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      Culex species diversity, susceptibility to insecticides and role as potential vector of Lymphatic filariasis in the city of Yaoundé, Cameroon

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          Abstract

          Background

          Culex species are widespread across Cameroon and responsible for high burden of nuisance in most urban settings. However, despite their high nuisance, they remain less studied compared to anophelines. The present study aimed to assess Culex species distribution, susceptibility to insecticide, bionomics and role in Lymphatic Filariasis (LF) transmission in the city of Yaoundé.

          Methods

          Mosquito collections were conducted from March to December 2017 using Centre for Disease Control light traps (CDC-LT), human landing catches (HLC) and larval collections. Mosquitoes were identified using morphological identification keys. Mosquitoes from the Culex pipiens complex were further identified using Polymerase Chain Reaction (PCR) to assess the presence of sibling species. Bioassays were conducted with 2–5 day-old unfed females to assess mosquito susceptibility to DDT, permethrin, deltamethrin and bendiocarb following WHO guidelines. Dead, control and surviving mosquitoes from bioassays were screened by PCR to detect the presence of knockdown resistance ( kdr) alleles. Pools of mosquitoes were examined by PCR to detect the presence of Wuchereria bancrofti.

          Results

          A total of 197,956 mosquitoes belonging to thirteen species were collected. The density of mosquito collected varied according to the collection methods, districts and seasons. Culex quinquefasciatus emerged as the most abundant and the only species of the Culex pipiens complex in Yaoundé. Culex species were found breeding in different types of breeding sites including polluted and unpolluted sites. All Culex species including Cx antennatus, Cx duttoni, Cx perfuscus and Cx tigripes were found to be highly resistant to permethrin, deltamethrin and DDT. Culex quinquefasciatus was also found to be resistant to bendiocarb. A high frequency of the West Africa kdr allele was recorded in resistant Cx. quinquefasciatus. Out of the 247 pooled samples of 25 Culex spp. examined for the presence of Wuchereria bancrofti, none was found infected.

          Conclusion

          The study confirms the high adaptation of Culex species particularly Culex quinquefasciatus to the urban environment and no implication of this species in the transmission of LF in Yaoundé Cameroon. Culex species predominance in urban settings highlight potential transmission risk of West Nile and rift valley fever in Yaoundé.

          Author summary

          Culex species are highly prevalent in both urban and rural settings in Cameroon and are responsible for high nuisance and transmission of pathogens such as Wuchereria bancrofti and arbovirus. Despite the important epidemiological role, that Culex could play, they are still less studied. The current study was conducted to assess Culex species distribution, susceptibility to insecticide and role in W. bancrofti transmission in the city of Yaoundé. Mosquito collection was conducted using three collection methods human landing catches, CDC light traps and larval collection. Once collected, mosquitoes were identified using morphological identification keys and PCR diagnostic tools. They were later processed to determine their infection status. Bioassays with Culex females of 2 to 5 days old were conducted to determine their susceptibility level to different insecticide families. Culex quinquefasciatus emerged as the most abundant species. Up to 13 different culicine species were recorded. Culex species were recorded to be highly resistant to DDT, permethrin and deltamethrin. A high frequency of the West Africa kdr allele was recorded. No mosquito was detected to be infected by LF.

          The study confirms the need for further xenomonitoring activities in order to control the risk of outbreaks due to Culex mosquitoes in the city of Yaoundé.

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          Most cited references57

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          Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics.

          Xenobiotic resistance in insects has evolved predominantly by increasing the metabolic capability of detoxificative systems and/or reducing xenobiotic target site sensitivity. In contrast to the limited range of nucleotide changes that lead to target site insensitivity, many molecular mechanisms lead to enhancements in xenobiotic metabolism. The genomic changes that lead to amplification, overexpression, and coding sequence variation in the three major groups of genes encoding metabolic enzymes, i.e., cytochrome P450 monooxygenases (P450s), esterases, and glutathione-S-transferases (GSTs), are the focus of this review. A substantial number of the adaptive genomic changes associated with insecticide resistance that have been characterized to date are transposon mediated. Several lines of evidence suggest that P450 genes involved in insecticide resistance, and perhaps insecticide detoxification genes in general, may share an evolutionary association with genes involved in allelochemical metabolism. Differences in the selective regime imposed by allelochemicals and insecticides may account for the relative importance of regulatory or structural mutations in conferring resistance.
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            "Bird biting" mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology.

