Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-11T00:43:25.234Z Has data issue: false hasContentIssue false
  • English
  • Français

Haemoparasites of common shrews (Sorex araneus) in Northwest England

Published online by Cambridge University Press:  09 February 2007

D. P. BRAY ,
K. J. BOWN ,
P. STOCKLEY ,
J. L. HURST ,
M. BENNETT  and
R. J. BIRTLES
D. P. BRAY*
Affiliation:
Mammalian Behaviour and Evolution Group, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
K. J. BOWN
Affiliation:
Department of Veterinary Pathology, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
P. STOCKLEY
Affiliation:
Mammalian Behaviour and Evolution Group, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
J. L. HURST
Affiliation:
Mammalian Behaviour and Evolution Group, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
M. BENNETT
Affiliation:
Department of Veterinary Pathology, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
R. J. BIRTLES
Affiliation:
Department of Veterinary Pathology, Faculty of Veterinary Science, University of Liverpool, Leahurst, Chester Road, Neston, Cheshire CH64 7TE, UK
*
*Corresponding author: Chemical Ecology Group, Centre for Applied Entomology and Parasitology, Institute of Science and Technology in Medicine, Huxley Building, Keele University, Staffordshire ST5 5BG, UK. Tel:+44 (0)1782 583682. Fax:+44 (0) 1782 583516. E-mail: d.p.bray@biol.keele.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

The presence of haemoparasites belonging to the taxa Anaplasma, Bartonella and Trypanosoma was determined among 76 common shrews (Sorex araneus) from Northwest England. Anaplasma phagocytophilum DNA was recovered from the blood of 1 shrew (1·3%), with the amplified 16S rRNA sequence identical to one previously reported from a bank vole (Clethrionomys glareolus). Trypanosoma spp. DNA was detected in 9 shrews (11·8%), the amplified 18S rDNA fragments being indistinguishable from one another, and distinct from previously published data. This represents the first report of trypanosome infection in S. araneus and suggests they are susceptible to an uncharacterized Trypanosoma species. Blood from 11 shrews (14·5%) yielded Bartonella spp., with characterization of isolates using comparative sequence analysis of partial gltA and 16S-23S rRNA intergenic spacer regions revealing 2 different genotypes. Phylogenetic inference from alignment of partial gltA sequences found that both UK S. araneus types formed a well-supported cluster with Bartonella sp. isolated from S. araneus in Sweden. No significant effect of host age, sex, or year of collection was found on prevalence of Bartonella or trypanosome infections. The results of this survey demonstrate that common shrews in the UK are susceptible to haemoparasitic infections, at prevalences similar to those reported from sympatric rodents.

Keywords

Anaplasma phagocytophilumBartonellacommon shrewSorex araneustrypanosomes
Type
Research Article
Information
Parasitology , Volume 134 , Issue 6 , June 2007 , pp. 819 - 826
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Albright, J. W. and Albright, J. F. (1991). Rodent trypanosomes: their conflict with the immune system of the host. Parasitology Today 7, 137–140.CrossRefGoogle ScholarPubMed
Anderson, B. E., Dawson, J. E., Jones, D. C. and Wilson, K. H. (1991). Ehrlichia chaffensis, a new species associated with human ehrlichiosis. Journal of Clinical Microbiology 29, 2838–2842.CrossRefGoogle Scholar
Barlough, J. E., Madigan, J. E., Turoff, D. R., Clover, J. R., Shelly, S. M. and Dumler, S. (1997). An Ehrlichia strain from a llama (Lama glama) and llama-associated ticks (Ixodes pacificus). Journal of Clinical Microbiology 35, 1005–1007.CrossRefGoogle ScholarPubMed
