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      Culicoides Latreille (Diptera: Ceratopogonidae) as potential vectors for Leishmania martiniquensis and Trypanosoma sp. in northern Thailand

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          Abstract

          Biting midges of genus Culicoides (Diptera: Ceratopogonidae) are the vectors of several pathogenic arboviruses and parasites of humans and animals. Several reports have suggested that biting midges might be a potential vector of Leishmania parasites. In this study, we screened for Leishmania and Trypanosoma DNA in biting midges collected from near the home of a leishmaniasis patient in Lamphun province, northern Thailand by using UV-CDC light traps. The identification of biting midge species was based on morphological characters and confirmed using the Cytochrome C oxidase subunit I ( COI) gene. The detection of Leishmania and Trypanosoma DNA was performed by amplifying the internal transcribed spacer 1 ( ITS1) and small subunit ribosomal RNA ( SSU rRNA) genes, respectively. All the amplified PCR amplicons were cloned and sequenced. The collected 223 biting midges belonged to seven species ( Culicoides mahasarakhamense, C. guttifer, C. innoxius, C. sumatrae, C. huffi, C. oxystoma, and C. palpifer). The dominant species found in this study was C. mahasarakhamense (47.53%). Leishmania martiniquensis DNA was detected in three samples of 106 specimens of C. mahasarakhamense tested indicating a field infection rate of 2.83%, which is comparable to reported rates in local phlebotomines. Moreover, we also detected Trypanosoma sp. DNA in one sample of C. huffi. To our knowledge, this is the first molecular detection of L. martiniquensis in C. mahasarakhamense as well as the first detection of avian Trypanosoma in C. huffi. Blood meal analysis of engorged specimens of C. mahasarakhamense, C. guttifer, and C. huffi revealed that all specimens had fed on avian, however, further studies of the host ranges of Culicoides are needed to gain a better insight of potential vectors of emerging leishmaniasis. Clarification of the vectors of these parasites is also important to provide tools to establish effective disease prevention and control programs in Thailand.

          Author summary

          Culicoides are known to be vectors of several pathogens, including arboviruses and parasites. However, other investigations have demonstrated that Culicoides could be involved in the transmission of Leishmania and Trypanosoma parasites. Our studies demonstrated the first detection of L. martiniquensis in Culicoides mahasarakhamense and Trypanosoma sp., which is closely related to avian Trypanosome in C. huffi from an endemic area of leishmaniasis in northern Thailand. The finding of this work suggested that Culicoides biting midges are suspected to be the potential vector of L. martiniquensis and Trypanosoma parasites in Thailand.

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          Most cited references57

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          The Molecular Evolutionary Genetics Analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.
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            DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates.

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            We describe "universal" DNA primers for polymerase chain reaction (PCR) amplification of a 710-bp fragment of the mitochondrial cytochrome c oxidase subunit I gene (COI) from 11 invertebrate phyla: Echinodermata, Mollusca, Annelida, Pogonophora, Arthropoda, Nemertinea, Echiura, Sipuncula, Platyhelminthes, Tardigrada, and Coelenterata, as well as the putative phylum Vestimentifera. Preliminary comparisons revealed that these COI primers generate informative sequences for phylogenetic analyses at the species and higher taxonomic levels.
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                Author and article information

                Contributors
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draft
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: Investigation
                Role: Methodology
                Role: Methodology
                Role: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                15 December 2021
                December 2021
                : 15
                : 12
                : e0010014
                Affiliations
                [1 ] Program in Medical Science, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand
                [2 ] Vector Biology and Vector Borne Disease Research Unit, Department of Parasitology, Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand
                [3 ] Department of Agricultural Technology, Ramkhamhaeng University, Bangkok, Thailand
                [4 ] Department of Medical Technology, School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat, Thailand
                [5 ] Research Excellence Center for Innovation and Health Products, Walailak University, Nakhon Si Thammarat, Thailand
                [6 ] Excellent Center for Dengue and Community Public Health (EC for DACH), Walailak University, Nakhon Si Thammarat, Thailand
                [7 ] Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, Australia
                Centre hospitalier de Cayenne, FRANCE
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-0223-8787
                https://orcid.org/0000-0002-7648-5871
                https://orcid.org/0000-0001-8243-7406
                https://orcid.org/0000-0003-2876-8268
                https://orcid.org/0000-0002-0266-2433
                https://orcid.org/0000-0002-9248-1678
                Article
                PNTD-D-21-00999
                10.1371/journal.pntd.0010014
                8673663
                34910720
                67570872-f469-41d2-91ec-d91ccba0586d
                © 2021 Sunantaraporn 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
                : 6 July 2021
                : 20 November 2021
                Page count
                Figures: 5, Tables: 1, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100012309, royal golden jubilee (rgj) ph.d. programme;
                Award ID: (grant number PHD0035/2561)
                Award Recipient :
                Funded by: the program management unit for human resources & institutional development, research and innovation
                Award ID: (grant number B16F630071)
                Award Recipient :
                Funded by: thailand science research innovation (tsri)
                Award ID: (grant number FRB640001)
                Award Recipient :
                Funded by: ratchadapisek sompote fund, chulalongkorn university
                Award ID: (grant number CU_GR_63_97_30_04)
                Award Recipient :
                Funded by: National Research Council of Thailand
                Award ID: N35A640452
                Award Recipient :
                Funded by: NIAID
                Award ID: 07-049-7012-52338
                Award Recipient :
                Funded by: research and development institute, ramkhamhaeng university and tsri fund
                Award ID: (RU_64A112000009)
                Award Recipient :
                This research was supported by the Thailand Research Fund through the Royal Golden Jubilee Ph.D. Program (grant number PHD/0035/2561) to SS., the program Management Unit for Human Resources & Institutional Development, Research and Innovation (grant number B16F630071) to PS., Thailand Science Research Innovation (TSRI) (grant number FRB640001) to PS., Ratchadapisek Sompote Fund, Chulalongkorn University (grant number CU_GR_63_97_30_04) to PS., National Research Council of Thailand: CGEN (grant number N35A640452) to PS., and NIH/NIAID/CREID/07-049-7012-52338 to PS. The partial financial was supported from Research and Development Institute, Ramkhamhaeng University and TSRI fund (RU_64A112000009) to AT. 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
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Trypanosoma
                Biology and Life Sciences
                Zoology
                Entomology
                Insects
                Culicoides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Culicoides
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Arthropoda
                Insects
                Culicoides
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Leishmania
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Cryptic Speciation
                People and Places
                Geographical Locations
                Asia
                Thailand
                Medicine and Health Sciences
                Medical Conditions
                Tropical Diseases
                Neglected Tropical Diseases
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Protozoan Infections
                Leishmaniasis
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Zoonoses
                Leishmaniasis
                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
                Custom metadata
                All data are in the manuscript.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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