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Serological Data Shows Low Levels of Chikungunya Exposure in Senegalese Nomadic Pastoralists

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Serological Data Shows Low Levels of Chikungunya Exposure in Senegalese Nomadic Pastoralists pathogens Article Serological Data Shows Low Levels of Chikungunya Exposure in Senegalese Nomadic Pastoralists Mame Cheikh Seck 1,*, Aida Sadikh Badiane 1, Julie Thwing 2,3, Delynn Moss 4, Fatou Ba Fall 5, Jules Francois Gomis 1 , Awa Bineta Deme 1, Khadim Diongue 1 , Mohamed Sy 1, Aminata Mbaye 1, Tolla Ndiaye 1, Aminata Gaye 1, Yaye Die Ndiaye 1, Mamadou Alpha Diallo 1, Daouda Ndiaye 1 and Eric Rogier 2,* 1 Department of Parasitology, Faculty of Medicine and Pharmacy, Cheikh Anta Diop University, Dakar 12500, Senegal 2 Malaria Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA 3 President’s Malaria Initiative, Atlanta, GA 30303, USA 4 Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA 5 Senegal National Malaria Control Program, Dakar 999066, Senegal * Correspondence: [email protected] (M.C.S.); [email protected] (E.R.) Received: 1 July 2019; Accepted: 21 July 2019; Published: 27 July 2019 Abstract: The chikungunya virus (CHIKV) is spread by Aedes aegypti and Ae. albopictus mosquitos worldwide; infection can lead to disease including joint pain, fever, and rash, with some convalescent persons experiencing chronic symptoms. Historically, CHIKV transmission has occurred in Africa and Asia, but recent outbreaks have taken place in Europe, Indonesia, and the Americas. From September to October 2014, a survey was undertaken with nomadic pastoralists residing in the northeast departments of Senegal. Blood dried on filter paper (dried blood spots; DBS) were collected from 1465 participants of all ages, and assayed for Immunoglobulin G (IgG) antibodies against CHIKV E1 antigen by a bead-based multiplex assay. The overall seroprevalence of all participants to CHIKV E1 was 2.7%, with no persons under 10 years of age found to be antibody positive. Above 10 years of age, clear increases of seroprevalence and IgG levels were observed with increasing age; 7.6% of participants older than 50 years were found to be positive for anti-CHIKV IgG. Reported net ownership, net usage, and gender were all non-significant explanatory variables of seropositivity. These data show a low-level historical exposure of this pastoralist population to CHIKV, with no evidence of recent CHIKV transmission in the past decade. Keywords: serology; chikungunya; seroprevalence; nomadic pastoralists; Senegal; multiplex bead assay 1. Introduction The chikungunya virus (CHIKV) belongs to the genus Alphavirus (family Togaviridae), and is transmitted to humans primarily by Aedes aegypti and Ae. albopictus mosquitos, although it has also been found in other mosquitos [1–4]. CHIKV infection can present as asymptomatic, but the majority of infected persons will develop symptoms such as headache, fever, myalgia, and moderate to severe joint pains [5,6]. CHIKV was first isolated from a Tanzanian patient with dengue-like symptoms in the early 1950s [7], and has been confirmed on the continent in numerous African studies since the initial report [8–10]. Besides attempting to identify persons with active infection, seroepidemiological studies have also shed light on individual- and population-level exposure to CHIKV, with the added Pathogens 2019, 8, 113; doi:10.3390/pathogens8030113 www.mdpi.com/journal/pathogens Pathogens 2019, 8, x FOR PEER REVIEW 2 of 11 Pathogensstudies2019 have, 8 ,also 113 shed light on individual- and population-level exposure to CHIKV, with the added2 of 11 advantage of expanding the window of time of finding a “positive” through antibody detection advantage[11,12]. Inof humans, expanding IgG the responses window ofare time known of finding to occur a “positive” to CHIKV through E1 and antibody E2 antigens, detection which [11, 12are]. Inattractive humans, for IgG serological responses studies are known [12–15]. to occur to CHIKV E1 and E2 antigens, which are attractive for serologicalThe CHIKV studies was [12– identified15]. in Senegal in the 1960s [16,17], with defined outbreaks occurring in 2009,The 2010, CHIKV and 2015, was identified and a known in Senegal sylvatic in cycle the 1960s with [ 16infected,17], with monkeys defined identified outbreaks in occurring multiple instudies 2009, 2010,[18–21]. and Recent 2015, and studies a known have sylvatic confirmed cycle withcurrent infected CHIKV monkeys presence identified in Senegal in multiple both by studies detection [18–21 of]. Recentactive studiesviremia have and confirmedserological current evidence CHIKV [19,20,22]. presence However, in Senegal almost both byall detectionhistorical ofand active even viremia recent andCHIKV serological studies evidence have been [19 ,conducted20,22]. However, in the almostrelative allly historicaltropical and and sparsely even recent populated CHIKV studiessoutheastern have beenzone conducted of Senegal in the[19,23,24]. relatively As tropical of early and 2019, sparsely no populatedpublished southeasternstudies could zone be ofidentified Senegal [ 19that,23 ,24had]. Asinvestigated of early 2019, population no published exposure studies tocould CHIKV be identifiedof persons that living had in investigated the dry northern population part exposure of Senegal. to CHIKVFurthermore, of persons epidemiological living in the dry studies northern of partinfectious of Senegal. disease Furthermore, exposure epidemiological in Senegalese studiesnomadic of infectiouspopulations disease is largely exposure nonexistent. in Senegalese nomadic populations is largely nonexistent. ForFor the the current current study, study, populations populations of of nomadic nomadic pastoralists pastoralists were were sampled sampled in Senegalin Senegal in 2014 in 2014 for anfor integratedan integrated seroepidemiological seroepidemiological study. study. This This population population has more has more permanent permanent dwellings dwellings in the in north the north and centraland central regions regions and spendsand spends the dry the season dry season in the in south the south in order in order to seek to seek appropriate appropriate grazing grazing lands lands for theirfor their cattle, cattle, which which is dependent is dependent on on the the rainy rainy and and dry dry seasons seasons [25 [25].]. This This report report outlines outlines the the findings findings regardingregarding anti-CHIKV anti-CHIKV IgG IgG antibodies antibodies found found in in this this study study population. population. 2.2. ResultsResults 2.1.2.1. StudyStudy PopulationPopulation andand SamplingSampling LocationsLocations inin SenegalSenegal FromFrom SeptemberSeptember toto OctoberOctober 2014,2014, participantparticipant enrollmentenrollment occurredoccurred inin fivefive districtsdistricts inin thethe northeasternnortheastern regionsregions of Senegal: Dagana, Dagana, Podor, Podor, Pé Pté,été Ranérou,, Ranérou, and and Kanel Kanel (Figure (Figure 1).1 ).Participant Participant age ageranged ranged from from 1 to 1 80 to years, 80 years, and and 43.5% 43.5% were were female. female. In total, In total, 1465 1465 persons persons provided provided a dried a dried blood blood spot spot(DBS) (DBS) sample sample to allow to allow for serological for serological data data collection collection of anti-CHIKV of anti-CHIKV IgG IgGantibodies. antibodies. Of these, Of these, 1463 1463(99.9%) (99.9%) provided provided valid valid serology serology data data as described as described in Methods. in Methods. FigureFigure 1.1. SenegaleseSenegalese districtsdistricts includedincluded inin thethe nomadicnomadic pastoralistpastoralist study.study. PersonsPersons ofof allall agesages werewere sampledsampled from from five five districts districts in in Senegal Senegal from from September September to to October October 2014. 2014. Pathogens 2019, 8, 113 3 of 11 Pathogens 2019, 8, x FOR PEER REVIEW 3 of 11 2.2.2.2. Range Range of of IgG IgG Responses Responses to to CHIKV CHIKV E1 E1 Antigen Antigen and and Seropositivity Seropositivity Definition Definition FromFrom the fluorescencefluorescence signal signal of theof the bead-based bead-based IgG detectionIgG detection assay (medianassay (median fluorescence fluorescence intensity intensityminus background, minus background, MFI-bg), a rangeMFI-bg), ofsignal a range intensities of signal was intensities observed forwas the observed blood samples for the from blood this samplespopulation from (Figure this population2). Log-transformation (Figure 2). Log-tran of these MFI-bgsformation data of showed these MFI-bg a clear unimodaldata showed population a clear unimodalof low signal population intensities of low (under signal 200 intensities MFI-bg), (under with few 200 individuals MFI-bg), with showing few individuals an assay signalshowing above an assaythis level. signal A above two-component this level. finiteA two-component mixture model finite (FMM) mixture was usedmodel to allow(FMM) maximum was used likelihood to allow maximumestimate (MLE) likelihood predictions estimate to (MLE) determine predictions if two uniqueto determine populations if two unique existed, populations and outputs existed, illustrated and outputstwo components illustrated with two a components statistically significantwith a statistica differencelly significant in the means. difference The two-component in the means. FMMThe two- had componenta very good FMM fit to had the a data, very with good a fit z valueto the ofdata, 62.6 with for fittinga z value both of to62.6 the for first fitting and both
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