Bermond, D., Boulouis, H. J., Heller, R., Van Laere, G., Monteil, H., Chomel, B. B., Sander, A., Dehio, C. and Piemont, Y. (2002). Bartonella bovis Bermond et al. sp. nov. and Bartonella capreoli sp. nov., isolated from European ruminants. International Journal of Systematic and Evolutionary Microbiology 52, 383–390.CrossRefGoogle ScholarPubMed
Bermond, D., Heller, R., Barrat, F., Delacour, G., Dehio, C., Alliot, A., Monteil, H., Chomel, B., Boulouis, H. J. and Piemont, Y. (2000). Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). International Journal of Systematic and Evolutionary Microbiology 50, 1973–1979.CrossRefGoogle ScholarPubMed
Birtles, R. J., Harrison, T. G. and Molyneux, D. H. (1994). Grahamella in small woodland mammals in the UK – isolation, prevalence and host-specificity. Annals of Tropical Medicine and Parasitology 88, 317–327.CrossRefGoogle ScholarPubMed
Birtles, R. J., Harrison, T. G., Saunders, N. A. and Molyneux, D. H. (1995). Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. International Journal of Systematic Bacteriology 45, 1–8.CrossRefGoogle ScholarPubMed
Birtles, R. J., Hazel, S. M., Bennett, M., Bown, K., Raoult, D. and Begon, M. (2001). Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126, 323–329.CrossRefGoogle ScholarPubMed
Birtles, R. J. and Raoult, D. (1996). Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. International Journal of Systematic Bacteriology 46, 891–897.CrossRefGoogle ScholarPubMed
Bown, K. J., Begon, M., Bennett, M., Woldehiwet, Z. and Ogden, N. H. (2003). Seasonal dynamics of Anaplasma phagocytophila in a rodent-tick (Ixodes trianguliceps) system, United Kingdom. Emerging Infectious Diseases 9, 63–70.CrossRefGoogle Scholar
Bown, K. J., Bennett, M. and Begon, M. (2004). Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerging Infectious Diseases 10, 684–687.CrossRefGoogle ScholarPubMed
Breitschwerdt, E. B. and Kordick, D. L. (2000). Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clinical Microbiology Reviews 13, 428–438.CrossRefGoogle ScholarPubMed
Churchfield, S. (1984). An investigation of the population dynamics of synyopic shrews inhabiting water-cress beds. Journal of Zoology 204, 229–240.CrossRefGoogle Scholar
Churchfield, S. (1990). The Natural History of Shrews. A & C Black, London.Google Scholar
Clarridge, J. E. 3rd, Raich, T. J., Pirwani, D., Simon, B., Tsai, L., Rodriguez-Barradas, M. C., Regnery, R., Zollo, A., Jones, D. C. and Rambo, C. (1995). Strategy to detect and identify Bartonella species in routine clinical laboratory yields Bartonella henselae from human immunodeficiency virus-positive patient and unique Bartonella strain from his cat. Journal of Clinical Microbiology 33, 2107–2113.CrossRefGoogle ScholarPubMed
Crawley, M. J. (1993). GLIM for Ecologists. Blackwell Scientific, Oxford.Google Scholar
Crowcroft, W. (1957). The Life of the Shrew. Max Reinhardt, London.Google Scholar
Dehio, C., Lanz, C., Pohl, R., Behrens, P., Bermond, D., Piemont, Y., Pelz, K. and Sander, A. (2001). Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. International Journal of Systematic and Evolutionary Microbiology 51, 1557–1565.CrossRefGoogle ScholarPubMed
Droz, S., Chi, B., Horn, E., Steigerwalt, A. G., Whitney, A. M. and Brenner, D. J. (1999). Bartonella koehlerae sp. nov., isolated from cats. Journal of Clinical Microbiology 37, 1117–1122.CrossRefGoogle ScholarPubMed
Dumler, J. S., Barbet, A. F., Bekker, C. P., Dasch, G. A., Palmer, G. H., Ray, S. C., Rikihisa, Y. and Rurangirwa, F. R. (2001). Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. International Journal of Systematic and Evolutionary Microbiology 51, 2145–2165.CrossRefGoogle ScholarPubMed
Engvall, E. O., Pettersson, B., Persson, M., Artursson, K. and Johansson, K. E. (1996). A 16S rRNA-based assay for detection and identification of granulocytic Ehrlichia species in dogs, horses and cattle. Journal of Clinical Microbiology 34, 2170–2174.CrossRefGoogle ScholarPubMed
