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      Evidence of transovarial transmission of Chikungunya and Dengue viruses in field-caught mosquitoes in Kenya

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          Abstract

          Arboviruses are among the most important emerging pathogens due to their increasing public health impact. In Kenya, continued population growth and associated urbanization are conducive to vector spread in both urban and rural environments, yet mechanisms of viral amplification in vector populations is often overlooked when assessing risks for outbreaks. Thus, the characterization of local arbovirus circulation in mosquito populations is imperative to better inform risk assessments and vector control practices. Aedes species mosquitoes were captured at varying stages of their life cycle during different seasons between January 2014 and May 2016 at four distinct sites in Kenya, and tested for chikungunya (CHIKV), dengue (DENV) and Zika (ZIKV) viruses by RT-PCR. CHIKV was detected in 45 (5.9%) and DENV in 3 (0.4%) mosquito pools. No ZIKV was detected. Significant regional variation in prevalence was observed, with greater frequency of CHIKV on the coast. DENV was detected exclusively on the coast. Both viruses were detected in immature mosquitoes of both sexes, providing evidence of transovarial transmission of these arboviruses in local mosquitoes. This phenomenon may be driving underlying viral maintenance that may largely contribute to periodic re-emergence among humans in Kenya.

          Author summary

          Transovarial transmission, or vertical transmission, is the spread of a pathogen from parent to offspring. It has been observed that some mosquito-borne viruses can be transmitted from female mosquitoes to their offspring during follicle development or during oviposition. The occurrence of transovarial transmission is evident in the presence of virally infected male mosquitoes, which typically do not take bloodmeals, and the presence of virus in immature mosquitoes of any sex. Transovarial transmission aids in the amplification of mosquito-borne viruses in the environment by increasing the number of infected mosquitoes in a given region, thus expanding the possibility of viral transmission to humans. The combination of transovarial transmission and the preservation of viable eggs during dry seasons may trigger sudden amplification of the virus after rainy periods, resulting in an outbreak. This study provides some of the first evidence of transovarial transmission of chikungunya and dengue viruses in Aedes aegypti mosquitoes in Africa during interepidemic periods, which has important implications for local virus persistence and epidemic patterns.

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          Most cited references71

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          A new, cost-effective, battery-powered aspirator for adult mosquito collections.

          We report the development of a new mosquito aspirator with the same aspiration capacity (airflow) of the CDC Backpack Aspirator (CDC-BP), but smaller and lighter (0.8 kg without battery), less expensive (US$45-70), easier to build, and compatible with the use of telescoping extension poles to access hard-to-reach locations. The performance of this new aspirator, named "Prokopack," was compared with the CDC-BP in laboratory settings as well as in paired collections in combined sewer overflow (CSO) tunnels in Atlanta, GA, and indoor mosquito collections in Iquitos, Peru. The difference in suction power between both aspirators (average, 0.29-0.43 m/s) was negligible. However, 2.3 times more mosquitoes were collected using the Prokopack in the upper wall (>1.5 m) and ceilings of CSO tunnels than with the CDC-BP in lower walls. Indoor collection in Iquitos yielded significantly more total mosquito numbers [including Culex pipiens complex, Culex (melanoconion) sp., and Mansonia sp.] and Aedes aegypti (L.) in the Prokopack than in the CDC-BP. Our results demonstrate the effectiveness of the Prokopack to collect different mosquito species in different epidemiological settings.
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            Seroprevalence of Chikungunya virus (CHIKV) infection on Lamu Island, Kenya, October 2004.

            An outbreak of Chikungunya virus (CHIKV) disease associated with high fever and severe protracted arthralgias was detected in Lamu, Kenya, peaking in July 2004. At least 1,300 cases were documented. We conducted a seroprevalence study to define the magnitude of transmission on Lamu Island. We conducted a systematic cross-sectional survey. We administered questionnaires and tested 288 sera from Lamu residents for IgM and IgG antibodies to CHIKV. Chikungunya virus infection (seropositivity) was defined as a person with IgG and/or IgM antibodies to CHIKV. IgM antibodies to CHIKV were detected in 18% (53/288) and IgG antibodies in 72% (206/288); IgM and/or IgG antibodies were present in 75% (215/288). The seroprevalence findings suggested that the outbreak was widespread, affecting 75% of the Lamu population; extrapolating the findings to the entire population, 13,500 (95% CI, 12,458-14328) were affected. Vector control strategies are needed to control the spread of this mosquito-borne infection.
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              Worldwide patterns of genetic differentiation imply multiple 'domestications' of Aedes aegypti, a major vector of human diseases.

              Understanding the processes by which species colonize and adapt to human habitats is particularly important in the case of disease-vectoring arthropods. The mosquito species Aedes aegypti, a major vector of dengue and yellow fever viruses, probably originated as a wild, zoophilic species in sub-Saharan Africa, where some populations still breed in tree holes in forested habitats. Many populations of the species, however, have evolved to thrive in human habitats and to bite humans. This includes some populations within Africa as well as almost all those outside Africa. It is not clear whether all domestic populations are genetically related and represent a single 'domestication' event, or whether association with human habitats has developed multiple times independently within the species. To test the hypotheses above, we screened 24 worldwide population samples of Ae. aegypti at 12 polymorphic microsatellite loci. We identified two distinct genetic clusters: one included all domestic populations outside of Africa and the other included both domestic and forest populations within Africa. This suggests that human association in Africa occurred independently from that in domestic populations across the rest of the world. Additionally, measures of genetic diversity support Ae. aegypti in Africa as the ancestral form of the species. Individuals from domestic populations outside Africa can reliably be assigned back to their population of origin, which will help determine the origins of new introductions of Ae. aegypti.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Investigation
                Role: Data curationRole: Investigation
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Methodology
                Role: Investigation
                Role: Investigation
                Role: Formal analysisRole: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: 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
                19 June 2020
                June 2020
                : 14
                : 6
                : e0008362
                Affiliations
                [1 ] Stanford University School of Medicine, Stanford, California, United States of America
                [2 ] Kenya Medical Research Institute, Kisumu, Kenya
                [3 ] Technical University of Mombasa, Mombasa, Kenya
                [4 ] Chuka University, Chuka, Kenya
                [5 ] Vector Borne Disease Unit, Msambweni, Kenya
                [6 ] Emory University, Atlanta, Georgia, United States of America
                [7 ] San Mateo County Mosquito and Vector Control District, Burlingame, California, United States of America
                [8 ] Case Western Reserve University, Cleveland, Ohio, United States of America
                University of Wisconsin Madison, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-2719-1973
                Article
                PNTD-D-19-01669
                10.1371/journal.pntd.0008362
                7329127
                32559197
                1db36336-f7fe-494b-a50a-d9eb6832ebb8
                © 2020 Heath 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
                : 7 October 2019
                : 4 May 2020
                Page count
                Figures: 3, Tables: 3, Pages: 17
                Funding
                Funded by: National Institutes of Health (US)
                Award ID: R01AI102918
                Award Recipient :
                This research was supported by National Institutes of Health (NIH) grant R01AI102918 (ADL). The funders had no role in the collection, analysis, or reporting of the data.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
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                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
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                Microbiology
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                Custom metadata
                vor-update-to-uncorrected-proof
                2020-07-01
                All relevant data are available at https://purl.stanford.edu/tr890xw5305.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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