High Rate of Subclinical Chikungunya Virus Infection and Association of Neutralizing Antibody with Protection in a Prospective Cohort in The Philippines
Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a countr...
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| Published in | PLoS neglected tropical diseases Vol. 9; no. 5; p. e0003764 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.05.2015
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation.
A prospective longitudinal cohort of subjects ≥6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2, 5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by ≥8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer ≥10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean.
Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. |
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| AbstractList | Chikungunya virus (CHIKV) is a re-emerging mosquito-borne pathogen for which the majority of infections have been considered to result in febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort of subjects greater than or equal to 6 months old who underwent active surveillance for acute febrile illness from 2012-13 in Cebu City, Philippines. Symptomatic CHIKV infections were detected by PCR and/or ELISA in acute/convalescent blood samples. Subclinical infections were identified by neutralizing antibody seroconversion between enrollment and 12-month visits without symptomatic infection. Among 853 subjects who completed all study activities at 12 months, 19 symptomatic and 87 subclinical infections occurred (2.19 and 10.03 per 100 person-years, respectively). A positive baseline CHIKV PRNT titer was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic infection. Phylogenetic analysis showed Asian genotype closely related to strains from the recent Caribbean epidemic. These findings can help to assess disease burden, understand virus transmission, and support vaccine development. Background Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation. Methods/Findings A prospective longitudinal cohort of subjects ≥6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2, 5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by ≥8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer ≥10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean. Conclusions Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. BACKGROUND:Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation. METHODS/FINDINGS:A prospective longitudinal cohort of subjects ≥6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2, 5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by ≥8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer ≥10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean. CONCLUSIONS:Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation. A prospective longitudinal cohort of subjects [greater than or equal to] 6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2,5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by [greater than or equal to] 8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer [greater than or equal to] 10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean. Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation. A prospective longitudinal cohort of subjects ≥6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2, 5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by ≥8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer ≥10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean. Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. Chikungunya virus (CHIKV) is a re-emerging mosquito-borne pathogen for which the majority of infections have been considered to result in febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort of subjects ≥6 months old who underwent active surveillance for acute febrile illness from 2012–13 in Cebu City, Philippines. Symptomatic CHIKV infections were detected by PCR and/or ELISA in acute/convalescent blood samples. Subclinical infections were identified by neutralizing antibody seroconversion between enrollment and 12-month visits without symptomatic infection. Among 853 subjects who completed all study activities at 12 months, 19 symptomatic and 87 subclinical infections occurred (2.19 and 10.03 per 100 person-years, respectively). A positive baseline CHIKV PRNT titer was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic infection. Phylogenetic analysis showed Asian genotype closely related to strains from the recent Caribbean epidemic. These findings can help to assess disease burden, understand virus transmission, and support vaccine development. BACKGROUNDChikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation.METHODS/FINDINGSA prospective longitudinal cohort of subjects ≥6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2, 5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by ≥8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer ≥10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean.CONCLUSIONSSubclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. Background Chikungunya virus (CHIKV) is a globally re-emerging arbovirus for which previous studies have indicated the majority of infections result in symptomatic febrile illness. We sought to characterize the proportion of subclinical and symptomatic CHIKV infections in a prospective cohort study in a country with known CHIKV circulation. Methods/Findings A prospective longitudinal cohort of subjects [greater than or equal to] 6 months old underwent community-based active surveillance for acute febrile illness in Cebu