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      The environmental drivers of bacterial meningitis epidemics in the Democratic Republic of Congo, central Africa

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          Abstract

          Introduction

          Bacterial meningitis still constitutes an important threat in Africa. In the meningitis belt, a clear seasonal pattern in the incidence of meningococcal disease during the dry season has been previously correlated with several environmental parameters like dust and sand particles as well as the Harmattan winds. In parallel, the evidence of seasonality in meningitis dynamics and its environmental variables remain poorly studied outside the meningitis belt. This study explores several environmental factors associated with meningitis cases in the Democratic Republic of Congo (DRC), central Africa, outside the meningitis belt area.

          Methods

          Non-parametric Kruskal-Wallis’ tests were used to establish the difference between the different health zones, climate and vegetation types in relation to both the number of cases and attack rates for the period 2000–2018. The relationships between the number of meningitis cases for the different health zones and environmental and socio-economical parameters collected were modeled using different generalized linear (GLMs) and generalized linear mixed models (GLMMs), and different error structure in the different models, i.e., Poisson, binomial negative, zero-inflated binomial negative and more elaborated multi-hierarchical zero-inflated binomial negative models, with randomization of certain parameters or factors (health zones, vegetation and climate types). Comparing the different statistical models, the model with the smallest Akaike’s information criterion (AIC) were selected as the best ones. 515 different health zones from 26 distinct provinces were considered for the construction of the different GLM and GLMM models.

          Results

          Non-parametric bivariate statistics showed that there were more meningitis cases in urban health zones than in rural conditions ( χ 2 = 6.910, p-value = 0.009), in areas dominated by savannah landscape than in areas with dense forest or forest in mountainous areas ( χ 2 = 15.185, p-value = 0.001), and with no significant difference between climate types ( χ 2 = 1.211, p-value = 0,449). Additionally, no significant difference was observed for attack rate between the two types of heath zones ( χ 2 = 0.982, p-value = 0.322). Conversely, strong differences in attack rate values were obtained for vegetation types ( χ 2 = 13.627, p-value = 0,001) and climate types ( χ 2 = 13.627, p-value = 0,001). This work demonstrates that, all other parameters kept constant, an urban health zone located at high latitude and longitude eastwards, located at low-altitude like in valley ecosystems predominantly covered by savannah biome, with a humid tropical climate are at higher risk for the development of meningitis. In addition, the regions with mean range temperature and a population with a low index of economic well-being (IEW) constitute the perfect conditions for the development of meningitis in DRC.

          Conclusion

          In a context of global environmental change, particularly climate change, our findings tend to show that an interplay of different environmental and socio-economic drivers are important to consider in the epidemiology of bacterial meningitis epidemics in DRC. This information is important to help improving meningitis control strategies in a large country located outside of the so-called meningitis belt.

          Author summary

          Bacterial meningitis remains an international public health threat. The most affected area worldwide is the Sahelian region between Senegal and Ethiopia called the meningitis belt. In parallel recurrent epidemics have also occurred out of the belt in Africa for the last twenty years. While environmental, socioeconomic and demographic factors are well described to explain the epidemiology of meningitis in the belt, very few studies have focused on the role of these factors to understand meningitis epidemics outside of the belt. Based on epidemiological, socio-economic, demographic and environmental data collected for the period 2000–2018 in the Democratic Republic of Congo (DRC), we used different statistical methods to explore the links between meningitis cases and the different explored factors. Our results showed that urbanized areas where populations have a low economic index of well-being, high latitude and longitude eastwards, medium to low altitude level, savannah-type vegetation, medium temperature value, are risk factors of meningitis outbreaks from North to South in the DRC. This information is important to help improving meningitis control strategies in a large country located outside the so-called meningitis belt.

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          Most cited references33

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          Impact of climate change on human infectious diseases: Empirical evidence and human adaptation.

