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

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), Sã...

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Veröffentlicht in:PLoS neglected tropical diseases 2024-03, Vol.18 (3), p.e0012013-e0012013
Hauptverfasser: Zini, Nathalia, Ávila, Matheus Henrique Tavares, Cezarotti, Natalia Morbi, Parra, Maisa Carla Pereira, Banho, Cecília Artico, Sacchetto, Livia, Negri, Andreia Francesli, Araújo, Emerson, Bittar, Cintia, Milhin, Bruno Henrique Gonçalves de Aguiar, Miranda Hernandes, Victor, Dutra, Karina Rocha, Trigo, Leonardo Agopian, Cecílio da Rocha, Leonardo, Alves da Silva, Rafael, Celestino Dutra da Silva, Gislaine, Fernanda Pereira Dos Santos, Tamires, de Carvalho Marques, Beatriz, Lopes Dos Santos, Andresa, Augusto, Marcos Tayar, Mistrão, Natalia Franco Bueno, Ribeiro, Milene Rocha, Pinheiro, Tauyne Menegaldo, Maria Izabel Lopes Dos Santos, Thayza, Avilla, Clarita Maria Secco, Bernardi, Victoria, Freitas, Caroline, Gandolfi, Flora de Andrade, Ferraz Júnior, Hélio Correa, Perim, Gabriela Camilotti, Gomes, Mirella Cezare, Garcia, Pedro Henrique Carrilho, Rocha, Rodrigo Sborghi, Galvão, Tayna Manfrin, Fávaro, Eliane Aparecida, Scamardi, Samuel Noah, Rogovski, Karen Sanmartin, Peixoto, Renan Luiz, Benfatti, Luiza, Cruz, Leonardo Teixeira, Chama, Paula Patricia de Freitas, Oliveira, Mânlio Tasso, Watanabe, Aripuanã Sakurada Aranha, Terzian, Ana Carolina Bernardes, de Freitas Versiani, Alice, Dibo, Margareth Regina, Chiaravalotti-Neto, Francisco, Weaver, Scott Cameron, Estofolete, Cassia Fernanda, Vasilakis, Nikos, Nogueira, Mauricio Lacerda
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container_title PLoS neglected tropical diseases
container_volume 18
creator Zini, Nathalia
Ávila, Matheus Henrique Tavares
Cezarotti, Natalia Morbi
Parra, Maisa Carla Pereira
Banho, Cecília Artico
Sacchetto, Livia
Negri, Andreia Francesli
Araújo, Emerson
Bittar, Cintia
Milhin, Bruno Henrique Gonçalves de Aguiar
Miranda Hernandes, Victor
Dutra, Karina Rocha
Trigo, Leonardo Agopian
Cecílio da Rocha, Leonardo
Alves da Silva, Rafael
Celestino Dutra da Silva, Gislaine
Fernanda Pereira Dos Santos, Tamires
de Carvalho Marques, Beatriz
Lopes Dos Santos, Andresa
Augusto, Marcos Tayar
Mistrão, Natalia Franco Bueno
Ribeiro, Milene Rocha
Pinheiro, Tauyne Menegaldo
Maria Izabel Lopes Dos Santos, Thayza
Avilla, Clarita Maria Secco
Bernardi, Victoria
Freitas, Caroline
Gandolfi, Flora de Andrade
Ferraz Júnior, Hélio Correa
Perim, Gabriela Camilotti
Gomes, Mirella Cezare
Garcia, Pedro Henrique Carrilho
Rocha, Rodrigo Sborghi
Galvão, Tayna Manfrin
Fávaro, Eliane Aparecida
Scamardi, Samuel Noah
Rogovski, Karen Sanmartin
Peixoto, Renan Luiz
Benfatti, Luiza
Cruz, Leonardo Teixeira
Chama, Paula Patricia de Freitas
Oliveira, Mânlio Tasso
Watanabe, Aripuanã Sakurada Aranha
Terzian, Ana Carolina Bernardes
de Freitas Versiani, Alice
Dibo, Margareth Regina
Chiaravalotti-Neto, Francisco
Weaver, Scott Cameron
Estofolete, Cassia Fernanda
Vasilakis, Nikos
Nogueira, Mauricio Lacerda
description 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. 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. 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.
