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A Retrospective Cohort Investigation of Seroprevalence of Marburg Virus and Ebolaviruses in Two Different Ecological Zones in Uganda Luke Nyakarahuka1,2* , Ilana J

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A Retrospective Cohort Investigation of Seroprevalence of Marburg Virus and Ebolaviruses in Two Different Ecological Zones in Uganda Luke Nyakarahuka1,2* , Ilana J Nyakarahuka et al. BMC Infectious Diseases (2020) 20:461 https://doi.org/10.1186/s12879-020-05187-0 RESEARCH ARTICLE Open Access A retrospective cohort investigation of seroprevalence of Marburg virus and ebolaviruses in two different ecological zones in Uganda Luke Nyakarahuka1,2* , Ilana J. Schafer3, Stephen Balinandi1, Sophia Mulei1, Alex Tumusiime1, Jackson Kyondo1, Barbara Knust3, Julius Lutwama1, Pierre Rollin3, Stuart Nichol3 and Trevor Shoemaker3 Abstract Background: Uganda has experienced seven Ebola Virus Disease (EVD) outbreaks and four Marburg Virus Disease (MVD) outbreaks between 2000 and 2019. We investigated the seroprevalence and risk factors for Marburg virus and ebolaviruses in gold mining communities around Kitaka gold mine in Western Uganda and compared them to non-mining communities in Central Uganda. Methods: A questionnaire was administered and human blood samples were collected from three exposure groups in Western Uganda (gold miners, household members of miners, non-miners living within 50 km of Kitaka mine). The unexposed controls group sampled was community members in Central Uganda far away from any gold mining activity which we considered as low-risk for filovirus infection. ELISA serology was used to analyse samples, detecting IgG antibodies against Marburg virus and ebolaviruses (filoviruses). Data were analysed in STATA software using risk ratios and odds ratios. Results: Miners in western Uganda were 5.4 times more likely to be filovirus seropositive compared to the control group in central Uganda (RR = 5.4; 95% CI 1.5–19.7) whereas people living in high-risk areas in Ibanda and Kamwenge districts were 3.6 more likely to be seropositive compared to control group in Luweeero district (RR = 3.6; 95% CI 1.1–12.2). Among all participants, filovirus seropositivity was 2.6% (19/724) of which 2.3% (17/724) were reactive to Sudan virus only and 0.1% (1/724) to Marburg virus. One individual seropositive for Sudan virus also had IgG antibodies reactive to Bundibugyo virus. The risk factors for filovirus seropositivity identified included mining (AOR = 3.4; 95% CI 1.3–8.5), male sex (AOR = 3.1; 95% CI 1.01–9.5), going inside mines (AOR = 3.1; 95% CI 1.2–8.2), cleaning corpses (AOR = 3.1; 95% CI 1.04–9.1) and contact with suspect filovirus cases (AOR = 3.9, 95% CI 1.04–14.5). (Continued on next page) * Correspondence: [email protected]; [email protected] 1Arbovirology, Emerging and Re-emerging Diseases, Uganda Virus Research Institute , Entebbe, Uganda 2Department of Biosecurity, Ecosystems and Veterinary Public Health, College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Nyakarahuka et al. BMC Infectious Diseases (2020) 20:461 Page 2 of 9 (Continued from previous page) Conclusions: These findings indicate that filovirus outbreaks may go undetected in Uganda and people involved in artisan gold mining are more likely to be exposed to infection with either Marburg virus or ebolaviruses, likely due to increased risk of exposure to bats. This calls for active surveillance in known high-risk areas for early detection and response to prevent filovirus epidemics. Keywords: Marburg virus disease, Ebola virus disease, Filovirus, Seroprevalence, Epidemiology, Ebolaviruses, Uganda, ELISA Background Workers in the mines and communities that live in and Viruses in the genera Ebolavirus and Marburgvirus be- around this reserve were considered to be at higher risk long to the family Filoviridae and cause classical viral of exposure to filovirus infection because of the Rouset- haemorrhagic fevers (VHFs) in humans, which are asso- tus aegyptiacus bats that live in the mines, a known res- ciated with high morbidity and mortality and pose a ser- ervoir for Marburg virus. A comparison group in ious threat to human and animal populations in Luweero district was chosen as a control, unexposed endemic countries. Uganda reported 11 filovirus out- group because it is in the Central region of the country breaks from 2000 to 2019. These include seven EVD far from Kitaka and any other mines, and we hypothe- outbreaks caused by Sudan virus (6 outbreaks) and Bun- sized that