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      Epidemiology of Chikungunya Virus Outbreaks in Guadeloupe and Martinique, 2014: An Observational Study in Volunteer Blood Donors

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          Abstract

          Background

          During Dec-2013, a chikungunya virus (CHIKV) outbreak was first detected in the French-West Indies. Subsequently, the virus dispersed to other Caribbean islands, continental America and many islands in the Pacific Ocean. Previous estimates of the attack rate were based on declaration of clinically suspected cases.

          Methods/Principal findings

          Individual testing for CHIKV RNA of all (n = 16,386) blood donations between Feb-24 th 2014 and Jan-31 st 2015 identified 0·36% and 0·42% of positives in Guadeloupe and Martinique, respectively. The incidence curves faithfully correlated with those of suspected clinical cases in the general population of Guadeloupe (abrupt epidemic peak), but not in Martinique (flatter epidemic growth). No significant relationship was identified between CHIKV RNA detection and age-classes or blood groups. Prospective (Feb-2014 to Jan-2015; n = 9,506) and retrospective (Aug-2013 to Feb-2014; n = 6,559) seroepidemiological surveys in blood donors identified a final seroprevalence of 48·1% in Guadeloupe and 41·9% in Martinique. Retrospective survey also suggested the absence or limited "silent" CHIKV circulation before the outbreak. Parameters associated with increased seroprevalence were: Gender (M>F), KEL-1, [RH+1/KEL-1], [A/RH+1] and [A/RH+1/KEL-1] blood groups in Martiniquan donors. A simulation model based on observed incidence and actual seroprevalence values predicted 2·5 and 2·3 days of asymptomatic viraemia in Martiniquan and Guadeloupian blood donors respectively.

          Conclusions/Significance

          This study, implemented promptly with relatively limited logistical requirements during CHIKV emergence in the Caribbean, provided unique information regarding retrospective and prospective epidemiology, infection risk factors and natural history of the disease. In the stressful context of emerging infectious disease outbreaks, blood donor-based studies can serve as robust and cost-effective first-line tools for public health surveys.

          Author Summary

          Chikungunya virus (CHIKV) is an emerging mosquito-borne arbovirus responsible of a large outbreak since December 2013 in the Americas from French islands in the Caribbean. Documentation of the epidemic was based on the survey of clinically suspected cases, providing limited information on the incidence of the disease overtime and the herd immunity of the general population at the end of the outbreak. Our study improved blood donors specimen collection and data obtained from the Nucleic Acid Testing (NAT) screening implemented during the outbreak in order to prevent CHIKV transmission by blood products. After an 11 month follow up, we determine for Martinique and Guadeloupe islands the CHIKV-RNA positive rate: 0.42% and 0.36% respectively and the final IgG seroprevalence: 41.2% and 48.1%. Using a simulation model, we estimate the CHIKV duration of asymptomatic viremia to be between 2.3 and 2.5 days. Our findings will help in the comprehension of the natural history of infection and provide helpful data for prevention of Transfusion transmitted infections. Our study provides evidence that monitoring of Chikungunya infection based on NAT screening of voluntary blood donors can be implemented rapidly and provides real-time epidemiological information. This should be of specific relevance to the case of epidemics caused by viral infections with high numbers of asymptomatic forms such as observed with the currently emerging Zika virus.

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          Most cited references16

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          Chikungunya in the Americas.

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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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              Estimating Chikungunya prevalence in La Réunion Island outbreak by serosurveys: Two methods for two critical times of the epidemic

