1. bookVolume 57 (2018): Issue 1 (January 2018)
Journal Details
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Format
Journal
eISSN
2545-3149
First Published
01 Mar 1961
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4 times per year
Languages
English, Polish
access type Open Access

FRANCISELLA TULARENSIS– REVIEW

Published Online: 23 May 2019
Volume & Issue: Volume 57 (2018) - Issue 1 (January 2018)
Page range: 58 - 67
Received: 01 Oct 2017
Accepted: 01 Dec 2017
Journal Details
License
Format
Journal
eISSN
2545-3149
First Published
01 Mar 1961
Publication timeframe
4 times per year
Languages
English, Polish
Abstract

In the early twentieth century, Francisella tularensis was identified as a pathogenic agent of tularaemia, one of the most dangerous zoonoses. Based on its biochemical properties, infective dose and geographical location, four subspecies have been distinguished within the species F. tularensis: the highly infectious F. tularensis subsp. tularensis (type A) occurring mainly in the United States of America, F. tularensis subsp. holarctica (type B) mainly in Europe, F. tularensis subsp. mediasiatica isolated mostly in Asia and F. tularensis subsp. novicida, non-pathogenic to humans. Due to its ability to infect and variable forms of the disease, the etiological agent of tularaemia is classified by the CDC (Centers for Disease Control and Prevention, USA) as a biological warfare agent with a high danger potential (group A). The majority of data describing incidence of tularaemia in Poland is based on serological tests. However, real-time PCR method and MST analysis of F. tularensis highly variable intergenic regions may be also applicable to detection, differentiation and determination of genetic variation among F. tularensis strains. In addition, the above methods could be successfully used in molecular characterization of tularaemia strains from humans and animals isolated in screening research, and during epizootic and epidemic outbreaks.

1. Historical overview. 2. Characteristics and taxonomy of F. tularensis. 3. Morphology. 4. Culture media and conditions. 5. Biochemical properties. 6. Survivability and persistence of F. tularensis. 7. F. tularensis as a biological weapon agent. 8. Tularaemia vaccines. 9. Pathogenicity of F. tularensis. 10. Tularaemia treatment. 11. Laboratory diagnostics of F. tularensis. 12. Summary

Keywords

Słowa kluczowe

Abd H., Johansson T., Golovliov I., Sandström G., Forsman M. Survival and growth of Francisella tularensis in Acanthamoeba castellanii. Appl. Environ. Microb. 69, 600–606 (2003)10.1128/AEM.69.1.600-606.200315241612514047Search in Google Scholar

Alibek K.: The Soviet Union’s Anti-Agricultural Biological Weapons. Ann. N.Y. Acad. Sci. 894, 18–19 (1999)Search in Google Scholar

Barns S.M., Grow C.C., Okinaka R.T., Keim P., Kuske C.R.: Detection of diverse new Francisella-like bacteria in environmental samples. Appl. Environ. Microb. 71, 5494–5500 (2005)Search in Google Scholar

Bielawska-Drózd A., Gaweł J., Bartoszcze M., Kołodziej M., Graniak G., Joniec J., Michalski A.: Identification of Francisella tularensis by real-time PCR with TaqMan probes. Lek. Wojsk. 2, 98–102 (2011)Search in Google Scholar

Bielawska-Drózd A., Niemcewicz M., Gawel J., Bartoszcze M., Graniak G., Joniec J., Kołodziej M.: Identyfikacja Francisella tularensis techniką real-time PCR z wykorzystaniem sond hybrydyzujących zaprojektowanych dla fragmentów sekwencji genów fopA i tul4. Med. Dosw. Mikrobiol. 62, 351–360 (2010)Search in Google Scholar

Bilecki Ś.: Tularemia. Państwowe Wydawnictwo Rolnicze i Leśne. Warszawa, 1974Search in Google Scholar

Birkbeck T.H., Bordevik M., Frøystad M.K., Baklien Å.: Identification of Francisella sp. from Atlantic salmon, Salmo salar L., in Chile. J. Fish Dis. 30, 505–507 (2007)10.1111/j.1365-2761.2007.00837.x17640254Search in Google Scholar

Brevik O.J., Ottem K.F., Kamaishi T., Watanabe K., Nylund A.: Francisella halioticida sp. Vov., a pathogen of farmed giant abalone (Haliotis gigantea) in Japan. J. Appl. Microbiol. 5, 1044–1056 (2011)Search in Google Scholar

