Vet Med - Czech, 2009, 54(2):64-74 | DOI: 10.17221/1913-VETMED

Susceptibility of selected murine and microtine species to infection by a wild strain of Francisella tularensis subsp. holoarctica

H. Bandouchova1, J. Sedlackova1, M. Hubalek2, M. Pohanka2, L. Peckova1, F. Treml1, F. Vitula1, J. Pikula1
1 University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
2 University of Defence, Hradec Kralove, Czech Republic

The purpose of this study was to compare susceptibility of BALB/c mice, common voles (Microtus arvalis) and yellow-necked mice (Apodemus flavicollis) to infection by a virulent Francisella tularensis subsp. holarctica strain. Median survival in these three species following experimental infection with 320 colony forming units of F. tularensis (both intraperitoneally and subcutaneously) amounted to 4.5, 7 and 4 days, respectively. Survival curves of BALB/c and yellow-necked mice were very similar and were significantly different from that of common voles. LD50 was 0.5 and 37.9 colony forming units in BALB/c mice and common voles, respectively. The bacterial burden in the spleen, liver, lung, kidney and blood of common voles started to develop later post exposure and amounted to lower levels (except in kidneys) than in BALB/c mice. The results demonstrate that yellow-necked mice are even more susceptible to infection by F. tularensis than BALB/c mice and that the common vole is a small mammalian host with a susceptibility which is two-orders-of-magnitude lower.

Keywords: tularaemia; survival time; minimum infectious dose; LD50; bacterial burden

Published: February 28, 2009  Show citation

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Bandouchova H, Sedlackova J, Hubalek M, Pohanka M, Peckova L, Treml F, et al.. Susceptibility of selected murine and microtine species to infection by a wild strain of Francisella tularensis subsp. holoarctica. Vet Med - Czech. 2009;54(2):64-74. doi: 10.17221/1913-VETMED.
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    References

