Current Clinical Microbiology Reports

, Volume 4, Issue 1, pp 36–42 | Cite as

Tularemia from a One Health Perspective

  • Herbert Tomaso
  • Helmut Hotzel
Bacteriology (N Borel, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Bacteriology


Tularemia is a rare zoonotic disease caused by Francisella tularensis and is also regarded as a potential biological agent. Therefore, it is prudent to monitor outbreaks of tularemia closely.

Purpose of review

The aim of this review is to provide essential information about diagnostic tools and to focus on the epidemiological situation, especially in Europe.

Recent findings

Outbreak investigations based on whole-genome sequencing data have strengths and limitations, because the genome of F. tularensis is highly conserved. Almost identical isolates can be found over large distances and long periods of time, which makes it necessary to perform phylogeographic analyses always in close conjunction with epidemiological and environmental investigations.


Many reservoir animals and arthropod vectors exist in varying habitats in different geographic regions, but changes of the climate and agricultural techniques will influence the environment and maybe also the relevance of hitherto observed transmission modes.


Tularemia Francisella Reservoir Transmission Genotyping Phylogeography 


Compliance with Ethics Guidelines

Conflict of Interest

Herbert Tomaso and Helmut Hotzel declare they have no competing interests.

Human and Animal Rights and Informed Consent

This article contains no studies with human or animal subjects performed by the authors.