Broman T., Thelaus J., Andersson A.C., Bäckman S., Wikström P., Larsson E., Forsman M.: Molecular detection of persistent Francisella tularensis subspecies holarctica in natural waters. Int. J. Microbiol. DOI: 10.1155/2011/851946 (2010)10.1155/2011/851946294658620885922Search in Google Scholar

Byström M., Böcher S., Magnusson A., Prag J., Johansson A.: Tularemia in Denmark: identification of a Francisella tularensis subsp. holarctica strain by real-time PCR and high-resolution typing by multiple-locus variable-number tandem repeat analysis. J. Clin. Microbiol. 43, 5355–5358 (2005)10.1128/JCM.43.10.5355-5358.2005124844816208017Search in Google Scholar

Carlsson H.E., Lindberg A.A., Lindberg G., Hederstedt B., Karlsson K.A., Agell B.O.: Enzyme-linked immunosorbent assay for immunological diagnosis of human tularemia. J. Clin. Microbiol. 10, 615–621 (1979)Search in Google Scholar

Chaignat V., Djordjevic-Spasic M., Ruettger A., Otto P., Klimpel D., Müller W., Tomaso H.: Performance of seven serological assays for diagnosing tularemia. BMC Infect. Dis. 14, 234 (2014)10.1186/1471-2334-14-234402134024885274Search in Google Scholar

Chróst A., Gielarowiec K., Kałużewski S., Rastawicki W. Występowanie zakażeń wywoływanych przez Francisella tularensisu ludzi w Polsce oraz laboratoryjna diagnostyka tularemii. Med. Dośw. Mikrobiol. 69, 55–63 (2017)Search in Google Scholar

Cianciotto N.P., Fields B.S.: Legionella pneumophila mip gene potentiates intracellular infection of protozoa and human macrophages. Proc. Nat. Acad. Sci. USA, 89, 5188–5191 (1992)10.1073/pnas.89.11.5188492551594630Search in Google Scholar

Cirillo J.D., Falkow S., Tompkins L.S.: Growth of Legionella pneumophila in Acanthamoeba castellanii enhances invasion. Infect. Immun. 62, 3254–3261 (1994)Search in Google Scholar

Croddy E., Krcalova S.: Tularemia, biological warfare, and the battle for Stalingrad (1942–1943). Mil. Med. 166, 837–838 (2001)Search in Google Scholar

Del Blanco N.G., Dobson M.E., Vela A.I., De La Puente V.A., Gutierrez C.B., Hadfield T.L., Ferri E.R.: Genotyping of Francisella tularensis strains by pulsed-field gel electrophoresis, amplified fragment length polymorphism fingerprinting, and 16S rRNA gene sequencing. J. Clin. Microbiol. 40, 2964–2972 (2002)10.1128/JCM.40.8.2964-2972.200212068212149360Search in Google Scholar

Dennis D.T., Inglesby T.V., Henderson D.A., Bartlett J.G., Ascher M.S., Eitzen E., Tonat K.: Tularemia as a biological weapon: medical and public health management. JAMA. 285, 2763–2773 (2001)10.1001/jama.285.21.276311386933Search in Google Scholar

Dentan C., Pavese P., Pelloux I., Boisset S., Brion J.P., Stahl J.P., Maurin M.: Treatment of tularemia in pregnant woman, France. Emerg. Infect. Dis. 19, 996–998 (2013)Search in Google Scholar

Ellis J., Oyston P.C.F., Green M., Titball R.W.: Tularemia. Clin. Microbiol. Rev. 15, 631–646 (2002)10.1128/CMR.15.4.631-646.200212685912364373Search in Google Scholar

Emanuel P.A., Bell R., Dang J.L., McClanahan R., David J.C., Burgess R.J., Hadfield T.: Detection of Francisella tularensis within infected mouse tissues by using a hand-held PCR thermocycler. J. Clin. Microbiol. 41, 689–693 (2003)Search in Google Scholar

Escudero R., Toledo A., Gil H., Kovácsová K., Rodríguez-Vargas M., Jado I., Anda P. Molecular method for discrimination between Francisella tularensis and Francisella-like endosymbionts. J. Clin. Microbiol. 46, 3139–3143 (2008)Search in Google Scholar