doi_str_mv 10.1371/journal.pntd.0012013
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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. 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. 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.</description><identifier>ISSN: 1935-2735</identifier><identifier>ISSN: 1935-2727</identifier><identifier>EISSN: 1935-2735</identifier><identifier>DOI: 10.1371/journal.pntd.0012013</identifier><identifier>PMID: 38484018</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aedes ; Animals ; Antibodies ; Antibodies, Neutralizing - genetics ; Antibodies, Viral ; Aquatic insects ; Asymptomatic ; Biology and life sciences ; Blood ; Brazil ; Brazil - epidemiology ; Care and treatment ; Chikungunya fever ; Chikungunya Fever - epidemiology ; Chikungunya virus ; Chikungunya virus - genetics ; Circulation ; Consent ; Control ; Cross-reactivity ; Culicidae ; Dengue - diagnosis ; Dengue - epidemiology ; Dengue fever ; Diagnosis ; Epidemics ; Epidemiology ; Genomic analysis ; Genotypes ; Health surveillance ; Human diseases ; Humans ; Immunoglobulin G ; Immunoglobulin M ; Infections ; Medical research ; Medicine and Health Sciences ; Mosquitoes ; Neighborhoods ; Neutralization ; Neutralizing ; Outbreaks ; People and places ; Phylogenetics ; Phylogeny ; Population dynamics ; Population studies ; Prospective Studies ; Public health ; Questionnaires ; Research and Analysis Methods ; Review boards ; Risk factors ; Seroconversion ; Seroepidemiologic Studies ; Serology ; Signs and symptoms ; Sociodemographics ; Surveillance ; Vector-borne diseases ; Viral infections ; Viruses</subject><ispartof>PLoS neglected tropical diseases, 2024-03, Vol.18 (3), p.e0012013-e0012013</ispartof><rights>Copyright: © 2024 Zini et al. 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This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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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. 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. 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.</description><subject>Aedes</subject><subject>Animals</subject><subject>Antibodies</subject><subject>Antibodies, Neutralizing - genetics</subject><subject>Antibodies, Viral</subject><subject>Aquatic insects</subject><subject>Asymptomatic</subject><subject>Biology and life sciences</subject><subject>Blood</subject><subject>Brazil</subject><subject>Brazil - epidemiology</subject><subject>Care and treatment</subject><subject>Chikungunya fever</subject><subject>Chikungunya Fever - epidemiology</subject><subject>Chikungunya virus</subject><subject>Chikungunya virus - genetics</subject><subject>Circulation</subject><subject>Consent</subject><subject>Control</subject><subject>Cross-reactivity</subject><subject>Culicidae</subject><subject>Dengue - diagnosis</subject><subject>Dengue - epidemiology</subject><subject>Dengue fever</subject><subject>Diagnosis</subject><subject>Epidemics</subject><subject>Epidemiology</subject><subject>Genomic analysis</subject><subject>Genotypes</subject><subject>Health surveillance</subject><subject>Human diseases</subject><subject>Humans</subject><subject>Immunoglobulin G</subject><subject>Immunoglobulin M</subject><subject>Infections</subject><subject>Medical research</subject><subject>Medicine and Health Sciences</subject><subject>Mosquitoes</subject><subject>Neighborhoods</subject><subject>Neutralization</subject><subject>Neutralizing</subject><subject>Outbreaks</subject><subject>People