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Exposure to Ebola Virus and Risk for Infection with Malaria Parasites, Rural Gabon Jessica L

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Exposure to Ebola Virus and Risk for Infection with Malaria Parasites, Rural Gabon Jessica L Exposure to Ebola Virus and Risk for Infection with Malaria Parasites, Rural Gabon Jessica L. Abbate, Pierre Becquart, Eric Leroy, Vanessa O. Ezenwa,1 Benjamin Roche1 diseases (1) and the high frequency of Plasmodium An association between malaria and risk for death spp. co-infection among patients undergoing treat- among patients with Ebola virus disease has suggested ment for confirmed EVD 2( ). At the individual level, within-host interactions between Plasmodium falciparum parasites and Ebola virus. To determine whether such several retrospective epidemiology studies of pa- an interaction might also influence the probability of ac- tients undergoing treatment for confirmed EVD have quiring either infection, we used a large snapshot sur- attempted to determine whether concurrent malaria veillance study from rural Gabon to test if past exposure affects patient outcomes. In Sierra Leone (3) and at to Ebola virus is associated with current infection with 1 Ebola treatment center in Liberia (4), mortality risk Plasmodium spp. during nonepidemic conditions. We was much higher among Ebola patients who were co- found a strong positive association, on population and infected with Plasmodium parasites than among pa- individual levels, between seropositivity for antibodies tients who were not co-infected, and a study in Guin- against Ebola virus and the presence of Plasmodium ea found that adverse outcomes were higher among parasites in the blood. According to a multiple regres- EVD patients with higher P. falciparum parasite loads sion model accounting for other key variables, antibodies than among those with lower levels of parasitemia (5). against Ebola virus emerged as the strongest individual- level risk factor for acquiring malaria. Our results suggest A similar study of patients at several Ebola treatment that within-host interactions between malaria parasites centers in Liberia reported the opposite relationship, and Ebola virus may underlie epidemiologic associations. that the probability of survival for EVD patients was positively associated with both presence and level of ajor outbreaks of infections with Ebola virus, Plasmodium spp. parasitemia (6). Together, these re- Msuch as the 2014–2016 West Africa epidemic sults point to a strong potential for biological interac- and the ongoing 2018–2019 outbreak in eastern Dem- tions between Plasmodium parasites and Ebola virus ocratic Republic of the Congo, pose several obvious that may influence the severity of EVD. and immediate threats to public health. Less obvious, At the population level, interruption of normal but as concerning for public health, is the possibility public health services and disease control measures— that Ebola virus might also interact with common co- including patient avoidance of healthcare facilities— circulating infectious agents at both the population during an EVD epidemic has been projected to cause and within-host (individual) levels. Indeed, much increases in untreated cases and deaths from malaria, attention has been paid to the relationship between in addition to several otherwise preventable or treat- malaria and Ebola virus disease (EVD), primar- able diseases (7–9). Yet whether biological interac- ily because of the clinical resemblance between the 2 tions at the within-host level, such as inflammatory processes leading to prolonged post-Ebola syndrome Author affiliations: Institut de Recherche pour le Développement, symptoms common in acute EVD survivors (10), may Unité Mixte de Recherche MIVEGEC, Montpellier, France also lead to a change in malaria transmission dynam- (J.L. Abbate, P. Becquart, E. Leroy, B. Roche); Institut de ics by influencing susceptibility remains unknown. Recherche pour le Développement, Unité Mixte Internationale Knowledge of the extent of possible interactions UMMISCO, Bondy, France (J.L. Abbate, B. Roche); CIRMF, between infection with Plasmodium parasites and Franceville, Gabon (E. Leroy); University of Georgia, Athens, Ebola virus is especially helpful because geographic Georgia, USA (V.O. Ezenwa); Universidad National Autonoma de regions where prevalence of antibodies against Ebola Mexico, Mexico City, Mexico (B. Roche) DOI: https://doi.org/10.3201/eid2602.181120 1These senior authors contributed equally to this article. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 2, February 2020 229 RESEARCH virus (hereafter called Ebola antibodies) is high are The survey included questions about sociodemo- also areas of high malaria endemicity (11), particu- graphics and medical history. All participants and larly the most severe form of malaria, caused by P. nonparticipants in each village were offered informa- falciparum (12). Historically, small, typically rural, tion about the study, free medical examinations, ma- outbreaks of Ebola virus have been the norm; many laria testing, blood typing, and medicines. Refusal to such outbreaks across central Africa have been de- participate was low (≈15% of eligible persons). The scribed since 1976 (13). However, the recent occur- study protocol was approved by the Gabonese Minis- rence of large outbreaks involving multiple urban try of Health (research organization no. 00093/MSP/ centers (14,15), including thousands of survivors and SG/SGAQM) and is described elsewhere (17–20). vaccinated persons, means that any interactions with malaria parasites have the potential to affect larger Individual Pathogen Exposure and Cofactors populations than in prior decades. Furthermore, it is Study volunteers were tested for previous exposure to estimated that less than half of the cross-species trans- Ebola virus by use of a Zaire ebolavirus (ZEBOV) IgG– mission events leading to a human EVD case are cor- specific ELISA 17( ,18). Current infection with Plasmo- rectly identified by current surveillance systems, sug- dium spp. was tested by using an in-field blood smear gesting that most of these events are treated locally as (17,18) and by high-throughput targeted sequencing an unknown fever or malaria (16). of Plasmodium-specific cytochrome b mitochondrial To investigate the potential epidemiologic links DNA to identify species (single and mixed infections between Ebola virus exposure and malaria parasites, of P. falciparum, P. malariae, and P. ovale were identi- we took advantage of a large snapshot surveillance fied) (19). For purposes of this study, we considered a study of 4,272 adults from 210 villages across Gabon, person to be infected with malaria parasites if either conducted during 2005–2008 (17–19), to test for popu- blood smear or sequence amplification was positive lationwide and individual associations between the (irrespective of the species) and to not be infected if 2 infections during nonepidemic conditions. At both both test results were negative. levels, we also tested for key cofactors that might In addition to participant sex and age group influence detection of an association. With an Ebola (16–30, 31–45, 46–60, >60 years), information was ob- antibody seroprevalence of 15.3% (17,18) and Plasmo- tained about several cofactors that could be indica- dium spp. prevalence of 52.1% (19), our study popula- tive of heterogeneous exposure or susceptibility to tion offered the unique opportunity for testing such both infections (17,18). These cofactors included the a link. presence of concurrent filarial worm infection (Loa loa and Mansonella perstans, each identified from blood Materials and Methods samples as described in [20]), sickle cell hemoglobin genotype (carriers vs. noncarriers, as determined in Study Population and Survey Methods [21]), participant education level (classified as less Our study was based on data previously generated than secondary education or secondary education from a snapshot surveillance study in rural Gabon and above, serving as a proxy for socioeconomic sta- (17–21). That study was conducted across 210 rural tus), participant regular contact with wild animals (population <300) villages in Gabon, located across through primary occupation (classified as hunters or a variety of open and forested habitats, and was de- nonhunters), the keeping of wild animals as pets (yes signed specifically to test for the prevalence of unde- or no), and specific exposure to bats by consumption tected exposure to Ebola virus (17,18). Villages were (yes or no). selected by using a stratified random sampling meth- od based on Gabon’s 9 administrative provinces; each Population Cofactors province was surveyed once during 1-month field For determination of population-level influences missions from July 2005 through May 2008, generally on patterns of pathogen exposure, factors common during the dry season. All but 5 of Gabon’s 49 admin- to all persons in a given department or village were istrative departments (grouping villages within prov- also examined. We obtained population density (no. inces) were represented (Appendix Figure 1, https:// persons/km2) at the department level by dividing wwwnc.cdc.gov/EID/article/26/2/18-1120-App1. population size (no. inhabitants/department based pdf). In each village, all permanent residents >15 years on 2003 national census data, https://www.city- of age were solicited for participation in the study if population.de/php/gabon-admin.php) by depart- they were willing to complete a 2-page survey and ment area (km2). Average household wealth and provide a blood sample along with written consent. frequency of insecticide-treated mosquito net (ITN) 230 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 26, No. 2,
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