    1. Abd H., Johansson T., Golovliov I., Sandstrom G., Forsman M. (2003): Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Applied and Environmental Microbology, 69, 600-606. Go to original source... Go to PubMed...
    2. Anthony L.S.D., Kongshavn P.A.L. (1987): Experimental murine tularemia caused by Francisella tularensis, live vaccine strain - a model of acquired cellular-resistance. Microbial Pathogenesis, 2, 3-14. Go to original source... Go to PubMed...
    3. Bell J.F., Stewart S.J. (1975): Chronic shedding tularemia nephritis in rodents: possible relation to occurrence of Francisella tularensis in lotic waters. Journal of Wildlife Diseases, 11, 421-430. Go to original source... Go to PubMed...
    4. Boyard C., Vourc'h G., Barnouin J. (2008): The relationships between Ixodes ricinus and small mammal species at the woodland-pasture interface. Experimental and Applied Acarology, 44, 61-76. Go to original source... Go to PubMed...
    5. Cerny Z. (2001): Changes of the epidemiology and the clinical picture of tularemia in Southern Moravia (the Czech Republic) during the period 1936-1999. European Journal of Epidemiology, 17, 637-642. Go to original source... Go to PubMed...
    6. Chen W.X., Shen H., Webb A., KuoLee R., Conlan J.W. (2003): Tularemia in BALB/c and C57BL/6 mice vaccinated with Francisella tularensis LVS and challenged intradermally, or by aerosol with virulent isolates of the pathogen: protection varies depending on pathogen virulence, route of exposure, and host genetic background. Vaccine, 21, 3690-3700. Go to original source... Go to PubMed...
    7. Chen W.X., KuoLee R., Shen H., Conlan J.W. (2004): Susceptibility of immunodeficient mice to aerosol and systemic infection with virulent strains of Francisella tularensis. Microbial Pathogenesis, 36, 311-318. Go to original source... Go to PubMed...
    8. Conlan J.W., Sjostedt A., North R.J. (1994): Cd4(+) and Cd8(+) T-cell-dependent and T-cell-independent host-defense mechanisms can operate to control and resolve primary and secondary Francisella tularensis Lvs infection in mice. Infection and Immunity, 62, 5603-5607. Go to original source... Go to PubMed...
    9. Conlan J.W., Chen W.X., Shen H., Webb A., KuoLee R. (2003): Experimental tularemia in mice challenged by aerosol or intradermally with virulent strains of Francisella tularensis: bacteriologic and histopathologic studies. Microbial Pathogenesis, 34, 239-248. Go to original source... Go to PubMed...
    10. Delattre P., Giraudoux P., Baudry J., Quere J.P., Fichet E. (1996): Effect of landscape structure on common vole (Microtus arvalis) distribution and abundance at several space scales. Landscape Ecology, 11, 279-288. Go to original source...
    11. Dowell S.F. (2001): Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerging Infectious Diseases, 7, 369-374. Go to original source...
    12. Dunaeva T.N., Olsufyev N.G. (1958): The possibility of a latent or chronic course of tularemia in water voles and other animal species highly susceptible to that infection. Zoologichesky Zhurnal, 37, 430-440.
    13. Eliasson H., Lindback J., Nuorti J.P., Arneborn M., Giesecke J., Tegnell A. (2002): The 2000 tularemia outbreak: A case-control study of risk factors in disease-endemic and emergent areas, Sweden. Emerging Infectious Diseases, 8, 956-960. Go to original source... Go to PubMed...
    14. Ellis J., Oyston P.C.F., Green M., Titball R.W. (2002): Tularemia. Clinical Microbiology Reviews, 15, 631-646. Go to original source... Go to PubMed...
    15. Farlow J., Wagner D.M., Dukerich M., Stanley M., Chu M., Kubota K., Petersen J., Keim P. (2005): Francisella tularensis in the United States. Emerging Infectious Diseases, 11, 1835-1841. Go to original source... Go to PubMed...
    16. Green M., Choules G., Rogers D., Titball R.W. (2005): Efficacy of the live attenuated Francisella tularensis vaccine (LVS) in a murine model of disease. Vaccine, 23, 2680-2686. Go to original source... Go to PubMed...
    17. Gurycova D. (1998): First isolation of Francisella tularensis subsp. tularensis in Europe. European Journal of Epidemiology, 14, 797-802. Go to original source... Go to PubMed...
