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      Bacterial and protozoal pathogens found in ticks collected from humans in Corum province of Turkey

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          Abstract

          Background

          Tick-borne diseases are increasing all over the word, including Turkey. The aim of this study was to determine the bacterial and protozoan vector-borne pathogens in ticks infesting humans in the Corum province of Turkey.

          Methodology/Principal findings

          From March to November 2014 a total of 322 ticks were collected from patients who attended the local hospitals with tick bites. Ticks were screened by real time-PCR and PCR, and obtained amplicons were sequenced. The dedected tick was belonging to the genus Hyalomma, Haemaphysalis, Rhipicephalus, Dermacentor and Ixodes. A total of 17 microorganism species were identified in ticks. The most prevalent Rickettsia spp. were: R. aeschlimannii (19.5%), R. slovaca (4.5%), R. raoultii (2.2%), R. hoogstraalii (1.9%), R. sibirica subsp. mongolitimonae (1.2%), R. monacensis (0.31%), and Rickettsia spp. (1.2%). In addition, the following pathogens were identified: Borrelia afzelii (0.31%), Anaplasma spp. (0.31%), Ehrlichia spp. (0.93%), Babesia microti (0.93%), Babesia ovis (0.31%), Babesia occultans (3.4%), Theileria spp. (1.6%), Hepatozoon felis (0.31%), Hepatozoon canis (0.31%), and Hemolivia mauritanica (2.1%). All samples were negative for Francisella tularensis, Coxiella burnetii, Bartonella spp., Toxoplasma gondii and Leishmania spp.

          Conclusions/Significance

          Ticks in Corum carry a large variety of human and zoonotic pathogens that were detected not only in known vectors, but showed a wider vector diversity. There is an increase in the prevalence of ticks infected with the spotted fever group and lymphangitis-associated rickettsiosis, while Ehrlichia spp. and Anaplasma spp. were reported for the first time from this region. B. microti was detected for the first time in Hyalomma marginatum infesting humans. The detection of B. occultans, B. ovis, Hepatozoon spp., Theileria spp. and Hemolivia mauritanica indicate the importance of these ticks as vectors of pathogens of veterinary importance, therefore patients with a tick infestation should be followed for a variety of pathogens with medical importance.

          Author summary

          Ticks are important vectors for different kind of pathogens, both of medical and veterinary importance, while tick-borne diseases (TBDs) are increasing all over the world. In Turkey, many important human and zoonotic TBDs such as, Lyme borreliosis, rickettsiosis, anaplasmosis, ehrlichiosis, tularemia, bartonellosis, babesiosis, theileriosis, and hepatozoonosis have been reported. Nonetheless, there is lack of research-based information concerning the epidemiology, ecology, and vector diversity of these tick-borne pathogens. In this study, we aimed to investigate broad-range bacterial and protozoan vector-borne pathogens by PCR/RT-PCR and sequencing, those ticks infesting humans in the Corum province. Spotted fever group rickettsiae and lymphangitis-associated rickettsiae, Borrelia afzelii, Anaplasma spp., Ehrlichia spp. were detected. Babesia microti was detected in Hyalomma marginatum infesting humans. Interestingly zoonotic pathogens like Babesia ovis, Babesia occultans, Theileria spp, Hepatozoon felis, Hepatozoon canis, and Hemolivia mauritanica were also detected, showing the role of ticks for diseases also of veterinary importance. This study provides important data for understanding the epidemiology of tick-borne pathogens and it is hoped that these results will challenge clinicians and veterinarians to unify their efforts in the management of TBDs.

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          Most cited references97

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          Ticks and tickborne bacterial diseases in humans: an emerging infectious threat.

          Ticks are currently considered to be second only to mosquitoes as vectors of human infectious diseases in the world. Each tick species has preferred environmental conditions and biotopes that determine the geographic distribution of the ticks and, consequently, the risk areas for tickborne diseases. This is particularly the case when ticks are vectors and reservoirs of the pathogens. Since the identification of Borrelia burgdorferi as the agent of Lyme disease in 1982, 15 ixodid-borne bacterial pathogens have been described throughout the world, including 8 rickettsiae, 3 ehrlichiae, and 4 species of the Borrelia burgdorferi complex. This article reviews and illustrate various aspects of the biology of ticks and the tickborne bacterial diseases (rickettsioses, ehrlichioses, Lyme disease, relapsing fever borrelioses, tularemia, Q fever), particularly those regarded as emerging diseases. Methods are described for the detection and isolation of bacteria from ticks and advice is given on how tick bites may be prevented and how clinicians should deal with patients who have been bitten by ticks.
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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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              Is Open Access