Recently published papers of particular interest have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Johansson A, Farlow J, Larsson P, et al. Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol. 2004;186(17):5808–18. doi: 10.1128/JB.186.17.5808-5818.2004.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Petersen JM, Schriefer ME. Tularemia: emergence/re-emergence. Vet Res. 2005;36(3):455–67. doi: 10.1051/vetres:2005006.CrossRefPubMedGoogle Scholar
  3. 3.
    Petersen JM, Mead PS, Schriefer ME. Francisella tularensis: an arthropod-borne pathogen. Vet Res. 2009;40(2):7. doi: 10.1051/vetres:2008045.CrossRefPubMedGoogle Scholar
  4. 4.
    Willke A, Meric M, Grunow R, et al. An outbreak of oropharyngeal tularaemia linked to natural spring water. J Med Microbiol. 2009;58(Pt 1):112–6. doi: 10.1099/jmm.0.002279-0.CrossRefPubMedGoogle Scholar
  5. 5.
    Dennis DT, Inglesby TV, Henderson DA, et al. Tularemia as a biological weapon: medical and public health management. JAMA. 2001;285(21):2763–73.CrossRefPubMedGoogle Scholar
  6. 6.
    Herriman R. ISIS and bioterrorism: Tularemia planned use in Turkey’s water. 2016.
  7. 7.
    Hepburn MJ, Simpson AJ. Tularemia: current diagnosis and treatment options. Expert Rev Anti-Infect Ther. 2008;6(2):231–40. doi: 10.1586/14787210.6.2.231.CrossRefPubMedGoogle Scholar
  8. 8.
    • Boisset S, Caspar Y, Sutera V, et al. New therapeutic approaches for treatment of tularaemia: a review. Front Cell Infect Microbiol. 2014;4:40. doi: 10.3389/fcimb.2014.00040. Summarizes recent therapeutic approaches.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    WHO. WHO Guidelines on Tularaemia; WHO/CDS/EPR/2007.7. 2007.Google Scholar
  10. 10.
    Glynn AR, Alves DA, Frick O, et al. Comparison of experimental respiratory tularemia in three nonhuman primate species. Comp Immunol Microbiol Infect Dis. 2015;39:13–24. doi: 10.1016/j.cimid.2015.01.003.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Tularemia (Francisella tularensis) 1999 Case Definition. Centers for Disease Control and Prevention. 1999. 2016.Google Scholar
  12. 12.
    • Chaignat V, Djordjevic-Spasic M, Ruettger A, et al. Performance of seven serological assays for diagnosing tularemia. BMC Infect Dis. 2014;14:234. doi: 10.1186/1471-2334-14-234. Summarizes serological assays for diagnosis.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Porsch-Ozcurumez M, Kischel N, Priebe H, et al. Comparison of enzyme-linked immunosorbent assay, Western blotting, microagglutination, indirect immunofluorescence assay, and flow cytometry for serological diagnosis of tularemia. Clin Diagn Lab Immunol. 2004;11(6):1008–15. doi: 10.1128/CDLI.11.6.1008-1015.2004.PubMedPubMedCentralGoogle Scholar
  14. 14.
    Birdsell DN, Vogler AJ, Buchhagen J, et al. TaqMan real-time PCR assays for single-nucleotide polymorphisms which identify Francisella tularensis and its subspecies and subpopulations. PLoS One. 2014;9(9), e107964. doi: 10.1371/journal.pone.0107964.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Versage JL, Severin DD, Chu MC, et al. Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J Clin Microbiol. 2003;41(12):5492–9.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Tomaso H, Scholz HC, Neubauer H, et al. Real-time PCR using hybridization probes for the rapid and specific identification of Francisella tularensis subspecies tularensis. Mol Cell Probes. 2007;21(1):12–6. doi: 10.1016/j.mcp.2006.06.001.CrossRefPubMedGoogle Scholar
  17. 17.
    Kilic S, Celebi B, Yesilyurt M. Evaluation of a commercial immunochromatographic assay for the serologic diagnosis of tularemia. Diagn Microbiol Infect Dis. 2012;74(1):1–5. doi: 10.1016/j.diagmicrobio.2012.05.030.CrossRefPubMedGoogle Scholar
  18. 18.
    Michelet L, Bonnet S, Madani N, et al. Discriminating Francisella tularensis and Francisella-like endosymbionts in Dermacentor reticulatus ticks: evaluation of current molecular techniques. Vet Microbiol. 2013;163(3–4):399–403. doi: 10.1016/j.vetmic.2013.01.014.CrossRefPubMedGoogle Scholar
  19. 19.
    Zasada AA, Forminska K, Zacharczuk K, et al. Comparison of eleven commercially available rapid tests for detection of Bacillus anthracis, Francisella tularensis and Yersinia pestis. Lett Appl Microbiol. 2015;60(5):409–13. doi: 10.1111/lam.12392.CrossRefPubMedGoogle Scholar
  20. 20.
    Seibold E, Bogumil R, Vorderwulbecke S, et al. Optimized application of surface-enhanced laser desorption/ionization time-of-flight MS to differentiate Francisella tularensis at the level of subspecies and individual strains. FEMS Immunol Med Microbiol. 2007;49(3):364–73. doi: 10.1111/j.1574-695X.2007.00216.x.CrossRefPubMedGoogle Scholar
  21. 21.
    Karatuna O, Celebi B, Can S, et al. The use of Matrix-assisted laser desorption ionization-time of flight mass spectrometry in the identification of Francisella tularensis. Bosn J Basic Med Sci. 2016;16(2):132–8. doi: 10.17305/bjbms.2016.894.PubMedPubMedCentralGoogle Scholar
  22. 22.
    •• OIE. Chapter 2.01.22 Tularemia. OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2016 2016. Official manual for diagnostics in veterinary medicine.Google Scholar
  23. 23.
    Tomaso H, Al Dahouk S, Hofer E, et al. Antimicrobial susceptibilities of Austrian Francisella tularensis holarctica biovar II strains. Int J Antimicrob Agents. 2005;26(4):279–84. doi: 10.1016/j.ijantimicag.2005.07.003.CrossRefPubMedGoogle Scholar
  24. 24.
    Valade E, Vaissaire J, Merens A, et al. Susceptibility of 71 French isolates of Francisella tularensis subsp. holarctica to eight antibiotics and accuracy of the Etest method. J Antimicrob Chemother. 2008;62(1):208–10. doi: 10.1093/jac/dkn146.CrossRefPubMedGoogle Scholar
  25. 25.
