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      Prevalence and molecular characterization of ticks and tick-borne pathogens of one-humped camels ( Camelus dromedarius) in Nigeria

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          Abstract

          Background

          Ticks are hematophagous arthropods responsible for maintenance and transmission of several pathogens of veterinary and medical importance. Current knowledge on species diversity and pathogens transmitted by ticks infesting camels in Nigeria is limited. Therefore, the aim of this study was to unravel the status of ticks and tick-borne pathogens of camels in Nigeria.

          Methods

          Blood samples ( n = 176) and adult ticks ( n = 593) were collected from one-humped camels ( Camelus dromedarius) of both sexes in three locations (Kano, Jigawa and Sokoto states) in north-western Nigeria and screened for the presence of Rickettsia spp., Babesia spp., Anaplasma marginale, Anaplasma spp. and Coxiella-like organisms using molecular techniques. All ticks were identified to species level using a combination of morphological and molecular methods.

          Results

          Ticks comprised the three genera Hyalomma, Amblyomma and Rhipicephalus. Hyalomma dromedarii was the most frequently detected tick species ( n = 465; 78.4%) while Amblyomma variegatum ( n = 1; 0.2%) and Rhipicephalus evertsi evertsi ( n = 1; 0.2%) were less frequent. Other tick species included H. truncatum ( n = 87; 14.7%), H. rufipes ( n = 19; 3.2%), H. impeltatum ( n = 18; 3.0%) and H. impressum ( n = 2; 0.3%). The minimum infection rates of tick-borne pathogens in 231 tick pools included Rickettsia aeschlimannii ( n = 51; 8.6%); Babesia species, ( n = 4; 0.7%) comprising of B. occultans ( n = 2), B. caballi ( n = 1) and Babesia sp. ( n = 1); Coxiella burnetii ( n = 17; 2.9%); and endosymbionts in ticks ( n = 62; 10.5%). We detected DNA of “ Candidatus Anaplasma camelli” in 40.3% of the blood samples of camels. Other tick-borne pathogens including Anaplasma marginale were not detected. Analysis of risk factors associated with both tick infestation and infection with Anaplasma spp. in the blood indicated that age and body condition scores of the camels were significant ( P < 0.05) risk factors while gender was not.

          Conclusions

          This study reports low to moderate prevalence rates of selected tick-borne pathogens associated with camels and their ticks in north-western Nigeria. The presence of zoonotic R. aeschlimannii emphasizes the need for a concerted tick control programme in Nigeria.

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          Most cited references 68

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          16S ribosomal DNA amplification for phylogenetic study.

          A set of oligonucleotide primers capable of initiating enzymatic amplification (polymerase chain reaction) on a phylogenetically and taxonomically wide range of bacteria is described along with methods for their use and examples. One pair of primers is capable of amplifying nearly full-length 16S ribosomal DNA (rDNA) from many bacterial genera; the additional primers are useful for various exceptional sequences. Methods for purification of amplified material, direct sequencing, cloning, sequencing, and transcription are outlined. An obligate intracellular parasite of bovine erythrocytes, Anaplasma marginale, is used as an example; its 16S rDNA was amplified, cloned, sequenced, and phylogenetically placed. Anaplasmas are related to the genera Rickettsia and Ehrlichia. In addition, 16S rDNAs from several species were readily amplified from material found in lyophilized ampoules from the American Type Culture Collection. By use of this method, the phylogenetic study of extremely fastidious or highly pathogenic bacterial species can be carried out without the need to culture them. In theory, any gene segment for which polymerase chain reaction primer design is possible can be derived from a readily obtainable lyophilized bacterial culture.
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            Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes.

            DNA sequences from specific genes, amplified by the polymerase chain reaction technique, were used as substrata for nonisotopic restriction endonuclease fragment length polymorphism differentiation of rickettsial species and genotypes. The products amplified using a single pair of oligonucleotide primers (derived from a rickettsial citrate synthase gene sequence) and cleaved with restriction endonucleases were used to differentiate almost all recognized species of rickettsiae. A second set of primers was used for differentiation of all recognized species of closely related spotted fever group rickettsiae. The procedure circumvents many technical obstacles previously associated with identification of rickettsial species. Multiple amplified DNA digest patterns were used to estimate the intraspecies nucleotide sequence divergence for the genes coding for rickettsial citrate synthase and a large antigen-coding gene of the spotted fever group rickettsiae. The estimated relationships deduced from these genotypic data correlate reasonably well with established rickettsial taxonomic schemes.
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              Phylogeny of hard- and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences.

               W Black,  J Piesman (1994)
              Ticks are parasitiform mites that are obligate hematophagous ectoparasites of amphibians, reptiles, birds, and mammals. A phylogeny for tick families, subfamilies, and genera has been described based on morphological characters, life histories, and host associations. To test the existing phylogeny, we sequenced approximately 460 bp from the 3' end of the mitochondrial 16S rRNA gene (rDNA) in 36 hard- and soft-tick species; a mesostigmatid mite, Dermanyssus gallinae, was used as an outgroup. Phylogenies derived using distance, maximum-parsimony, or maximum-likelihood methods were congruent. The existing phylogeny was largely supported with four exceptions. In hard ticks (Ixodidae), members of Haemaphysalinae were monophyletic with the primitive Amblyomminae and members of Hyalomminae grouped within the Rhipicephalinae. In soft ticks (Argasidae), the derived phylogeny failed to support a monophyletic relationship among members of Ornithodorinae and supported placement of Argasinae as basal to the Ixodidae, suggesting that hard ticks may have originated from an Argas-like ancestor. Because most Argas species are obligate bird octoparasites, this result supports earlier suggestions that hard ticks did not evolve until the late Cretaceous.
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                Author and article information

                Contributors
                et.onyiche@unimaid.edu.ng
                cristian.raileanu@fli.de
                oliver.tauchmann@fli.de
                susanne.fischer@fli.de
                ana.vasic@fli.de
                mandy.schaefer@fli.de
                biuvet@yahoo.com
                ogoendy@yahoo.com
                oriel.thekisoe@nwu.ac.za
                cornelia.silaghi@fli.de
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                24 August 2020
                24 August 2020
                2020
                : 13
                Affiliations
                [1 ]GRID grid.417834.d, Institute of Infectology, , Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, ; Südufer 10, 17493 Greifswald-Insel Riems, Germany
                [2 ]GRID grid.25881.36, ISNI 0000 0000 9769 2525, Unit for Environmental Sciences and Management, , North-West University, ; Potchefstroom Campus, Private Bag X6001, Potchefstroom, 2520 South Africa
                [3 ]GRID grid.413017.0, ISNI 0000 0000 9001 9645, Department of Veterinary Parasitology and Entomology, , University of Maiduguri, ; P. M. B. 1069, Maiduguri, 600230 Nigeria
                [4 ]GRID grid.419813.6, Parasitology Division, , National Veterinary Research Institute, ; Vom, Plateau State Nigeria
                [5 ]GRID grid.5603.0, Department of Biology, , University of Greifswald, ; Domstrasse 11, 17489 Greifswald, Germany
                Article
                4272
                10.1186/s13071-020-04272-2
                7445909
                32838795
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001655, Deutscher Akademischer Austauschdienst;
                Award ID: 91709125
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology

                ticks, tick-borne pathogens, piroplasms, “candidatus anaplasma camelli”, camels, nigeria

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