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      Systematic literature review of Rift Valley fever virus seroprevalence in livestock, wildlife and humans in Africa from 1968 to 2016

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          Abstract

          Background

          Rift Valley fever virus (RVFV) is a zoonotic arbovirus that causes severe disease in livestock and humans. The virus has caused recurrent outbreaks in Africa and the Arabian Peninsula since its discovery in 1931. This review sought to evaluate RVFV seroprevalence across the African continent in livestock, wildlife and humans in order to understand the spatio-temporal distribution of RVFV seroprevalence and to identify knowledge gaps and areas requiring further research. Risk factors associated with seropositivity were identified and study designs evaluated to understand the validity of their results.

          Methodology

          The Preferred Reporting of Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were used to produce a protocol to systematically search for RVFV seroprevalence studies in PubMed and Web of Science databases. The Strengthening the Reporting of Observational studies in Epidemiology (STROBE) statement guided the evaluation of study design and analyses.

          Principal findings

          A total of 174 RVFV seroprevalence studies in 126 articles fulfilled the inclusion criteria. RVFV seroprevalence was recorded in 31 African countries from 1968 to 2016 and varied by time, species and country. RVFV seroprevalence articles including either livestock and humans or livestock and wildlife seroprevalence records were limited in number (8/126). No articles considered wildlife, livestock and human seroprevalence concurrently, nor wildlife and humans alone. Many studies did not account for study design bias or the sensitivity and specificity of diagnostic tests.

          Conclusions

          Future research should focus on conducting seroprevalence studies at the wildlife, livestock and human interface to better understand the nature of cross-species transmission of RVFV. Reporting should be more transparent and biases accounted for in future seroprevalence research to understand the true burden of disease on the African continent.

          Author summary

          Rift Valley fever virus (RVFV) is a vector-borne virus that infects wildlife and livestock, and can subsequently spread to humans. Due to the nature of the disease it has the potential to cause substantial economic and public health impacts. Rift Valley Fever (RVF) has been identified in Africa and the Arabian Peninsula, but has the potential to spread more widely. This systematic review assessed the distribution of RVF in livestock and humans in Africa by collating all the relevant studies we could find, extracting the data and critically evaluating them. Understanding when and where RVF has occurred in Africa and why some animals and humans get disease helps target control strategies and, in particular, those that reduce spread from livestock to humans. Furthermore, by evaluating past studies we can ensure that future ones are more robust and reproducible, so they can help us better understand the disease.

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          Most cited references80

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          Rift Valley fever epidemic in Saudi Arabia: epidemiological, clinical, and laboratory characteristics.

          This cohort descriptive study summarizes the epidemiological, clinical, and laboratory characteristics of the Rift Valley fever (RVF) epidemic that occurred in Saudi Arabia from 26 August 2000 through 22 September 2001. A total of 886 cases were reported. Of 834 reported cases for which laboratory results were available, 81.9% were laboratory confirmed, of which 51.1% were positive for only RVF immunoglobulin M, 35.7% were positive for only RVF antigen, and 13.2% were positive for both. The mean age (+/- standard deviation) was 46.9+/-19.4 years, and the ratio of male to female patients was 4:1. Clinical and laboratory features included fever (92.6% of patients), nausea (59.4%), vomiting (52.6%), abdominal pain (38.0%), diarrhea (22.1%), jaundice (18.1%), neurological manifestations (17.1%), hemorrhagic manifestations (7.1%), vision loss or scotomas (1.5%), elevated liver enzyme levels (98%), elevated lactate dehydrogenase level (60.2%), thrombocytopenia (38.4%), leukopenia (39.7%), renal impairment or failure (27.8%), elevated creatine kinase level (27.3%), and severe anemia (15.1%). The mortality rate was 13.9%. Bleeding, neurological manifestations, and jaundice were independently associated with a high mortality rate. Patients with leukopenia had significantly a lower mortality rate than did those with a normal or high leukocyte count (2.3% vs. 27.9%; odds ratio, 0.09; 95% confidence interval, 0.01-0.63).
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            Rift Valley fever virus (family Bunyaviridae, genus Phlebovirus). Isolations from Diptera collected during an inter-epizootic period in Kenya.