Fedorowa V.A., Sayapina l.V., Corbel M.J., Motin V.L.: Russian vaccines against especially dangerous bacterial pathogens. Emerg. Microbes Infect. 3, DOI:10.1038/emi.2014.82 (2014)10.1038/emi.2014.82431763626038506Search in Google Scholar

Fong I.W., Alibek K.: Bioterrorism and infectious agents: a new dilemma for the 21st century (Vol. 4) (w) Tularemia and Bioterrorism, Chapter 3, red. L. Hodges, R.L. Penn, Springer Science & Business Media, Berlin, 2005, s. 71–9810.1007/b102143Search in Google Scholar

Formińska K., Zasada A.A., Rastawicki W., Śmietańska K., Bander D., Wawrzynowicz-Syczewska M., Yanushevych M., Niściogórska-Olsen J., Wawszczak M.: Increasing role of arthropod bites in tularemia transmission in Poland – case of reports and diagnostic methods. Ann. Agric. Environ. Med. 22, 443–446 (2015)Search in Google Scholar

Formińska K., Zasada A.A.: Francisella tularensis– podstępny patogen. Post. Mikrobiol. 56, 187–195 (2017)Search in Google Scholar

Forsman M., Henningson E.W., Larsson E., Johansson T., Sandström G. Francisella tularensis does not manifest virulence in viable but non-culturable state. FEMS Microbiol Ecol. 31, 217–224 (2000)10.1111/j.1574-6941.2000.tb00686.x10719202Search in Google Scholar

Forsman M., Sandström G., Jaurin B.: Identification of Francisella species and discrimination of type A and type B strains of F. tularensis by 16S rRNA analysis. Appl. Environ. Microb. 56, 949–955 (1990)10.1128/aem.56.4.949-955.19901843271692676Search in Google Scholar

Forsman M., Sandstrom G., Sjöstedt A.: Analysis of 16S ribosomal DNA sequences of Francisella strains and utilization for determination of the phylogeny of the genus and for identification of strains by PCR. Int J Syst Microbiol. 44, 38–46 (1994)10.1099/00207713-44-1-388123561Search in Google Scholar

Franke J., Fritzsch J., Tomaso H., Straube E., Dorn W., Hildebrandt A. Coexistence of Pathogens in Host-Seeking and Feeding Ticks within a Single Natural Habitat in Central Germany. Appl. Environ. Microbiol. 76, 6829–6836 (2010)Search in Google Scholar

Friend M.: Tularemia. U.S. Geological Survey, Reston, 2006, s. 1–6810.3133/cir1297Search in Google Scholar

Fujita O., Tatsumi M. Tanabayashi K., Jamada A.: Development of a real-time PCR assay for detection and quantification of Francisella tularensis. Jpn. J. Infect. Dis. 59, 46–51 (2006)Search in Google Scholar

Garrity G.M., Bell J.A., Lilburn T.G.: Taxonomic Outline of the Procaryotes Release 5.0. Bergey’s Manual of and Systematic Bacteriology, 2nd ed, Springer, 2004Search in Google Scholar

Grossman T.H., Anderson M.S., Christ D., Gooldy M., Henning L.N., Heine H.S., Kindt M.V., Lin W., Siefkas-Patterson K., Radclitt A.K., Tam, V.H. Sutclifle J.H. The fluorocycline TP-271 is efficacious in models of aerosolized Francisella tularensis SCHU S4 infection in BALB/c mice and cynomolgus macaques. Antimicrob. Agents and Ch. doi:10.1128/AAC.00448-17 (2017)10.1128/AAC.00448-17552762528559261Search in Google Scholar

Gunnell M.K., Robinson R.A., Adams B.J.: Natural selection in virulence genes of Frnacisella tularensis. J. Mol. Evol. 82, 264–278 (2016)Search in Google Scholar

Gürcan Ş.: Epidemiology of Tularemia. Balk. Med. J. 31, 3–10 (2014)10.5152/balkanmedj.2014.13117411599825207161Search in Google Scholar

Higgins J.A., Hubalek Z., Halouzka J., Elkins K.L., Sjöstedt A., Shipley M., Ibrahim M.S.: Detection of Francisella tularensis in infected mammals and vectors using a probe-based polymerase chain reaction. Am. J. Trop. Med. Hyg. 62, 310–318 (2000)Search in Google Scholar