            The transmission of vector-borne pathogens is greatly influenced by the ecology of their vector, which is in turn shaped by genetic ancestry, the environment, and the hosts that are fed on. One group of vectors, the mosquitoes in the Culex pipiens complex, play key roles in the transmission of a range of pathogens including several viruses such as West Nile and St. Louis encephalitis viruses, avian malaria (Plasmodium spp.), and filarial worms. The Cx. pipiens complex includes Culex pipiens pipiens with two forms, pipiens and molestus, Culex pipiens pallens, Culex quinquefasciatus, Culex australicus, and Culex globocoxitus. While several members of the complex have limited geographic distributions, Cx. pipienspipiens and Cx. quinquefasciatus are found in all known urban and sub-urban temperate and tropical regions, respectively, across the world, where they are often principal disease vectors. In addition, hybrids are common in areas of overlap. Although gaps in our knowledge still remain, the advent of genetic tools has greatly enhanced our understanding of the history of speciation, domestication, dispersal, and hybridization. We review the taxonomy, genetics, evolution, behavior, and ecology of members of the Cx. pipiens complex and their role in the transmission of medically important pathogens. The adaptation of Cx. pipiens complex mosquitoes to human-altered environments led to their global distribution through dispersal via humans and, combined with their mixed feeding patterns on birds and mammals (including humans), increased the transmission of several avian pathogens to humans. We highlight several unanswered questions that will increase our ability to control diseases transmitted by these mosquitoes. Copyright © 2011 Elsevier B.V. All rights reserved.
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              Malaria transmission in urban sub-Saharan Africa.

              The rapid increase in the world's urban population has major implications for the epidemiology of malaria. A review of malaria transmission in sub-Saharan African cities shows the strong likelihood of transmission occurring within these sprawling cities, whatever the size or characteristics of their bioecologic environment. A meta-analysis of results from studies of malaria transmission in sub-Saharan Africa shows a loose linear negative relationship between mean annual entomologic inoculation rates (EIR) and the level of urbanicity. Few studies have failed to find entomologic evidence of some transmission. Our results show mean annual EIRs of 7.1 in the city centers, 45.8 in periurban areas, and 167.7 in rural areas. The impact of urbanization in reducing transmission is more marked in areas where the mean rainfall is low and seasonal. Considerable variation in the level of transmission exists among cities and within different districts in the same city. This article presents evidence from past literature to build a conceptual framework to begin to explain this heterogeneity. The potential for malaria epidemics owing to decreasing levels of natural immunity may be offset by negative impacts of urbanization on the larval ecology of anopheline mosquitoes. Malaria control in urban environments may be simpler as a result of urbanization; however, much of what we know about malaria transmission in rural environments might not hold in the urban context.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: Methodology
                Role: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: Methodology
                Role: Data curationRole: InvestigationRole: Methodology
                Role: MethodologyRole: Supervision
                Role: MethodologyRole: Supervision
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: ValidationRole: 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
                3 April 2019
                April 2019
                : 13
                : 4
                : e0007229
                Affiliations
                [1 ] Laboratoire de Recherche sur le Paludisme, Organisation de Coordination pour la lutte Contreles Endémies en Afrique Centrale (OCEAC), Yaoundé, Cameroon
                [2 ] Faculty of Science, University of Yaoundé I, Yaoundé, Cameroon
                [3 ] Vector Borne Infectious Disease Unit of the Laboratory of Applied Biology and Ecology (VBID-LABEA), Department of Animal Biology, Faculty of Science, University of Dschang, Dschang, Cameroon
                [4 ] Vector Biology Liverpool School of Tropical medicine Pembroke Place, Liverpool, United Kingdom
                Federal University of Agriculture, NIGERIA
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0073-1578
                Article
                PNTD-D-18-01548
                10.1371/journal.pntd.0007229
                6464241
                30943198
                5177e4d8-148c-4c6a-ae89-49ac827e7d8f
                © 2019 Nchoutpouen 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 2018
                : 10 February 2019
                Page count
                Figures: 3, Tables: 4, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100004440, Wellcome Trust;
                Award ID: 202687/Z/16/Z
                Award Recipient :
                CAN received funding from the Wellcome Trust Senior Fellowship in Public Health and Tropical Medicine grants N° 202687/Z/16/Z https://wellcome.ac.uk/ The funding body did not had any role in the design, collection of data, analysis and interpretation of data and in writing of the manuscript.
                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
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Culex Quinquefasciatus
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Mosquitoes
                Culex Quinquefasciatus
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Mosquitoes
                Culex Quinquefasciatus
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Nematoda
                Wuchereria
                Wuchereria Bancrofti
                People and Places
                Geographical Locations
                Africa
                Cameroon
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Agriculture
                Agrochemicals
                Insecticides
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Death Rates
                Custom metadata
                vor-update-to-uncorrected-proof
                2019-04-15
                All relevant data are within the manuscript and its Supporting Information files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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