City, Philippines from 2012-13. Subjects with fever history were clinically evaluated at acute, 2,5, and 8 day visits, and at a 3-week convalescent visit. Blood was collected at the acute and 3-week convalescent visits. Symptomatic CHIKV infections were identified by positive CHIKV PCR in acute blood samples and/or CHIKV IgM/IgG ELISA seroconversion in paired acute/convalescent samples. Enrollment and 12-month blood samples underwent plaque reduction neutralization test (PRNT) using CHIKV attenuated strain 181/clone25. Subclinical CHIKV infections were identified by [greater than or equal to] 8-fold rise from a baseline enrollment PRNT titer <10 without symptomatic infection detected during the intervening surveillance period. Selected CHIKV PCR-positive samples underwent viral isolation and envelope protein-1 gene sequencing. Of 853 subjects who completed all study procedures at 12 months, 19 symptomatic infections (2.19 per 100 person-years) and 87 subclinical infections (10.03 per 100 person-years) occurred. The ratio of subclinical-to-symptomatic infections was 4.6:1 varying with age from 2:1 in 6 month-5 year olds to 12:1 in those >50 years old. Baseline CHIKV PRNT titer [greater than or equal to] 10 was associated with 100% (95%CI: 46.1, 100.0) protection from symptomatic CHIKV infection. Phylogenetic analysis demonstrated Asian genotype closely related to strains from Asia and the Caribbean. Conclusions Subclinical infections accounted for a majority of total CHIKV infections. A positive baseline CHIKV PRNT titer was associated with protection from symptomatic CHIKV infection. These findings have implications for assessing disease burden, understanding virus transmission, and supporting vaccine development. |
| Audience | Academic |
| Author | Alera, Maria Theresa Velasco, John Mark Srikiatkhachorn, Anon Lago, Catherine B. Fernandez, Stefan Hermann, Laura L. Roque, Vito G. Levy, Jens W. Macareo, Louis R. Klungthong, Chonticha Villa, Daisy Nisalak, Ananda Thaisomboonsuk, Butsaya Yoon, In-Kyu Tac-An, Ilya A. Salje, Henrik |
| AuthorAffiliation | 2 Philippines-AFRIMS Virology Research Unit, Cebu City, Philippines 1 Department of Virology, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand 7 Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America 4 National Epidemiology Center, Department of Health, Manila, Philippines Centers for Disease Control and Prevention, UNITED STATES 3 Cebu City Health Department, Cebu City, Philippines 5 Department of Epidemiology, Johns Hopkins School of Public Health, Baltimore, Maryland, United States of America 6 Department of Medicine, University of Toronto, Toronto, Ontario, Canada |
| AuthorAffiliation_xml | – name: 1 Department of Virology, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand – name: 5 Department of Epidemiology, Johns Hopkins School of Public Health, Baltimore, Maryland, United States of America – name: 6 Department of Medicine, University of Toronto, Toronto, Ontario, Canada – name: 7 Division of Infectious Diseases and Immunology, Department of Medicine, University of Massachusetts Medical School, Worcester, Massachusetts, United States of America – name: Centers for Disease Control and Prevention, UNITED STATES – name: 2 Philippines-AFRIMS Virology Research Unit, Cebu City, Philippines – name: 4 National Epidemiology Center, Department of Health, Manila, Philippines – name: 3 Cebu City Health Department, Cebu City, Philippines |
| Author_xml | – sequence: 1 givenname: In-Kyu surname: Yoon fullname: Yoon, In-Kyu – sequence: 2 givenname: Maria Theresa surname: Alera fullname: Alera, Maria Theresa – sequence: 3 givenname: Catherine B. surname: Lago fullname: Lago, Catherine B. – sequence: 4 givenname: Ilya A. surname: Tac-An fullname: Tac-An, Ilya A. – sequence: 5 givenname: Daisy surname: Villa fullname: Villa, Daisy – sequence: 6 givenname: Stefan surname: Fernandez fullname: Fernandez, Stefan – sequence: 7 givenname: Butsaya surname: Thaisomboonsuk fullname: Thaisomboonsuk, Butsaya – sequence: 8 givenname: Chonticha surname: Klungthong fullname: Klungthong, Chonticha – sequence: 9 givenname: Jens W. surname: Levy fullname: Levy, Jens W. – sequence: 10 givenname: John Mark surname: Velasco fullname: Velasco, John Mark – sequence: 11 givenname: Vito G. surname: Roque fullname: Roque, Vito G. – sequence: 12 givenname: Henrik surname: Salje fullname: Salje, Henrik – sequence: 13 givenname: Louis R. surname: Macareo fullname: Macareo, Louis R. – sequence: 14 givenname: Laura L. surname: Hermann fullname: Hermann, Laura L. – sequence: 15 givenname: Ananda surname: Nisalak fullname: Nisalak, Ananda – sequence: 16 givenname: Anon surname: Srikiatkhachorn fullname: Srikiatkhachorn, Anon |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25951202$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2015 Public Library of Science 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Yoon I-K, Alera MT, Lago CB, Tac-An IA, Villa D, Fernandez S, et al. (2015) High Rate of Subclinical Chikungunya Virus Infection and Association of Neutralizing Antibody with Protection in a Prospective Cohort in The Philippines. PLoS Negl Trop Dis 9(5): e0003764. doi:10.1371/journal.pntd.0003764 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: IKY MTA SF BT CK AS. Performed the experiments: IKY MTA CBL SF BT CK JMV AN AS. Analyzed the data: IKY MTA CBL IATA DV SF BT CK JWL JMV VGR HS LRM LLH AN AS. Wrote the paper: IKY MTA CBL IATA DV SF BT CK JWL JMV VGR HS LRM LLH AN AS. The authors have declared that no competing interests exist. |
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