    18. Gurycova D., Vyrostekova V., Khanakah G., Kocianova E., Stanek G. (2001): Importance of surveillance of tularemia natural foci in the known endemic area of Central Europe, 1991-1997. Wiener Klinische Wochenschrift, 113, 433-438.
    19. Hartl G.B., Suchentrunk F., Willing R., Markowski J., Ansorge H. (1992): Inconsistency of Biochemical Evolutionary Rates Affecting Allozyme Divergence within the Genus Apodemus (Muridae, Mammalia). Biochemical Systematics and Ecology, 20, 363-372. Go to original source...
    20. Hernychova L., Stulik J., Halada P., Macela A., Kroca M., Johansson T., Malina M. (2001): Construction of a Francisella tularensis two-dimensional electrophoresis protein database. Proteomics, 1, 508-515. Go to original source... Go to PubMed...
    21. Hubalek Z., Juricova Z., Svobodova S., Halouzka J. (1993): A serologic survey for some bacterial and viral zoonoses in game animals in the Czech Republic. Journal of Wildlife Diseases, 29, 604-607. Go to original source... Go to PubMed...
    22. Hubalek Z., Treml F., Halouzka J., Juricova Z., Hunady M., Janik V. (1996): Frequent isolation of Francisella tularensis from Dermacentor reticulatus ticks in an enzootic focus of tularaemia. Medical and Veterinary Entomology, 10, 241-246. Go to original source... Go to PubMed...
    23. Hubalek M., Hernychova L., Brychta M., Lenco J., Zechovska J., Stulik J. (2004): Comparative proteome analysis of cellular proteins extracted from highly virulent Francisella tularensis ssp. tularensis and less virulent F. tularensis ssp. holarctica and F. tularensis ssp. mediaasiatica. Proteomics, 4, 3048-3060. Go to original source... Go to PubMed...
    24. Kozuch O., Gurycova D., Lysy J., Labuda M. (1995): Mixed natural focus of tick-borne encephalitis, tularemia and hemorrhagic-fever with renal syndrome in west Slovakia. Acta Virologica, 39, 95-98. Go to PubMed...
    25. Kruse H., Kirkemo A.M., Handeland K. (2004): Wildlife as source of zoonotic infections. Emerging Infectious Diseases, 10, 2067-2072. Go to original source... Go to PubMed...
    26. KuoLee R., Harris G., Conlan J.W., Chen W.X. (2007): Oral immunization of mice with the live vaccine strain (LVS) of Francisella tularensis protects mice against respiratory challenge with virulent type A F. tularensis. Vaccine, 25, 3781-3791. Go to original source... Go to PubMed...
    27. Lambin X., Bretagnolle V., Yoccoz N.G. (2006): Vole population cycles in northern and southern Europe: Is there a need for different explanations for single pattern? Journal of Animal Ecology, 75, 340-349. Go to original source... Go to PubMed...
    28. Moerner T. (1992): The ecology of tularaemia. Revue Scientifique et Technique de l Office International des Epizooties, 11, 1123-1130. Go to original source...
    29. Murray P.R., Baron E.J., Jorgensen J.H., Pfaller M.A., Yolken R.H. (2003): Manual of Clinical Microbiology. 8th ed. ASM Press, Washington.
    30. Petersen J.M., Schriefer M.E. (2005): Tularemia: emergence/re-emergence. Veterinar y Research, 36, 455-467. Go to original source... Go to PubMed...
    31. Petersen J.M., Schriefer M.E., Carter L.G., Zhou Y., Sealy T., Bawiec D., Yockey B., Urich S., Zeidner N.S., Avashia S., Kool J.L., Buck J., Lindley C., Celeda L., Monteneiri J.A., Gage K.L., Chu M.C. (2004): Laboratory analysis of tularemia in wild-trapped, commercially traded prairie dogs, Texas, 2002. Emerging Infectious Diseases, 10, 419-425.
    32. Pikula J., Treml F., Beklova M., Holesovska Z., Pikulova J. (2002): Geographic information systems in epidemiology - ecology of common vole and distribution of natural foci of tularaemia. Acta Veterinaria Brno, 71, 379-387. Go to original source...
    33. Pikula J., Treml F., Beklova M., Holesovska Z., Pikulova J. (2003): Ecological conditions of natural foci of tularaemia in the Czech Republic. European Journal of Epidemiology, 18, 1091-1095. Go to original source... Go to PubMed...
    34. Pikula J., Beklova M., Holesovska Z., Treml F. (2004a): Spatio-temporal aspects of tularemia in Southern Moravia (Czech Republic). Veterinarni Medicina, 49, 15-18. Go to original source...
    35. Pikula J., Beklova M., Holesovska Z., Treml F. (2004b): Prediction of possible distribution of tularemia in the Czech Republic. Veterinarni Medicina, 49, 61-64. Go to original source...