Fernandes, A. P., Nelson, K. and Beverley, S. M. (1993). Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: perspectives on the age and origins of parasitism. Proceedings of the National Academy of Sciences, USA 90, 11608–11612.CrossRefGoogle ScholarPubMed
Genstat 5 Committee. (1987). Genstat 5 Reference Manual. Oxford Science, Oxford.Google Scholar
Haag, J., O'Huigin, C. and Overath, P. (1998). The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Molecular and Biochemical Parasitology 91, 37–49.CrossRefGoogle ScholarPubMed
Healing, T. D. and Nowell, F. (1985). Diseases and parasites of woodland rodent populations. Symposium of the Zoological Society of London 55, 193–218.Google Scholar
Heller, R., Kubina, M., Mariet, P., Riegel, P., Delacour, G., Dehio, C., Lamarque, F., Kasten, R., Boulouis, H. J., Monteil, H., Chomel, B. and Piemont, Y. (1999). Bartonella alsatica sp. nov., a new Bartonella species isolated from the blood of wild rabbits. International Journal of Systematic Bacteriology 49, 283–288.Google Scholar
Heller, R., Riegel, P., Hansmann, Y., Delacour, G., Bermond, D., Dehio, C., Lamarque, F., Monteil, H., Chomel, B. and Piemont, Y. (1998). Bartonella tribocorum sp. nov., a new Bartonella species isolated from the blood of wild rats. International Journal of Systematic Bacteriology 48, 1333–1339.CrossRefGoogle Scholar
Holmberg, M., Mills, J. N., McGill, S., Benjamin, G. and Ellis, B. A. (2003). Bartonella infection in sylvatic small mammals of central Sweden. Epidemiology and Infection 130, 149–157.CrossRefGoogle ScholarPubMed
Houpikian, P., Fournier, P. E. and Raoult, D. (2001). Phylogenetic position of Bartonella vinsonii subsp. arupensis based on 16S rDNA and gltA gene sequences. International Journal of Systematic and Evolutionary Microbiology 51, 179–182.CrossRefGoogle ScholarPubMed
Hoyte, H. M. (1956). Grahamella (Rickettsiales) in the common shrew Sorex araneus. Parasitology 46, 224–234.CrossRefGoogle ScholarPubMed
Laakkonen, J. (2000). Microparasites of three species of shrew from Finnish Lapland. Annales Zoologici Fennici 37, 37–41.Google Scholar
Laakkonen, J., Haukisalmi, V. and Merritt, J. F. (1998). Blood parasites of shrews from Pennsylvania. Journal of Parasitology 84, 1300–1303.CrossRefGoogle ScholarPubMed
LaScola, B. and Raoult, D. (1997). Laboratory diagnosis of rickettsioses: current approaches to diagnosis of old and new rickettsial diseases. Journal of Clinical Microbiology 35, 2715–2727.CrossRefGoogle Scholar
Liz, J. S., Anderes, L., Sumner, J. W., Massung, R. F., Gern, L., Rutti, B. and Brossard, M. (2000). PCR detection of granulocytic Ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. Journal of Clinical Microbiology 38, 1002–1007.CrossRefGoogle ScholarPubMed
Maillard, R., Riegel, P., Barrat, F., Bouillin, C., Thibault, D., Gandoin, C., Halos, L., Demanche, C., Alliot, A., Guillot, J., Piemont, Y., Boulouis, H. J. and Vayssier-Taussat, M. (2004). Bartonella chomelii sp. nov., isolated from French domestic cattle (Bos taurus). International Journal of Systematic and Evolutionary Microbiology 54, 215–220.CrossRefGoogle ScholarPubMed
Maraghi, S. and Molyneux, D. H. (1989). Studies on cross-immunity in Herpetosoma trypanosomes of Microtus, Clethrionomys and Apodemus. Parasitology Research 75, 175–177.CrossRefGoogle ScholarPubMed
Maslov, D. A., Avila, H. A., Lake, J. A. and Simpson, L. (1994). Evolution of RNA editing in kinetoplastid protozoa. Nature 368, 345–348.CrossRefGoogle ScholarPubMed
Massung, R. F., Slater, K., Owens, J. H., Nicholson, W. L., Mather, T. N., Solberg, V. B. and Olson, J. G. (1998). Nested PCR assay for detection of granulocytic ehrlichiae. Journal of Clinical Microbiology 36, 1090–1095.CrossRefGoogle ScholarPubMed