Hodges L., Penn R. L.: Tularemia and bioterrorism (w) Bioterrorism and infectious agents: A new dilemma for the 21st century, red. I.W. Fong, Kenneth Alibek, Springer, New York, 2005, s. 71–9810.1007/0-387-23685-6_3Search in Google Scholar

Hollis D.G., Weaver R.E., Steigerwalt A.G., Wenger J.D., Moss C.W., Brenner D.J.: Francisella philomiragia comb. nov. (formerly Yersinia philomiragia) and Francisella tularensis biogroup novicida (formerly Francisella novicida) associated with human disease. J. Clin. Microbiol. 27, 1601–1608 (1989)10.1128/jcm.27.7.1601-1608.19892676222671019Search in Google Scholar

Hubalek Z., Rudolf, I.: Francisella tularensis prevalence and load in Dermacentor reticulatus ticks in an endemic area in Central Europe. Med. Vet. Entomol. 31, 234–239 (2017)Search in Google Scholar

Huber B., Escudero R., Busse H.J., Seibold E., Scholz H.C., Anda P., Splettstoesse W.D.: Description of Francisella hispaniensis sp. nov., isolated from human blood, reclassification of Francisella novicida (Larson et al. 1955) Olsufiev et al. 1959 as Francisella tularensis subsp. novicida comb. nov. and emended description of the genus Francisella. Int. J. Syst. Evol. Micr. 60, 1887–1896 (2010)10.1099/ijs.0.015941-019783615Search in Google Scholar

Ivanov I.N., Mitkova N., Reye A.L., Hübschen J.M., Vatcheva-Dobrevska R.S., Dobreva E.G., Muller C.P.: Detection of new Francisella-like tick endosymbionts in Hyalomma spp. and Rhipicephalus spp.(Acari: Ixodidae) from Bulgaria. Appl. Environ. Microb. 77, 5562–5565 (2011)10.1128/AEM.02934-10314744621705542Search in Google Scholar

Jones C.L., Napier B.A., Sampson T.R., Llewellyn A.C., Schroeder M.R., Weiss D.S.: Subversion of host recognition and defense systems by Francisella spp. Microbiol. Mol. Biol. Rev. 76,383–404 (2012)Search in Google Scholar

Kamaishi T., Fukuda Y., NishiJama M., Kawakami H., Matsu-Jama T., Yoshinaga T., Oseko N.: Identification and pathogenicity of intracellular Francisella bacterium in three-line grunt Parapristipoma trilineatum. Fish Pathology. 40, 67–72 (2005)10.3147/jsfp.40.67Search in Google Scholar

Kay W., Petersen B.O., Duus J.Ø., Perry M.B., Vinogradov E.: Characterization of the lipopolysaccharide and β-glucan of the fish pathogen Francisella victoria. FEBS J. 273, 3002–3013 (2006)10.1111/j.1742-4658.2006.05311.x16759227Search in Google Scholar

Keim P., Johansson A., Wagner D.M.: Molecular epidemiology, evolution, and ecology of Francisella. Ann. NY. Acad. Sci. 1105, 30–66 (2007)Search in Google Scholar

Kłapeć T., Cholewa A.: Tularemia – wciąż groźna choroba. Med. Og. Nauk Zdr. 17, 155–160 (2011)Search in Google Scholar

Knap J. Tularemia (Tularaemia) (w) Choroby zakaźne i pasożytnicze – epidemiologia i profilaktyka. 6th ed., red. W. Magdzik D. Naruszewicz-Lesiuk, A. Zieliński, α-medica press, Bielsko-Biała, 2007 s. 312–317Search in Google Scholar

Kocik J. Tularemia (w) Bioterroryzm. Zasady postępowania lekarskiego, red. K. Chomiczewski, J. Kocik, M.T. Szkoda, Państwowy Zakład Wydawnictw Lekarskich, Warszawa, 2002, s. 142–152Search in Google Scholar

Kugeler K.J., Gurfield N., Creek J.G., Mahoney K.S., Versage J.L., Petersen J.M.: Discrimination between Francisella tularensis and Francisella-like endosymbionts when screening ticks by PCR. Appl. Environ. Microb. 71, 7594–7597 (2005)Search in Google Scholar