Rousettus aegyptiacus bats may not inhabit dibugyo virus (one outbreak) and four Marburg virus this region due to lack of suitable habitat, no previously disease (MVD) outbreaks caused by Marburg virus and reported MVD cases, and therefore inhabitants would Ravn virus [1]. In Ibanda and neighbouring Kamwenge mostly likely be at low risk for exposure to filoviruses. districts of western Uganda, there were two documented Despite EVD being reported in Luweero district in 2011 outbreaks of MVD [2, 3] including one in which cases and 2012, the ecology of this place is different from that were gold miners in Kitaka cave [3]. Previous studies of of Ibanda and Kamwenge districts as it is not forested bats sampled from Kitaka and python caves have shown and not have suitable habitat for the putative filovirus Rousettus aegyptiacus bats to be the known reservoir for reservoirs (Fig. 1). The Luweero population was used as Marburg virus [4–6]. In 2012, the MVD outbreak investi- an unexposed group as the investigation of the previous gations in Ibanda district traced the outbreak’s origin to cases of EVD did not reveal any possible sources of virus villages near Kitaka mines where artisanal gold mining is spillover from wildlife in Luweero. practised [2]. We designed an investigation to better understand the possible link between artisanal gold min- ing activities in Kitaka and the transmission of Marburg Sampling procedure and inclusion criteria virus and ebolaviruses in Ibanda and Kamwenge dis- We sampled three groups of exposed individuals in tricts. We compared these communities with those in Ibanda and Kamwenge districts that included: 1) Arti- Luweero district where there are no mining operations sanal miners and persons that worked in the Kitaka or bat-inhabited caves, no previously identified human mines from 2007 to 2015, 2) Members of the household cases of MVD, and there is a different ecological zone. or family housing compound of a miner during the Although there have been outbreaks of EVD in Luweero period that the miner was actively working in Kitaka in 2010 and 2012, investigations did not reveal any po- mines, 3) Members of households that resided within a tential sources of spillovers in the Luweero area in terms 50 km radius from any open mining site associated with of bat-inhabited caves and forested areas (Fig. 1) and we Kitaka mines, and that were not included in above hypothesise that these cases could have been imported groups 1 or 2. This third group also acted as a control from other hotspots in Uganda. for groups 1 and 2 above to assess the risk for filovirus infection between people with direct or indirect expos- ure to the mine versus living near it. We then sampled Methods the 4th group of unexposed individuals who are residents Sampling sites, population, and hypothesis of Luweero district. The sample size needed for this Participants were sampled from Ibanda, Kamwenge and study was calculated to be 500 individuals in total. This Luweero districts (Fig. 1). The bat-inhabited Kitaka calculation included 100 persons in group ‘1’ (as listed in mines are located within the boundary of Ibanda and «Inclusion Criteria» above), 200 persons between groups Kamwenge within Kasyoha-Kitomi Forest Reserve. The ‘2’ and ‘3’ and 200 persons in group ‘4’. This calculation caves were created as a resultant of abandoned decom- was done estimating a 15% prevalence of Marburg virus missioned gold mines during colonial times, however, exposure in group ‘1,’ 5% prevalence in groups ‘2’ and ‘3, some minimal artisanal mining still happens update. ’ and 0.5% prevalence of exposure in group ‘4,’ as well as Nyakarahuka et al. BMC Infectious Diseases (2020) 20:461 Page 3 of 9 Fig. 1 Reported filovirus outbreaks, cohort investigation districts, water and forest cover of Uganda a 95% confidence interval, 80% power, and a ratio of 2 districts of Kamwenge, Ibanda and Luweero. Participants controls to each exposed person. However, because of that consented to inclusion in the study were inter- the high response rate (144.8%) during participant re- viewed to complete a risk factor questionnaire and pro- cruitment, a total of 724 individuals were sample (group vided their answers verbally. One blood sample (4 ml) 1 = 161, group 2 = 138, group 3 = 134 and group 4 = was collected from each participant for serological test- 291). For groups 1 and 2, a purposive sampling proced- ing for filovirus (marburgviruses, Sudan virus, Bundibu- ure was used with a snowball approach.
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