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      Seroprevalence of Anti-Chikungunya Virus Antibodies in Children and Adults in Managua, Nicaragua, After the First Chikungunya Epidemic, 2014-2015

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          Abstract

          Chikungunya is a viral disease transmitted by Aedes aegypti and Ae. albopictus mosquitoes. In late 2013, chikungunya virus (CHIKV) was introduced into the Caribbean island of St. Martin. Since then, approximately 2 million chikungunya cases have been reported by the Pan American Health Organization, and most countries in the Americas report autochthonous transmission of CHIKV. In Nicaragua, the first imported case was described in July 2014 and the first autochthonous case in September 2014. Here, we conducted two studies to analyze the seroprevalence of anti-CHIKV antibodies after the first chikungunya epidemic in a community-based cohort study (ages 2–14 years) and in a cross-sectional survey of persons aged ≥15 years in the same area of Managua, Nicaragua. Routine annual serum samples collected from 3,362 cohort participants in March/April 2014 and 2015, and 848 age-stratified samples collected from persons ≥15 years old at the end of May-beginning of June 2015 were used to estimate the seroprevalence of anti-CHIKV antibodies after the first epidemic (October 2014 to February 2015 in the study population). Using an Inhibition ELISA assay that measures total anti-CHIKV antibodies, the seroprevalence was significantly higher in those aged ≥15 (13.1% (95%CI: 10.9, 15.5)) than in the pediatric population (6.1% (95%CI: 5.3, 6.9)). The proportion of inapparent infections was 58.3% (95%CI: 51.5, 65.1) in children and 64.9% (95%CI: 55.2, 73.7) in the ≥15 study population. We identified age, water availability, household size, and socioeconomic status as factors associated with the presence of anti-CHIKV antibodies. Overall, this is the first report of CHIKV seropositivity in continental Latin America and provides useful information for public health authorities in the region.

          Author Summary

          Chikungunya is a viral disease primarily characterized by high fever and joint pain. Chikungunya virus (CHIKV) is transmitted by infected Aedes aegypti and Ae. albopictus mosquitos. Although chikungunya was first described in 1952 and CHIKV has circulated in parts of Africa and Asia, since then, it was not introduced into the Americas until late 2013. Chikungunya poses a threat in tropical countries where the vector mosquitoes reside and in particular in CHIKV-naïve populations. In this study, we aimed to explore the dissemination of CHIKV through the first epidemic in Nicaragua and evaluate possible factors associated with infection. By analyzing the sera of two study populations, pediatric (2–14 years old) and ≥15 years participants, for anti-CHIKV antibodies, we determined who was infected during the first outbreak in Nicaragua. The seroprevalence of anti-CHIKV antibodies in the pediatric and ≥15 year-old study populations was 6.1% and 13.1%, respectively. Furthermore, using a demographic/household survey, we found that age, water availability, household size, and socioeconomic status were associated with CHIKV seropositivity. In conclusion, this study indicates the level of protective immunity the population has developed and can help government institutions develop intervention strategies.

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          Most cited references22

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          The Newala epidemic. III. The virus: isolation, pathogenic properties and relationship to the epidemic.

          R. W. Ross (1956)
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            Persistent arthralgia associated with chikungunya virus: a study of 88 adult patients on reunion island.

            An outbreak of chikungunya virus infection occurred on Reunion Island during the period 2005-2006. Persistent arthralgia after chikungunya virus infection has been reported, but few studies have treated this aspect of the disease. Adult patients with laboratory-confirmed acute chikungunya virus infection who were referred to Groupe Hospitalier Sud Reunion during the period 2005-2006 were asked to participate in the study. Patients were assessed a mean of 18 months after acute disease occurred. Assessment consisted of answering questions on a standard form, undergoing a medical examination, and being tested for the presence of IgM antibodies to chikungunya virus. Eighty-eight patients (mean age, 58.3 years; male-to-female ratio, 1.1:1.0) were included in this study. Fifty-eight patients (65.9%) had been hospitalized for acute chikungunya virus infection, and a history of arthralgia before chikungunya virus infection was reported by 39 patients (44%). Fifty-six patients (63.6%) reported persistent arthralgia related to chikungunya virus infection, and in almost one-half of the patients, the joint pain had a negative impact on everyday activities. Arthralgia was polyarticular in all cases, and pain was continuous in 31 patients (55.4%). Overall, 35 patients (39.7%) had test results positive for IgM antibodies to chikungunya virus. Persistent and disabling arthralgia was a frequent concern in this cohort of patients who had experienced severe chikungunya virus infection approximately 18 months earlier. Further studies are needed to evaluate the prevalence of persistent arthralgia in the general population to determine the real burden of the disease.
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              Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004.