              Ixodes ricinus and Its Transmitted Pathogens in Urban and Peri-Urban Areas in Europe: New Hazards and Relevance for Public Health

              Tick-borne diseases represent major public and animal health issues worldwide. Ixodes ricinus, primarily associated with deciduous and mixed forests, is the principal vector of causative agents of viral, bacterial, and protozoan zoonotic diseases in Europe. Recently, abundant tick populations have been observed in European urban green areas, which are of public health relevance due to the exposure of humans and domesticated animals to potentially infected ticks. In urban habitats, small and medium-sized mammals, birds, companion animals (dogs and cats), and larger mammals (roe deer and wild boar) play a role in maintenance of tick populations and as reservoirs of tick-borne pathogens. Presence of ticks infected with tick-borne encephalitis virus and high prevalence of ticks infected with Borrelia burgdorferi s.l., causing Lyme borreliosis, have been reported from urbanized areas in Europe. Emerging pathogens, including bacteria of the order Rickettsiales (Anaplasma phagocytophilum, “Candidatus Neoehrlichia mikurensis,” Rickettsia helvetica, and R. monacensis), Borrelia miyamotoi, and protozoans (Babesia divergens, B. venatorum, and B. microti) have also been detected in urban tick populations. Understanding the ecology of ticks and their associations with hosts in a European urbanized environment is crucial to quantify parameters necessary for risk pre-assessment and identification of public health strategies for control and prevention of tick-borne diseases.
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                Author and article information

                Contributors
                Role: MethodologyRole: SoftwareRole: ValidationRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: Investigation
                Role: InvestigationRole: MethodologyRole: Validation
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Validation
                Role: Data curationRole: Formal analysisRole: Investigation
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Investigation
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Visualization
                Role: Data curationRole: InvestigationRole: Methodology
                Role: InvestigationRole: MethodologyRole: Validation
                Role: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: 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
                12 April 2018
                April 2018
                : 12
                : 4
                : e0006395
                Affiliations
                [1 ] Department of Medical Microbiology, Hitit University, Corum, Turkey
                [2 ] Department of Biology, Faculty of Arts and Science, Hitit University, Corum, Turkey
                [3 ] National High Risk Pathogens Reference Laboratory, Public Health Institution of Turkey, Ankara, Turkey
                [4 ] Department of Infectious Diseases and Clinical Microbiology, Hitit University, Corum, Turkey
                [5 ] Department of Biology, Faculty of Science and Arts, Gaziosmanpasa University, Tokat, Turkey
                [6 ] Emergency Medicine, Hitit University Corum Training and Research Hospital, Corum, Turkey
                [7 ] Department of Emergency Medicine, Faculty of Medicine; Hitit University, Corum, Turkey
                [8 ] National Parasitology Reference Laboratory, Public Health Institution of Turkey, Ankara, Turkey
                [9 ] Parasitology Unit, Department of Microbiology and Molecular Genetics, The Kuvin Center for the Study of Infectious and Tropical Diseases, The Hebrew University-Hadassah Medical School, Jerusalem, Israel
                [10 ] Department of Medical and Clinical Microbiology, Faculty of Medicine, Near East University, Nicosia, Northern Cyprus
                Mahidol University, THAILAND
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-8421-3625
                Article
                PNTD-D-17-01821
                10.1371/journal.pntd.0006395
                5916866
                29649265
                c6f466d3-8603-42ef-afca-2a66524ac23c
                © 2018 Karasartova 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
                : 13 November 2017
                : 21 March 2018
                Page count
                Figures: 2, Tables: 5, Pages: 19
                Funding
                Funded by: Hitit University, Scientific Research Support
                Award ID: TIP19001.15.006
                Award Recipient :
                This study was funded by the Hitit University Scientific Research Projects (Grant no: TIP TIP19001.15.006). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Disease Vectors
                Ticks
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Ticks
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Arachnida
                Ixodes
                Ticks
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Biology and Life Sciences
                Organisms
                Bacteria
                Rickettsia
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Rickettsia
                Biology and Life Sciences
                Parasitology
                Parasite Groups
                Apicomplexa
                Babesia
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Babesia
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Ehrlichia
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Ehrlichia
                Biology and Life Sciences
                Organisms
                Bacteria
                Rickettsiales
                Ehrlichia
                Custom metadata
                vor-update-to-uncorrected-proof
                2018-04-24
                Representative nucleotide sequences from this study were submitted to GenBank under accession numbers MF383491-MF383615 and MF494656-MF494660.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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