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      Hopping species and borders: detection of Bartonella spp. in avian nest fleas and arctic foxes from Nunavut, Canada

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          Abstract

          Background

          In a warmer and more globally connected Arctic, vector-borne pathogens of zoonotic importance may be increasing in prevalence in native wildlife. Recently, Bartonella henselae, the causative agent of cat scratch fever, was detected in blood collected from arctic foxes ( Vulpes lagopus) that were captured and released in the large goose colony at Karrak Lake, Nunavut, Canada. This bacterium is generally associated with cats and cat fleas, which are absent from Arctic ecosystems. Arctic foxes in this region feed extensively on migratory geese, their eggs, and their goslings. Thus, we hypothesized that a nest flea, Ceratophyllus vagabundus vagabundus (Boheman, 1865), may serve as a vector for transmission of Bartonella spp.

          Methods

          We determined the prevalence of Bartonella spp. in (i) nest fleas collected from 5 arctic fox dens and (ii) 37 surrounding goose nests, (iii) fleas collected from 20 geese harvested during arrival at the nesting grounds and (iv) blood clots from 57 adult live-captured arctic foxes. A subsample of fleas were identified morphologically as C. v. vagabundus. Remaining fleas were pooled for each nest, den, or host. DNA was extracted from flea pools and blood clots and analyzed with conventional and real-time polymerase chain reactions targeting the 16S-23S rRNA intergenic transcribed spacer region.

          Results

          Bartonella henselae was identified in 43% of pooled flea samples from nests and 40% of pooled flea samples from fox dens. Bartonella vinsonii berkhoffii was identified in 30% of pooled flea samples collected from 20 geese. Both B. vinsonii berkhoffii ( n = 2) and B. rochalimae ( n = 1) were identified in the blood of foxes.

          Conclusions

          We confirm that B. henselae, B. vinsonii berkhoffii and B. rochalimae circulate in the Karrak Lake ecosystem and that nest fleas contain B. vinsonii and B. henselae DNA, suggesting that this flea may serve as a potential vector for transmission among Arctic wildlife.

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          Most cited references38

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          Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera

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            Experimental transmission of Bartonella henselae by the cat flea.

            Bartonella henselae is an emerging bacterial pathogen, causing cat scratch disease and bacillary angiomatosis. Cats bacteremic with B. henselae constitute a large reservoir from which humans become infected. Prevention of human infection depends on elucidation of the natural history and means of feline infection. We studied 47 cattery cats in a private home for 12 months to determine the longitudinal prevalence of B. henselae bacteremia, the prevalence of B. henselae in the fleas infesting these cats, and whether B. henselae is transmitted experimentally to cats via fleas. Vector-mediated transmission of B.henselae isolates was evaluated by removing fleas from the naturally bacteremic, flea-infested cattery cats and transferring these fleas to specific-pathogen-free (SPF) kittens housed in a controlled, arthropod-free University Animal Facility. B. henselae bacteremia was detected in 89% of the 47 naturally infected cattery cats. A total of 132 fleas were removed from cats whose blood was simultaneously cultured during different seasons and were tested individually for the presence of B. henselae DNA by PCR. B. henselae DNA was detected in 34% of 132 fleas, with seasonal variation, but without an association between the presence or the level of bacteremia in the corresponding cat. Cat fleas removed from bacteremic cattery cats transmitted B. henselae to five SPF kittens in two separate experiments; however, control SPF kittens housed with highly bacteremic kittens in the absence of fleas did not become infected. These data demonstrate that the cat flea readily transmits B. henselae to cats. Control of feline infestation with this arthropod vector may provide an important strategy for the prevention of infection of both humans and cats.
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              Vector transmission of Bartonella species with emphasis on the potential for tick transmission.

              Bartonella species are gram-negative bacteria that infect erythrocytes, endothelial cells and macrophages, often leading to persistent blood-borne infections. Because of the ability of various Bartonella species to reside within erythrocytes of a diverse number of animal hosts, there is substantial opportunity for the potential uptake of these blood-borne bacteria by a variety of arthropod vectors that feed on animals and people. Five Bartonella species are transmitted by lice, fleas or sandflies. However, Bartonella DNA has been detected or Bartonella spp. have been cultured from numerous other arthropods. This review discusses Bartonella transmission by sandflies, lice and fleas, the potential for transmission by other vectors, and data supporting transmission by ticks. Polymerase chain reaction (PCR) or culture methods have been used to detect Bartonella in ticks, either questing or host-attached, throughout the world. Case studies and serological or molecular surveys involving humans, cats and canines provide indirect evidence supporting transmission of Bartonella species by ticks. Of potential clinical relevance, many studies have proposed co-transmission of Bartonella with other known tick-borne pathogens. Currently, critically important experimental transmission studies have not been performed for Bartonella transmission by many potential arthropod vectors, including ticks.
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                Author and article information

                Contributors
                kab048@usask.ca
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                14 September 2020
                14 September 2020
                2020
                : 13
                : 469
                Affiliations
                [1 ]GRID grid.25152.31, ISNI 0000 0001 2154 235X, Department of Veterinary Microbiology, Western College of Veterinary Medicine, , University of Saskatchewan, ; 52 Campus Drive, Saskatoon, SK S7N 5B4 Canada
                [2 ]GRID grid.40803.3f, ISNI 0000 0001 2173 6074, Intracellular Pathogens Research Laboratory, College of Veterinary Medicine, , North Carolina State University, ; 1060 William Moore Drive, Raleigh, NC 27606 USA
                [3 ]GRID grid.21613.37, ISNI 0000 0004 1936 9609, Department of Entomology, Faculty of Agricultural and Food Sciences, , University of Manitoba, ; 12 Dafoe Road, Winnipeg, MB R3T 2N2 Canada
                [4 ]GRID grid.25152.31, ISNI 0000 0001 2154 235X, Department of Biology, , University of Saskatchewan, ; Science Place, Saskatoon, SK S7N 5E2 Canada
                [5 ]GRID grid.410334.1, ISNI 0000 0001 2184 7612, Prairie and Northern Wildlife Research Centre, Wildlife Research Division, , Environment and Climate Change Canada, ; 115 Perimeter Road, Saskatoon, SK S7N 0X4 Canada
                [6 ]Snow Leopard Trust, 4649 Sunnyside Ave North, Suite 325, Seattle, WA 98103 USA
                Author information
                http://orcid.org/0000-0001-9520-8784
                Article
                4344
                10.1186/s13071-020-04344-3
                7490881
                bd6138e6-dceb-4ecc-b7f4-30f950bd4b3f
                © 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.

                History
                : 28 May 2020
                : 5 September 2020
                Funding
                Funded by: NSERC Discovery Grant
                Funded by: FundRef http://dx.doi.org/10.13039/501100000003, ArcticNet;
                Funded by: Northern Scientific Training Program
                Funded by: FundRef http://dx.doi.org/10.13039/100012258, Polar Knowledge Canada;
                Award ID: NST-1718-0012
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology
                arctic fox,bartonella,disease ecology,flea,geese,nunavut,vector-borne disease,wildlife,zoonotic
                Parasitology
                arctic fox, bartonella, disease ecology, flea, geese, nunavut, vector-borne disease, wildlife, zoonotic

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