Larson M.A., Nalbantoglu U., Dayood K., Zentz E.B., Cer R.Z., Iwen P.C., Francesconi S.C., Bishop-Lilly K.A., Mokashi V.P., Sjosted A., Hinrischs S.H.: Reclassification of Wolbachia persica as Francisella persica comb. nov. and emended description of the family Francisellaceae. Int. J. Syst. Evol. Microbiol. 66, 1200– 1205 (2016)Search in Google Scholar

Manuel M.J., Soto E., Moralis J.A., Hawke J.: A piscirickettsiosis-like syndrome in cultured Nile tilapia in Latin America with Francisella spp. as the pathogenic agent. J. Aquat. Anim. Health. 19, 27–34 (2007)Search in Google Scholar

Maron M.E., Barry E.M.: Live attenuated tularemia vaccines: recent development and future goal. Vaccine31, 3485–3491 (2013)10.1016/j.vaccine.2013.05.096376692523764535Search in Google Scholar

Mikalsen J., Colquhoun D.J.: Francisella asiatica sp. nov. isolated from farmed tilapia (Oreochromis sp.) and elevation of Francisella philomiragia subsp. noatunensis to species rank as Francisella noatunensis comb. nov., sp. nov. Int. J. Syst. Evol. Micr. DOI:10.1099/ijs.0.002139-0 (2009)10.1099/ijs.0.002139-019783606Search in Google Scholar

Mikalsen J., Olsen A.B., Tengs T., Colquhoun D.J.: Francisella philomiragia subsp. noatunensis subsp. nov., isolated from farmed Atlantic cod (Gadus morhua L.). Int. J. Syst. Evol. Micr. 57, 1960–1965 (2007)Search in Google Scholar

Mitchell J.L., Chatwell N., Christensen D., Diaper H., Minogue T.D., Parsons T.M., Weller S.A.: Development of real-time PCR assays for the specific detection of Francisella tularensis ssp. tularensis, holarctica and mediaasiatica. Mol. Cell. Probes. 24, 72–76 (2010)Search in Google Scholar

Mitchell S.L., Griffin K.F., Titball R.W.: Tularemia pathogenesis and immunity (w) Microorganisms and Bioterrorism, Springer, New York, 2006 s. 121–13710.1007/0-387-28159-2_7Search in Google Scholar

Morris B.J., Buse H.Y., Adcock N.J., Rice E.W. A novel broth medium for enhanced growth of Francisella tularensis. Lett. Appl. Microbiol. 64, 394–400 (2017)10.1111/lam.12725619880428255998Search in Google Scholar

Nano F., Elkins K.: The Genus Francisella. Chapter 3.3.44, Procaryotes. 6, 1119–1132 (2003)Search in Google Scholar

Olsufjev N.G., Meshcheryakova I.S.: Subspecific taxonomy of Francisella tularensis McCoy and Chapin 1912. Int. J. Syst. Evol. Micr. 13, 872–874 (1983)Search in Google Scholar

Ostland V.E., Stannard J.A., Creek J.J., Hedrick R.P., Ferguson H.W., Carlberg J.M., Westerman M.E.: Aquatic Francisella-like bacterium associated with mortality of intensively cultured hybrid striped bass Morone chrsops × M. saxatilis. Dis. Aquat. Organ. 72, 135–145 (2006)Search in Google Scholar

Ottem K.F., Nylund A., Karlsbakk E., Friis-Møller A., Krossøy B., Knappskog D.: New species in the genus Francisella (Gammaproteobacteria; Francisellaceae); Francisella piscicida sp. nov. isolated from cod (Gadus morhua). Arch. Microbiol. 188, 547–550 (2007)Search in Google Scholar

Ottem K.F., Nylund A., Karlsbakk E., Friis-Møller A., Kamaishi T.: Elevation of Francisella philomiragia subsp. noatunensis to Francisella noatunensis comb. nov. [syn. Francisella piscicidaOttem et al. (2008) syn. nov.] and characterization of Francisella noatunensis subsp. orientalis subsp. nov., two important fish pathogens. J. Appl. Microbiol. 106, 1231–1243 (2009)Search in Google Scholar

Oyston P.C.: Francisella tularensis: unravelling the secrets of an intracellular pathogen. J. Med. Microbiol. 57, 921–930 (2008)10.1099/jmm.0.2008/000653-018628490Search in Google Scholar