    36. Pikula J., Beklova M., Holesovska Z., Treml F. (2004c): Ecology of European brown hare and distribution of natural foci of tularaemia in the Czech Republic. Acta Veterinaria Brno, 73, 267-273. Go to original source...
    37. Pohanka M., Treml F., Hubalek M., Bandouchova H., Beklova M., Pikula J. (2007): Piezoelectric biosensor for a simple serological diagnosis of tularemia in infected European brown hares (Lepus europaeus). Sensors, 7, 2825-2834. Go to original source... Go to PubMed...
    38. Pohanka M., Hubalek M., Neubauerova V., Macela A., Faldyna M., Bandouchova H., Pikula J. (2008). Current and emerging assays for Francisella tularensis detection: a review. Veterinarni Medicina, 53, 585-594. Go to original source...
    39. Rosa R., Pugliese A., Ghosh M., Perkins S.E., Rizzoli A. (2007): Temporal variation of Ixodes ricinus intensity on the rodent host Apodemus flavicollis in relation to local climate and host dynamics. Vector-Borne and Zoonotic Diseases, 7, 285-295. Go to original source... Go to PubMed...
    40. Schaper M.M., Thompson R.D., Well C.S. (1994): Computer-Programs for calculation of median effective dose Ld(50) or Ed(50) using the method of moving average interpolation. Archives of Toxicology, 68, 332-337. Go to original source... Go to PubMed...
    41. Shlygina K.N., Olsufyev N.G. (1982): Latent tularemia in common voles in the experiment. Zhurnal Mikrobiologii Epidemiologii i Immunobiologii, 4, 101- 104.
    42. Shlygina K.N., Baranovsky P.M., Ananova E.V., Olsufyev N.G. (1987): On the possibility of the atypical course of tularemia (persistence) in common voles (Microtus arvalis Pall). Zhurnal Mikrobiologii Epidemiologii i Immunobiologii, 3, 26-29.
    43. Shlygina K.N., Ananova E.V., Olsufyev N.G. (1989): To the problem of some mechanisms of the formation of chronic tularemia in highly sensitive species of animals (Microtus rossiae-meridionalis). Zhurnal Mikrobiologii Epidemiologii i Immunobiologii, 4, 17-21.
    44. Stanek G. (2005): Disease pathogens transmissable through ticks in Central Europe. Wiener Klinische Wochenschrift, 117, 373-380. Go to original source... Go to PubMed...
    45. Staples J.E., Kubota K.A., Chalcraft L.G., Mead P.S., Petersen J.M. (2006): Epidemiologic and molecular analysis of human tularemia, United States, 1964-2004. Emerging Infectious Diseases, 12, 1113-1118. Go to original source... Go to PubMed...
    46. Talleklint L., Jaenson T.G.T. (1997): Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in southcentral Sweden. Experimental and Applied Acarology, 21, 755-771. Go to original source... Go to PubMed...
    47. Tarnvik A., Berglund L. (2003): Tularaemia. European Respiratory Journal, 21, 361-373. Go to original source... Go to PubMed...
    48. Tarnvik A., Sandstrom G., Sjostedt A. (1996): Epidemiological analysis of tularemia in Sweden 1931-1993. FEMS Immunology and Medical Microbiology, 13, 201-204. Go to original source... Go to PubMed...
    49. Tkadlec E., Stenseth N.C. (2001): A new geographical gradient in vole population dynamics. Proceedings of the Royal Society of London Series B - Biological Sciences, 268, 1547-1552. Go to original source... Go to PubMed...
    50. Treml F., Pikula J., Bandouchova H., Horakova J. (2007): European brown hare as a potential source of zoonotic agents. Veterinarni Medicina, 52, 451-456. Go to original source...
    51. Vyrostekova V., Khanakah G., Kocianova E., Gurycova D., Stanek G. (2002): Prevalence of coinfection with Francisella tularensis in reservoir animals of Borrelia burgdorferi sensu lato. Wiener Klinische Wochenschrift, 114, 482-488.
    52. Zgrabczynska E., Pilacinska B. (2002): Social relations in family-groups of wood mice Apodemus sylvaticus under laboratory and enclosure conditions. Acta Theriologica, 47, 151-162. Go to original source...
    53. Zhang F., Liu W., Chu M.C., He J., Duan Q., Wu X.M., Zhang P.H., Zhao Q.M., Yang H., Xin Z.T., Cao W.C. (2006): Francisella tularensis in rodents, China. Emerging Infectious Diseases, 12, 994-996. Go to original source... Go to PubMed...

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