              An outbreak of Chikungunya virus (CHIKV) disease associated with high fever and severe protracted arthralgias was detected in Lamu, Kenya, peaking in July 2004. At least 1,300 cases were documented. We conducted a seroprevalence study to define the magnitude of transmission on Lamu Island. We conducted a systematic cross-sectional survey. We administered questionnaires and tested 288 sera from Lamu residents for IgM and IgG antibodies to CHIKV. Chikungunya virus infection (seropositivity) was defined as a person with IgG and/or IgM antibodies to CHIKV. IgM antibodies to CHIKV were detected in 18% (53/288) and IgG antibodies in 72% (206/288); IgM and/or IgG antibodies were present in 75% (215/288). The seroprevalence findings suggested that the outbreak was widespread, affecting 75% of the Lamu population; extrapolating the findings to the entire population, 13,500 (95% CI, 12,458-14328) were affected. Vector control strategies are needed to control the spread of this mosquito-borne infection.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                20 June 2016
                June 2016
                : 10
                : 6
                : e0004773
                Affiliations
                [1 ]Centro de Salud Sócrates Flores Vivas, Ministry of Health, Managua, Nicaragua
                [2 ]Sustainable Sciences Institute, Managua, Nicaragua
                [3 ]Division of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, United States of America
                [4 ]National Virology Laboratory, Centro Nacional de Diagnóstico y Referencia, Ministry of Health, Managua, Nicaragua
                [5 ]Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, United States of America
                Florida Department of Health, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GK LG AG AB EH. Performed the experiments: GK SR SO NS DC NG JCM. Analyzed the data: GK SR LG SO MM AB EH. Contributed reagents/materials/analysis tools: AB EH. Wrote the paper: GK SR LG AG AB EH.

                Article
                PNTD-D-15-02147
                10.1371/journal.pntd.0004773
                4913910
                27322692
                ab79b4e5-797c-42f5-872d-95c250b0ec41
                © 2016 Kuan et al

                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.

                History
                : 21 December 2015
                : 20 May 2016
                Page count
                Figures: 2, Tables: 3, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000060, National Institute of Allergy and Infectious Diseases;
                Award ID: R01 AI099631
                Award Recipient :
                Funded by: Pan American Health Organization
                Award Recipient :
                This work was supported by grant R01 AI099631 (AB) from the National Institute of Allergy and Infectious Diseases (NIAID) of the National Institutes of Health (NIH) and by the Nicaraguan office of the Pan American Health Organization through the PAHO/WHO-SSI Framework Agreement for Scientific and Technical Cooperation. We also thank the Minority Health and Health Disparities International Research Training (MHIRT) program at the University of California, Berkeley (grant T37 MD003406 from the National Institute on Minority Health and Health Disparities (NIMHD) of the NIH) for its support and funding. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Chikungunya Infection
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Pediatrics
                Research and Analysis Methods
                Immunologic Techniques
                Immunoassays
                Enzyme-Linked Immunoassays
                Medicine and Health Sciences
                Pediatrics
                Pediatric Infections
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                North America
                Central America
                Nicaragua
                Research and Analysis Methods
                Research Design
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                Physiology
                Immune Physiology
                Antibodies
                Medicine and Health Sciences
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                Custom metadata
                De-identified data from the cohort study are available from the Committee for Protection of Human Subjects (CPHS) for research purposes consistent with the approved study protocol. The CPHS may be contacted via the University of California, Berkeley Office for the Protection of Human Subjects at ophs@ 123456berkeley.edu . De-indentified data from the adult study are available from the Comite Institucional de Revision Etica (CIRE) of the Nicaragua Ministry of Health purposes consistent with the approved study protocol. CIRE may be contacted at parasitologia@ 123456minsa.gob.ni . The data cannot be made publicly available for legal reasons (e.g., public availability would violate the IRB protocol and informed consent and would compromise patient privacy).

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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