Middleton, A. D. (1931). A contribution to the biology of the common shrew, Sorex araneus Linnaeus. Proceedings of the Zoological Society of London 1931, 133–143.CrossRefGoogle Scholar
Norman, A. F., Regnery, R., Jameson, P., Greene, C. and Krause, D. C. (1995). Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. Journal of Clinical Microbiology 33, 1797–1803.CrossRefGoogle ScholarPubMed
Noyes, H. A., Ambrose, P., Barker, F., Begon, M., Bennett, M., Bown, K. J. and Kemp, S. J. (2002). Host specificity of Trypanosoma (Herpetosoma) species: evidence that bank voles (Clethrionomys glareolus) carry only one T. (H.) evotomys 18S rRNA genotype but wood mice (Apodemus sylvaticus) carry at least two polyphyletic parasites. Parasitology 124, 185–190.CrossRefGoogle Scholar
Ogden, N. H., Bown, K., Horrocks, B. K., Woldehiwet, Z. and Bennett, M. (1998). Granulocytic Ehrlichia infection in Ixodid ticks and mammals in woodlands and uplands of the UK. Medical and Veterinary Entomology 12, 423–429.CrossRefGoogle Scholar
Page, R. D. M. (1996). TreeView: An application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357–358.Google ScholarPubMed
Pernetta, J. C. (1976). Diets of the shrews Sorex araneus L. and Sorex minutus L. in Wytham grassland. Journal of Animal Ecology 45, 899–912.CrossRefGoogle Scholar
Randolph, S. E. (1975). Seasonal dynamics of a host-parasite system – Ixodes trianguliceps (Acarina Ixodidae) and its small mammal hosts. Journal of Animal Ecology 44, 425–449.CrossRefGoogle Scholar
Roux, V., Eykyn, S. J., Wyllie, S. and Raoult, D. (2000). Bartonella vinsonii subsp. berkhoffii as an agent of afebrile blood culture-negative endocarditis in a human. Journal of Clinical Microbiology 38, 1698–1700.CrossRefGoogle ScholarPubMed
Searle, J. B. (1985). Methods for determining the sex of common shrews (Sorex araneus). Journal of Zoology 206, 279–282.CrossRefGoogle Scholar
Sebek, Z. (1975). Blutparasiten der wildlebenden Kleinsauger in der Tschechoslowakei. Folia Parasitologica 22, 11–20.Google Scholar
Shillito, J. F. (1963). Field observations on growth, reproduction and activity of a woodland population of the common shrew Sorex araneus L. Proceedings of the Zoological Society of London 140, 99–114.Google Scholar
Smit, F. G. A. M. (1957). Handbooks for the Identification of British Insects. Royal Entomological Society of London, London.Google Scholar
Stevens, J. R. and Gibson, W. (1999). The molecular evolution of trypanosomes. Parasitology Today 15, 432–437.CrossRefGoogle ScholarPubMed
Stevens, J. R., Noyes, H., Dover, G. A. and Gibson, W. C. (1999 a). The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118, 107–116.CrossRefGoogle ScholarPubMed
Stevens, J. R., Teixeira, M. M., Bingle, L. E. and Gibson, W. C. (1999 b). The taxonomic position and evolutionary relationships of Trypanosoma rangeli. International Journal for Parasitology 29, 749–757.CrossRefGoogle ScholarPubMed
Taylor, L. H., Latham, S. M. and Woolhouse, M. E. (2001). Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 356, 983–989.CrossRefGoogle ScholarPubMed
Telfer, S., Bown, K. J., Sekules, R., Begon, M., Hayden, T. and Birtles, R. (2005). Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130, 661–668.CrossRefGoogle ScholarPubMed
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Votypka, J., Obornik, M., Volf, P., Svobodova, M. and Lukes, J. (2002). Trypanosoma avium of raptors (Falconiformes): phylogeny and identification of vectors. Parasitology 125, 253–263.CrossRefGoogle ScholarPubMed
Wilson, K. and Grenfell, B. T. (1997 a). Generalized linear modelling for parasitologists. Parasitology Today 13, 33–38.CrossRefGoogle ScholarPubMed
Wilson, K. and Grenfell, B. T. (1997 b). Generalized linear modelling for parasitologists (vol 13, pg 33, pg 1997). Parasitology Today 13, 162.CrossRefGoogle Scholar