Penn R.L.: Francisella tularensis (Tularemia) (w) Principles and Practice of Infectious Diseases, red. L. Gerald, J.E. Mandell, R.D. Bennett, D. Mendel, Bennett, 7th ed. Churchill Livingstone, Elsevier, 2010, volume 2, s. 2927–295010.1016/B978-0-443-06839-3.00227-7Search in Google Scholar

Petersen J.M., Schriefer M.E., Carter L.G., Zhou Y., Sealy T., Bawiec D., Chu M.C.: Laboratory analysis of tularemia in wild-trapped, commercially traded prairie dogs, Texas, 2002. Emerg. Infect. Dis. 10, 419–425 (2004)Search in Google Scholar

Petersen J.M., Schriefer M.E., Gage K.L., Montenieri J.A., Carter L.G., Stanley M., Chu M.C.: Methods for enhanced culture recovery of Francisella tularensis. Appl. Environ. Microb. 70, 3733–3735 (2004)Search in Google Scholar

Porsch-Özcürümez M., Kischel N., Priebe H., Splettstösser W., Finke E.J., Grunow R.: Comparison of enzyme-linked immunosorbent assay, Western blotting, microagglutination, indirect immunofluorescence assay, and flow cytometry for serological diagnosis of tularemia. Clin. Diagn. Lab. Immunol. 11, 1008–1015 (2004)Search in Google Scholar

Qu P.H., Chen S.Y., Scholz H.C., Busse H.J., Gu Q., Kämpfer P., Yang Z.C.: Francisella guangzhouensis sp. nov., isolated from air-conditioning systems. Int. J. Syst. Evol. Micr. 63, 3628–3635 (2013)Search in Google Scholar

Rastawicki W., Jagielski M.: Tularemia. Post Mikrobiol. 44, 265–273 (2005)Search in Google Scholar

Rastawicki W.: Tularemia (Tularaemia) (w) Choroby zakaźne i pasożytnicze – epidemiologia i profilaktyka, 7th ed., red. A. Bauman-Popczyk, M. Sadkowska-Todys, A. Zieliński, α-medica press, Bielsko-Biała, 2014, s. 423–433Search in Google Scholar

Reis C., Cote M., Paul R.E., Bonnet S. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis. 11, 907–916 (2011)10.1089/vbz.2010.010321158500Search in Google Scholar

Rydzewski K., Schulz T., Brzuszkiewicz E., Holland G., Lück C., Fleischer J., Heuner K.: Genome sequence and phenotypic analysis of a first German Francisella sp. isolate (W12-1067) not belonging to the species Francisella tularensis. BMC Microb. 14, 169 (2014)10.1186/1471-2180-14-169423079624961323Search in Google Scholar

Santic M., Akimana C., Asare R., Kouokam J.C., Atay S., Kwaik Y.A.: Intracellular fate of Francisella tularensis within arthropod-derived cells. Environ. Microb. 11, 1473–1481 (2009)Search in Google Scholar

Sato T., Fujita H., Ohara Y., Homma M.: Microagglutination test for early and specific serodiagnosis of tularemia. J. Clin. Microbiol. 28, 2372–2374 (1990)Search in Google Scholar

Schmitt P., Splettstoesser W., Porsch-Özcürümez M., Finke E.J., Grunow R.A.: Novel screening ELISA and a confirmatory Western blot useful for diagnosis and epidemiological studies of tularemia. Epidemiol. Infect. 133, 759–766 (2005)Search in Google Scholar

Schrallhammer M., Schweikert M., Vallesi A., Verni F., Petroni G.: Detection of a novel subspecies of Francisella noatunensis as endosymbiont of the ciliate Euplotes raikovi. Microbial Ecology. 61, 455–464 (2011)10.1007/s00248-010-9772-921110016Search in Google Scholar

Scoles G.A. Phylogenetic analysis of the Francisella-like endosymbionts of Dermacentor ticks. J. Med. Entomol. 41, 277–286 (2004)10.1603/0022-2585-41.3.27715185926Search in Google Scholar

Sharma N., Hotta A., Jamamoto Y., Fujita O., Uda A., Morikawa S., Tanabayashi K.: Detection of Francisella tularensis-specific antibodies in patients with tularemia by a novel competitive enzyme-linked immunosorbent assay. Clin. Vaccine Immunol. 20, 9–16 (2013)10.1128/CVI.00516-12353576923114700Search in Google Scholar