              Background Chikungunya virus (CHIKV) caused a major two-wave seventeen-month-long outbreak in La Réunion Island in 2005–2006. The aim of this study was to refine clinical estimates provided by a regional surveillance-system using a two-stage serological assessment as gold standard. Methods Two serosurveys were implemented: first, a rapid survey using stored sera of pregnant women, in order to assess the attack rate at the epidemic upsurge (s1, February 2006; n = 888); second, a population-based survey among a random sample of the community, to assess the herd immunity in the post-epidemic era (s2, October 2006; n = 2442). Sera were screened for anti-CHIKV specific antibodies (IgM and IgG in s1, IgG only in s2) using enzyme-linked immunosorbent assays. Seroprevalence rates were compared to clinical estimates of attack rates. Results In s1, 18.2% of the pregnant women were tested positive for CHIKV specific antibodies (13.8% for both IgM and IgG, 4.3% for IgM, 0.1% for IgG only) which provided a congruent estimate with the 16.5% attack rate calculated from the surveillance-system. In s2, the seroprevalence in community was estimated to 38.2% (95% CI, 35.9 to 40.6%). Extrapolations of seroprevalence rates led to estimate, at 143,000 and at 300,000 (95% CI, 283,000 to 320,000), the number of people infected in s1 and in s2, respectively. In comparison, the surveillance-system estimated at 130,000 and 266,000 the number of people infected for the same periods. Conclusion A rapid serosurvey in pregnant women can be helpful to assess the attack rate when large seroprevalence studies cannot be done. On the other hand, a population-based serosurvey is useful to refine the estimate when clinical diagnosis underestimates it. Our findings give valuable insights to assess the herd immunity along the course of epidemics.
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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
                12 January 2017
                January 2017
                : 11
                : 1
                : e0005254
                Affiliations
                [1 ]Etablissement Français du Sang (EFS) Alpes Méditerranée, Marseille, France
                [2 ]Aix Marseille Université, IRD U190, INSERM U1207, EHESP: "Emergence des Pathologies Virales", Marseille, France
                [3 ]Institut Hospitalo Universitaire (IHU) Méditerranée Infection, Marseille, France
                [4 ]Etablissement Français du Sang (EFS) La Plaine-Saint-Denis, France
                [5 ]Centre National de Référence (CNR) des Arbovirus, Institut de Recherche Biomédicale des Armée, Hôpital d’Instruction des Armées Laveran, Marseille, France
                [6 ]Etablissement Français du Sang (EFS) Martinique, Fort de France, France
                [7 ]Etablissement Français du Sang (EFS) Guadeloupe-Guyane, Point a Pitre, France
                [8 ]Université de Franche- Comté, Besançon, France
                Oswaldo Cruz Foundation, BRAZIL
                Author notes

                The authors have declared that no competing interests exist.

                • Investigation: PG ILG OF.

                • Project administration: XdL PG JC RD.

                • Resources: PR FM.

                • Visualization: PG XdL.

                • Writing – review & editing: ILG RC PT.

                Article
                PNTD-D-16-01047
                10.1371/journal.pntd.0005254
                5230756
                28081120
                2ab80283-e3bc-4b47-b640-20b52b0e33ca
                © 2017 Gallian 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
                : 9 June 2016
                : 13 December 2016
                Page count
                Figures: 4, Tables: 2, Pages: 14
                Funding
                Funded by: Etablissement Français du Sang (EFS)
                Award Recipient :
                Funded by: Alliance pour les sciences de la vie et de la santé (AVIESAN)
                Award Recipient :
                Funded by: Institut National de la Santé et de la Recherche Médicale (INSERM)
                Award Recipient :
                Funded by: European programmes PREDEMICS
                Award ID: FP7-n°278433
                Award Recipient : Rémi CHARREL
                Funded by: European Virus Archive goes Global
                Award ID: EVAg, H2020-n°653316
                Award Recipient :
                Funded by: European Network for Diagnostics of Imported Viral Diseases
                Award Recipient : Rémi CHARREL
                This work was supported by Etablissement Français du Sang (EFS), Alliance pour les sciences de la vie et de la santé (AVIESAN), Institut National de la Santé et de la Recherche Médicale (INSERM) and in part by the European programmes PREDEMICS (FP7-n°278433), European Virus Archive goes Global (EVAg, H2020-n°653316) and European Network for Diagnostics of Imported Viral Diseases (ENIVD, European Centre for Disease Prevention and Control). The work of RC was done under the frame of EurNegVec COST Action TD1303. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Chikungunya Infection
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