          Climate change refers to long-term shifts in weather conditions and patterns of extreme weather events. It may lead to changes in health threat to human beings, multiplying existing health problems. This review examines the scientific evidences on the impact of climate change on human infectious diseases. It identifies research progress and gaps on how human society may respond to, adapt to, and prepare for the related changes. Based on a survey of related publications between 1990 and 2015, the terms used for literature selection reflect three aspects--the components of infectious diseases, climate variables, and selected infectious diseases. Humans' vulnerability to the potential health impacts by climate change is evident in literature. As an active agent, human beings may control the related health effects that may be effectively controlled through adopting proactive measures, including better understanding of the climate change patterns and of the compound disease-specific health effects, and effective allocation of technologies and resources to promote healthy lifestyles and public awareness. The following adaptation measures are recommended: 1) to go beyond empirical observations of the association between climate change and infectious diseases and develop more scientific explanations, 2) to improve the prediction of spatial-temporal process of climate change and the associated shifts in infectious diseases at various spatial and temporal scales, and 3) to establish locally effective early warning systems for the health effects of predicated climate change.
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            Climate change impacts in Sub-Saharan Africa: from physical changes to their social repercussions

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              Impact of MenAfriVac in nine countries of the African meningitis belt, 2010-15: an analysis of surveillance data.

              In preparation for the introduction of MenAfriVac, a meningococcal group A conjugate vaccine developed for the African meningitis belt, an enhanced meningitis surveillance network was established. We analysed surveillance data on suspected and confirmed cases of meningitis to quantify vaccine impact.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: MethodologyRole: Writing – review & editing
                Role: Conceptualization
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                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
                7 October 2020
                October 2020
                : 14
                : 10
                : e0008634
                Affiliations
                [1 ] Département de Microbiologie, Faculté de Médecine, Université de Kinshasa, Kinshasa, Democratic Republic of Congo
                [2 ] MIVEGEC, IRD, CNRS, Université de Montpellier, Montpellier, France
                [3 ] Département de Parasitologie-Mycologie, Faculté de Médecine, Université Cheikh Anta Diop (UCAD), Dakar, Sénégal
                [4 ] Centre de Recherche en Evolution et Ecologie de la Santé (CREES), Montpellier, France
                [5 ] Chrono-Environnement, UMR CNRS 6249 Université de Franche-Comté, Besançon, France
                [6 ] ASTRE, INRAE, Cirad, Université de Montpellier, Campus International de Baillarguet, Montpellier, France
                [7 ] oneHEALTH Global Research Programme, FutureEarth programme, Paris, France
                University of Washington, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-2176-2261
                Article
                PNTD-D-19-01692
                10.1371/journal.pntd.0008634
                7540884
                33027266
                5a0a3fdf-040a-4253-abd5-be996e20d16f
                © 2020 Mazamay 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
                : 18 October 2019
                : 23 July 2020
                Page count
                Figures: 1, Tables: 2, Pages: 16
                Funding
                The NGO « Organisation pour le Développement Durable de Mai-ndombe » (NGO ODDM), the URF-ECMI (Training and Research Unit in Ecology of infectious diseases, Medicine Faculty, University of Kinshasa, DRC) and IRD/MIVEGEC, UMR CNRS IRD UM, Montpellier, France. Jean-François Guégan is supported by an “Investissement d’Avenir” grant managed by Agence Nationale de la Recherche (LABEX CEBA: ANR-10-LABX-25-01), and is also supported by Institut de recherche pour le développement (IRD), Institut national de recherche pour l’agriculture, l’alimentation et l’environnement (INRAE), Université de Montpellier and Ecole des Hautes Etudes en Santé Publique (EHESP). 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
                Medical Conditions
                Infectious Diseases
                Infectious Diseases of the Nervous System
                Meningitis
                Medicine and Health Sciences
                Neurology
                Infectious Diseases of the Nervous System
                Meningitis
                Medicine and Health Sciences
                Medical Conditions
                Inflammatory Diseases
                Meningitis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Bacterial Diseases
                Bacterial Meningitis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Infectious Diseases of the Nervous System
                Meningitis
                Bacterial Meningitis
                Medicine and Health Sciences
                Neurology
                Infectious Diseases of the Nervous System
                Meningitis
                Bacterial Meningitis
                Medicine and Health Sciences
                Medical Conditions
                Inflammatory Diseases
                Meningitis
                Bacterial Meningitis
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                Epidemiology
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                Ecology and Environmental Sciences
                Terrestrial Environments
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                Infectious disease & Microbiology
                Infectious disease & Microbiology

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