            A total of 134 876 Diptera collected in Kenya during a 3-year period were tested in 3383 pools for Rift Valley fever (RVF) virus. Nineteen pools of unengorged mosquitoes were found positive for RVF. All isolations were made from specimens collected at or near the naturally or artificially flooded grassland depressions that serve as the developmental sites for the immature stages of many mosquito species. The isolation of virus from adult male and female A. lineatopennis which had been reared from field-collected larvae and pupae suggests that transovarial transmission of the virus occurs in this species.
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              An Outbreak of Rift Valley Fever in Northeastern Kenya, 1997-98

              In December 1997, 170 hemorrhagic fever-associated deaths were reported in Carissa District, Kenya. Laboratory testing identified evidence of acute Rift Valley fever virus (RVFV). Of the 171 persons enrolled in a cross-sectional study, 31(18%) were anti-RVFV immunoglobulin (Ig) M positive. An age-adjusted IgM antibody prevalence of 14% was estimated for the district. We estimate approximately 27,500 infections occurred in Garissa District, making this the largest recorded outbreak of RVFV in East Africa. In multivariate analysis, contact with sheep body fluids and sheltering livestock in one’s home were significantly associated with infection. Direct contact with animals, particularly contact with sheep body fluids, was the most important modifiable risk factor for RVFV infection. Public education during epizootics may reduce human illness and deaths associated with future outbreaks.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: VisualizationRole: 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
                23 July 2018
                July 2018
                : 12
                : 7
                : e0006627
                Affiliations
                [1 ] Transmission Biology Group, The Pirbright Institute, Pirbright, Woking, United Kingdom
                [2 ] The Jenner Institute, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
                [3 ] Biosciences Department, Kenya Medical Research Institute-Wellcome Trust Research Programme, Kilifi, Kenya
                [4 ] Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford, Oxford, United Kingdom
                [5 ] Vesicular Disease Reference Laboratories, The Pirbright Institute, Pirbright, Woking, United Kingdom
                University of California, Davis, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-9532-7927
                http://orcid.org/0000-0003-0538-4173
                Article
                PNTD-D-17-01615
                10.1371/journal.pntd.0006627
                6072204
                30036382
                7a519237-e2fe-4da2-a662-8fe2c078ea32
                © 2018 Clark 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 October 2017
                : 22 June 2018
                Page count
                Figures: 5, Tables: 4, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100001275, Oak Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000277, Department for Environment, Food and Rural Affairs;
                Award ID: SE2943
                Award Recipient :
                Funded by: Department of Health
                Award ID: GHR Project:16/107/03
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BBS/E/I/00007033
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BBS/E/I/00007036
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BBS/E/I/00007036
                Award Recipient :
                MHAC is supported by a Pirbright Institute studentship with funding from Biotechnology and Biological Sciences Research Council (BBSRC; bbsrc.ac.uk) and the Department of Health ( https://www.gov.uk/government/organisations/department-of-health; GHR Project:16/107/03 - Advanced development of a safe and effective Rift Valley Fever vaccine for livestock). This project is independent research funded by the Department of Health and funded from an ODA budget. The views expressed in this publication are those of the author(s) and not necessarily those of the Department of Health. NAL is supported by the Biotechnology and Biological Sciences Research Council (grant code: BBS/E/I/00007036). GMW is supported by an Oak Foundation fellowship ( http://oakfnd.org/). SG is supported by the Biotechnology and Biological Sciences Research Council (grant codes: BBS/E/I/00007033 and BBS/E/I/00007036). ADN is supported by the United Kingdom Department for Environment Food and Rural Affairs (Defra; http://www.defra.gov.uk) grant code: SE2943. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Bunyaviruses
                Rift Valley fever virus
                Biology and life sciences
                Microbiology
                Medical microbiology
                Microbial pathogens
                Viral pathogens
                Bunyaviruses
                Rift Valley fever virus
                Medicine and health sciences
                Pathology and laboratory medicine
                Pathogens
                Microbial pathogens
                Viral pathogens
                Bunyaviruses
                Rift Valley fever virus
                Biology and life sciences
                Organisms
                Viruses
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                Bunyaviruses
                Rift Valley fever virus
                Biology and Life Sciences
                Agriculture
                Livestock
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Animal Types
                Wildlife
                Biology and Life Sciences
                Zoology
                Animal Types
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                Research and Analysis Methods
                Research Assessment
                Systematic Reviews
                Biology and Life Sciences
                Veterinary Science
                Veterinary Diseases
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Ruminants
                Sheep
                Medicine and health sciences
                Tropical diseases
                Neglected tropical diseases
                Rift Valley fever
                Medicine and health sciences
                Infectious diseases
                Viral diseases
                Rift Valley fever
                Medicine and health sciences
                Infectious diseases
                Zoonoses
                Rift Valley fever
                People and Places
                Geographical Locations
                Africa
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-08-02
                All relevant data are within the paper and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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