chikungunya virus (CHIKV) has spread across Brazil with varying incidence rates depending on the affected areas. Due to cocirculation of arboviruses and overlapping disease symptoms, CHIKV infection may be underdiagnosed. To understand the lack of CHIKV epidemics in São José do Rio Preto (SJdRP), São Paulo (SP), Brazil, we evaluated viral circulation by investigating anti-CHIKV IgG seroconversion in a prospective study of asymptomatic individuals and detecting anti-CHIKV IgM in individuals suspected of dengue infection, as well as CHIKV presence in Aedes mosquitoes. The opportunity to assess two different groups (symptomatic and asymptomatic) exposed at the same geographic region aimed to broaden the possibility of identifying the viral circulation, which had been previously considered absent.

Methodology/principal findings

Based on a prospective population study model and demographic characteristics (sex and age), we analyzed the anti-CHIKV IgG seroconversion rate in 341 subjects by ELISA over four years. The seroprevalence increased from 0.35% in the first year to 2.3% after 3 years of follow-up. Additionally, we investigated 497 samples from a blood panel collected from dengue-suspected individuals during the 2019 dengue outbreak in SJdRP. In total, 4.4% were positive for anti-CHIKV IgM, and 8.6% were positive for IgG. To exclude alphavirus cross-reactivity, we evaluated the presence of anti-Mayaro virus (MAYV) IgG by ELISA, and the positivity rate was 0.3% in the population study and 0.8% in the blood panel samples. In CHIKV and MAYV plaque reduction neutralization tests (PRNTs), the positivity rate for CHIKV-neutralizing antibodies in these ELISA-positive samples was 46.7%, while no MAYV-neutralizing antibodies were detected. Genomic sequencing and phylogenetic analysis revealed CHIKV genotype ECSA in São José do Rio Preto, SP. Finally, mosquitoes collected to complement human surveillance revealed CHIKV positivity of 2.76% of A. aegypti and 9.09% of A. albopictus (although it was far less abundant than A. aegypti) by RT–qPCR.

Conclusions/significance

Our data suggest cryptic CHIKV circulation in SJdRP detected by continual active surveillance. These low levels, but increasing, of viral circulation highlight the possibility of CHIKV outbreaks, as there is a large naïve population. Improved knowledge of the epidemiological situation might aid in outbreaks prevention.