Sinclair R., Boone S.A., Greenberg D., Keim P., Gerba C.P.: Persistence of category A select agents in the environment. Appl. Environ. Microb. 74, 555–563 (2005)Search in Google Scholar

Sjöstedt A., Eriksson U., Berglund L., Tärnvik A.: Detection of Francisella tularensis in ulcers of patients with tularemia by PCR. J. Clin. Microbiol. 35, 1045–1048 (1997)Search in Google Scholar

Sjöstedt A.: Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann. NY Acad. 1105, 1–29 (2007)10.1196/annals.1409.00917395726Search in Google Scholar

Skottman T., Piiparinen H., Hyytiäinen H., Myllys V., Skurnik M., Nikkari S.: Simultaneous real-time PCR detection of Bacillus anthracis, Francisella tularensis and Yersinia pestis. Eur. J. Clin. Microbiol. Infect. Dis. 26, 207–211 (2007)Search in Google Scholar

Skrodzki E.: Tularemia. Państwowy Zakład Wydawnictw Lekarskich. Warszawa, 1978Search in Google Scholar

Steiner D.J., Furuya Y., Jordan M.B., Metzger D.W.: Protective role for macrophages in respiratory Francisella tularensis infection. Infect. Immun. 85, e00064-17 (2017)Search in Google Scholar

Sun L.V., Scoles G.A., Fish D., O’Neill S.L. Francisella-like endosymbionts of ticks. J. Invertebr. Pathol. 76(4), 301–303 (2000)10.1006/jipa.2000.498311112376Search in Google Scholar

Svensson K., Larsson P., Johansson D., Byström M., Forsman M., Johansson A.: Evolution of subspecies of Francisella tularensis. J. Bacteriol. 187, 3903–3908 (2005)10.1128/JB.187.11.3903-3908.2005111205715901721Search in Google Scholar

Tärnvik A., Sandström G., Sjöstedt A. Epidemiological analysis of tularemia in Sweden 1931–1993. FEMS Immunol. Med. Mic. 13, 201–204 (1996)10.1111/j.1574-695X.1996.tb00237.x8861029Search in Google Scholar

Thelaus J., Andersson A., Broman T., Bäckman S., Granberg M., Karlsson L., Forsman M.: Francisella tularensis subspecies holarctica occurs in Swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding. Micro. Ecol. 67, 96–107 (2014)10.1007/s00248-013-0285-1390766724057273Search in Google Scholar

Titball R.W., Petrosino J.F.: Francisella tularensis genomics and proteomics. Ann. NY. Acad. Sci. 1105, 98–121 (2007)Search in Google Scholar

Tomanowić S., Radulović Z., Masuzawa T., Milutinović M. Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia. Parasitic Zoonoses in Europe. 17, 211–217 (2010)Search in Google Scholar

Tomaso H., Scholz H.C., Neubauer H., Al Dahouk S., Seibold E., Landt O., Splettstoesser W.D.: Real-time PCR using hybridization probes for the rapid and specific identification of Francisella tularensis subspecies tularensis. Mol. Cell Probe. 21, 12–16 (2007)10.1016/j.mcp.2006.06.00116893624Search in Google Scholar

Versage J.L., Severin D.D., Chu M.C., Petersen J.M.: Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J. Clin. Microbiol. 41, 5492–5499 (2003)Search in Google Scholar

Wójcik-Fatla A., Zając V., Sawczyn A., Cisak E., Sroka J., Dutkiewicz J. Occurrence of Francisella spp. in Dermacentor reticulatus and Ixodes ricinus ticks collected in eastern Poland. Ticks Tick-Born Dis. 6, 253–257 (2005)10.1016/j.ttbdis.2015.01.00525666656Search in Google Scholar

World Health Organization: Tularemia, https://www.cdc.gov/tularemia/diagnosistreatment/index.html. (26.09.2017)Search in Google Scholar

Zhang F., Liu W., Wu X.M., Xin Z.T., Zhao Q.M., Yang H., Cao W. C. Detection of Francisella tularensis in ticks and identification of their genotypes using multiple-locus variable-number tandem repeat analysis. BMC Microbiology, 8, 152 (2008)10.1186/1471-2180-8-152256798318798995Search in Google Scholar

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