and places</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Population dynamics</subject><subject>Population studies</subject><subject>Prospective Studies</subject><subject>Public health</subject><subject>Questionnaires</subject><subject>Research and Analysis Methods</subject><subject>Review boards</subject><subject>Risk 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circulation of chikungunya virus in São Jose do Rio Preto, Brazil, 2015-2019</title><author>Zini, Nathalia ; Ávila, Matheus Henrique Tavares ; Cezarotti, Natalia Morbi ; Parra, Maisa Carla Pereira ; Banho, Cecília Artico ; Sacchetto, Livia ; Negri, Andreia Francesli ; Araújo, Emerson ; Bittar, Cintia ; Milhin, Bruno Henrique Gonçalves de Aguiar ; Miranda Hernandes, Victor ; Dutra, Karina Rocha ; Trigo, Leonardo Agopian ; Cecílio da Rocha, Leonardo ; Alves da Silva, Rafael ; Celestino Dutra da Silva, Gislaine ; Fernanda Pereira Dos Santos, Tamires ; de Carvalho Marques, Beatriz ; Lopes Dos Santos, Andresa ; Augusto, Marcos Tayar ; Mistrão, Natalia Franco Bueno ; Ribeiro, Milene Rocha ; Pinheiro, Tauyne Menegaldo ; Maria Izabel Lopes Dos Santos, Thayza ; Avilla, Clarita Maria Secco ; Bernardi, Victoria ; Freitas, Caroline ; Gandolfi, Flora de Andrade ; Ferraz Júnior, Hélio Correa ; Perim, Gabriela Camilotti ; Gomes, Mirella Cezare ; Garcia, Pedro Henrique Carrilho ; Rocha, Rodrigo Sborghi ; Galvão, Tayna Manfrin ; Fávaro, Eliane Aparecida ; Scamardi, Samuel Noah ; Rogovski, Karen Sanmartin ; Peixoto, Renan Luiz ; Benfatti, Luiza ; Cruz, Leonardo Teixeira ; Chama, Paula Patricia de Freitas ; Oliveira, Mânlio Tasso ; Watanabe, Aripuanã Sakurada Aranha ; Terzian, Ana Carolina Bernardes ; de Freitas Versiani, Alice ; Dibo, Margareth Regina ; Chiaravalotti-Neto, Francisco ; Weaver, Scott Cameron ; Estofolete, Cassia Fernanda ; Vasilakis, Nikos ; Nogueira, Mauricio Lacerda</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c574t-78e2440f086a2ee40f358264bd16d8fae96109231d444576d757d4832891e8db3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aedes</topic><topic>Animals</topic><topic>Antibodies</topic><topic>Antibodies, Neutralizing - genetics</topic><topic>Antibodies, Viral</topic><topic>Aquatic insects</topic><topic>Asymptomatic</topic><topic>Biology and 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Sciences</topic><topic>Mosquitoes</topic><topic>Neighborhoods</topic><topic>Neutralization</topic><topic>Neutralizing</topic><topic>Outbreaks</topic><topic>People and places</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Population dynamics</topic><topic>Population studies</topic><topic>Prospective Studies</topic><topic>Public health</topic><topic>Questionnaires</topic><topic>Research and Analysis Methods</topic><topic>Review boards</topic><topic>Risk factors</topic><topic>Seroconversion</topic><topic>Seroepidemiologic Studies</topic><topic>Serology</topic><topic>Signs and symptoms</topic><topic>Sociodemographics</topic><topic>Surveillance</topic><topic>Vector-borne diseases</topic><topic>Viral infections</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zini, Nathalia</creatorcontrib><creatorcontrib>Ávila, Matheus Henrique Tavares</creatorcontrib><creatorcontrib>Cezarotti, Natalia 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zini, Nathalia</au><au>Ávila, Matheus Henrique Tavares</au><au>Cezarotti, Natalia Morbi</au><au>Parra, Maisa Carla Pereira</au><au>Banho, Cecília Artico</au><au>Sacchetto, Livia</au><au>Negri, Andreia