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

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

• Document type: Journal article
• Source: PLoS Neglected Tropical Diseases; v. 18, n. 3, p. 27-pg., 2024-03-01.

Abstract

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 Sao Jose do Rio Preto (SJdRP), Sao 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 Sao Jose 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 naive population. Improved knowledge of the epidemiological situation might aid in outbreaks prevention. Chikungunya virus (CHIKV) circulation has been causing large epidemics throughout the tropics and subtropics, affecting the quality of life of the global population. Additionally, the asymptomatic or subclinical case numbers are unclear due to a paucity of epidemiological studies. Since 2013, CHIKV epidemics have been spreading in the Americas, and more than 900,000 CHIKV infection cases were confirmed in Brazil in 2020. In Sao Jose do Rio Preto (SJdRP), only 41 cases of CHIKV infection were confirmed from 2015-2020, according to official bulletins. In the same period, our study revealed seven participants among 340 (2.05%) who seroconverted to anti-CHIKV IgG, while in a blood panel collected during a dengue outbreak, 22 samples among 497 (4.42%) had anti-CHIKV IgM. These results demonstrate that the cryptic CHIKV circulation in SJdRP and the high percentage of naive individuals could represent an imminent risk of outbreaks. Additionally, our data might assist public health authorities in the development of health measures for epidemiological and vector surveillance programs. (AU)

• FAPESP's process: 22/03645-1 - Study of the virus-vector interaction and the mechanisms involved in modulating the dynamics of viral transmission
• Grantee: Maurício Lacerda Nogueira
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 13/21719-3 - Epidemiological study of dengue (serotypes1-4) in a cohort of São José do Rio Preto, São Paulo, Brazil, during 2014-2018
• Grantee: Maurício Lacerda Nogueira
• Support Opportunities: Research Projects - Thematic Grants