Francesli</au><au>Araújo, Emerson</au><au>Bittar, Cintia</au><au>Milhin, Bruno Henrique Gonçalves de Aguiar</au><au>Miranda Hernandes, Victor</au><au>Dutra, Karina Rocha</au><au>Trigo, Leonardo Agopian</au><au>Cecílio da Rocha, Leonardo</au><au>Alves da Silva, Rafael</au><au>Celestino Dutra da Silva, Gislaine</au><au>Fernanda Pereira Dos Santos, Tamires</au><au>de Carvalho Marques, Beatriz</au><au>Lopes Dos Santos, Andresa</au><au>Augusto, Marcos Tayar</au><au>Mistrão, Natalia Franco Bueno</au><au>Ribeiro, Milene Rocha</au><au>Pinheiro, Tauyne Menegaldo</au><au>Maria Izabel Lopes Dos Santos, Thayza</au><au>Avilla, Clarita Maria Secco</au><au>Bernardi, Victoria</au><au>Freitas, Caroline</au><au>Gandolfi, Flora de Andrade</au><au>Ferraz Júnior, Hélio Correa</au><au>Perim, Gabriela Camilotti</au><au>Gomes, Mirella Cezare</au><au>Garcia, Pedro Henrique Carrilho</au><au>Rocha, Rodrigo Sborghi</au><au>Galvão, Tayna Manfrin</au><au>Fávaro, Eliane Aparecida</au><au>Scamardi, Samuel Noah</au><au>Rogovski, Karen Sanmartin</au><au>Peixoto, Renan Luiz</au><au>Benfatti, Luiza</au><au>Cruz, Leonardo Teixeira</au><au>Chama, Paula Patricia de Freitas</au><au>Oliveira, Mânlio Tasso</au><au>Watanabe, Aripuanã Sakurada Aranha</au><au>Terzian, Ana Carolina Bernardes</au><au>de Freitas Versiani, Alice</au><au>Dibo, Margareth Regina</au><au>Chiaravalotti-Neto, Francisco</au><au>Weaver, Scott Cameron</au><au>Estofolete, Cassia Fernanda</au><au>Vasilakis, Nikos</au><au>Nogueira, Mauricio Lacerda</au><au>Viennet, Elvina</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cryptic circulation of chikungunya virus in São Jose do Rio Preto, Brazil, 2015-2019</atitle><jtitle>PLoS neglected tropical diseases</jtitle><addtitle>PLoS Negl Trop Dis</addtitle><date>2024-03-01</date><risdate>2024</risdate><volume>18</volume><issue>3</issue><spage>e0012013</spage><epage>e0012013</epage><pages>e0012013-e0012013</pages><issn>1935-2735</issn><issn>1935-2727</issn><eissn>1935-2735</eissn><abstract>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. 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. 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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38484018</pmid><doi>10.1371/journal.pntd.0012013</doi><orcidid>https://orcid.org/0000-0003-1102-2419</orcidid><oa>free_for_read</oa></addata></record>
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subjects Aedes
Animals
Antibodies
Antibodies, Neutralizing - genetics
Antibodies, Viral
Aquatic insects
Asymptomatic
Biology and life sciences
Blood
Brazil
Brazil - epidemiology
Care and treatment
Chikungunya fever
Chikungunya Fever - epidemiology
Chikungunya virus
Chikungunya virus - genetics
Circulation
Consent
Control
Cross-reactivity
Culicidae
Dengue - diagnosis
Dengue - epidemiology
Dengue fever
Diagnosis
Epidemics
Epidemiology
Genomic analysis
Genotypes
Health surveillance
Human diseases
Humans
Immunoglobulin G
Immunoglobulin M
Infections
Medical research
Medicine and Health Sciences
Mosquitoes
Neighborhoods
Neutralization
Neutralizing
Outbreaks
People and places
Phylogenetics
Phylogeny
Population dynamics
Population studies
Prospective Studies
Public health
Questionnaires
Research and Analysis Methods
Review boards
Risk factors
Seroconversion
Seroepidemiologic Studies
Serology
Signs and symptoms
Sociodemographics
Surveillance
Vector-borne diseases
Viral infections
Viruses
title Cryptic circulation of chikungunya virus in São Jose do Rio Preto, Brazil, 2015-2019
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