    Kreizinger Z, Makrai L, Helyes G, et al. Antimicrobial susceptibility of Francisella tularensis subsp. holarctica strains from Hungary, Central Europe. J Antimicrob Chemother. 2013;68(2):370–3. doi: 10.1093/jac/dks399.CrossRefPubMedGoogle Scholar
  26. 26.
    Georgi E, Schacht E, Scholz HC, et al. Standardized broth microdilution antimicrobial susceptibility testing of Francisella tularensis subsp. holarctica strains from Europe and rare Francisella species. J Antimicrob Chemother. 2012;67(10):2429–33. doi: 10.1093/jac/dks238.CrossRefPubMedGoogle Scholar
  27. 27.
    Becker S, Lochau P, Jacob D, et al. Successful re-evaluation of broth medium T for growth of Francisella tularensis ssp. and other highly pathogenic bacteria. J Microbiol Methods. 2016;121:5–7. doi: 10.1016/j.mimet.2015.11.018.CrossRefPubMedGoogle Scholar
  28. 28.
    Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard - Eigth Edition. vol CLSI document M07-A8. Clinical and Laboratory Standards Institute; 2009.Google Scholar
  29. 29.
    Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria; Approved Guideline - Second Edition. CLSI document M45-A2. 2010.Google Scholar
  30. 30.
    Tarnvik A, Priebe HS, Grunow R. Tularaemia in Europe: an epidemiological overview. Scand J Infect Dis. 2004;36(5):350–5.CrossRefPubMedGoogle Scholar
  31. 31.
    Rossow H, Sissonen S, Koskela KA, et al. Detection of Francisella tularensis in voles in Finland. Vector Borne Zoonotic Dis. 2014;14(3):193–8. doi: 10.1089/vbz.2012.1255.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Kuehn A, Schulze C, Kutzer P, et al. Tularaemia seroprevalence of captured and wild animals in Germany: the fox (Vulpes vulpes) as a biological indicator. Epidemiol Infect. 2013;141(4):833–40. doi: 10.1017/S0950268812001008.CrossRefPubMedGoogle Scholar
  33. 33.
    Otto P, Chaignat V, Klimpel D, et al. Serological investigation of wild boars (Sus scrofa) and red foxes (Vulpes vulpes) as indicator animals for circulation of Francisella tularensis in Germany. Vector Borne Zoonotic Dis. 2014;14(1):46–51. doi: 10.1089/vbz.2013.1321.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Al Dahouk S, Nockler K, Tomaso H, et al. Seroprevalence of brucellosis, tularemia, and yersiniosis in wild boars (Sus scrofa) from north-eastern Germany. J Vet Med B Infect Dis Vet Public Health. 2005;52(10):444–55. doi: 10.1111/j.1439-0450.2005.00898.x.CrossRefPubMedGoogle Scholar
  35. 35.
    Maraha B, Hajer G, Sjodin A, et al. Indigenous Infection with Francisella tularensis holarctica in The Netherlands. Case Rep Infect Dis. 2013;2013:916985. doi: 10.1155/2013/916985.PubMedPubMedCentralGoogle Scholar
  36. 36.
    Rijks JM, Kik M, Koene MG et al. Tularaemia in a brown hare (Lepus europaeus) in 2013: first case in the Netherlands in 60 years. Euro Surveill. 2013;18(49).Google Scholar
  37. 37.
    van de Wetering D. Oliveira dos Santos C, Wagelaar M et al. A cluster of tularaemia after contact with a dead hare in the Netherlands. Neth J Med. 2015;73(10):481–2.PubMedGoogle Scholar
  38. 38.
    Dupont E, Van Eeckhoudt S, Thissen X, et al. About three cases of ulceroglandular tularemia, is this the re-emergence of Francisella tularensis in Belgium? Acta Clin Belg. 2015;70(5):364–8. doi: 10.1179/2295333715Y.0000000022.CrossRefPubMedGoogle Scholar
  39. 39.
    Rossow H, Ollgren J, Klemets P, et al. Risk factors for pneumonic and ulceroglandular tularaemia in Finland: a population-based case-control study. Epidemiol Infect. 2014;142(10):2207–16. doi: 10.1017/S0950268813002999.CrossRefPubMedGoogle Scholar
  40. 40.
    Decors A, Lesage C, Jourdain E et al. Outbreak of tularaemia in brown hares (Lepus europaeus) in France, January to March 2011. Euro Surveill. 2011;16(28).Google Scholar
  41. 41.
    Tobudic S, Nedomansky K, Poeppl W, et al. Seroprevalence for Coxiella burnetii, Francisella tularensis, Brucella abortus and Brucella melitensis in Austrian adults: a cross-sectional survey among military personnel and civilians. Ticks Tick Borne Dis. 2014;5(3):315–7. doi: 10.1016/j.ttbdis.2013.12.007.CrossRefPubMedGoogle Scholar
  42. 42.
    Zakutna L, Dorko E, Rimarova K, et al. Pilot Cross-Sectional Study of Three Zoonoses (Lyme Disease, Tularaemia, Leptospirosis) among Healthy Blood Donors in Eastern Slovakia. Cent Eur J Public Health. 2015;23(2):100–6. doi: 10.21101/cejph.a4052.CrossRefGoogle Scholar
  43. 43.
    Jurke A, Bannert N, Brehm K, et al. Serological survey of Bartonella spp., Borrelia burgdorferi, Brucella spp., Coxiella burnetii, Francisella tularensis, Leptospira spp., Echinococcus, Hanta-, TBE- and XMR-virus infection in employees of two forestry enterprises in North Rhine-Westphalia, Germany, 2011-2013. Int J Med Microbiol. 2015;305(7):652–62. doi: 10.1016/j.ijmm.2015.08.015.CrossRefPubMedGoogle Scholar
  44. 44.
    Zukiewicz-Sobczak W, Zwolinski J, Chmielewska-Badora J, et al. Prevalence of antibodies against selected zoonotic agents in forestry workers from eastern and southern Poland. Ann Agric Environ Med. 2014;21(4):767–70. doi: 10.5604/12321966.1129930.CrossRefPubMedGoogle Scholar
  45. 45.
    Rossow H, Ollgren J, Hytonen J, et al. Incidence and seroprevalence of tularaemia in Finland, 1995 to 2013: regional epidemics with cyclic pattern. Euro Surveill. 2015;20(33):21209.CrossRefPubMedGoogle Scholar
  46. 46.
    Mailles A, Vaillant V. 10 years of surveillance of human tularaemia in France. Euro Surveill. 2014;19(45):20956.CrossRefPubMedGoogle Scholar
  47. 47.
    Hauri AM, Hofstetter I, Seibold E, et al. Investigating an airborne tularemia outbreak. Germany Emerg Infect Dis. 2010;16(2):238–43. doi: 10.3201/eid1602.081727.CrossRefPubMedGoogle Scholar
  48. 48.
    Elashvili E, Kracalik I, Burjanadze I, et al. Environmental Monitoring and Surveillance of Rodents and Vectors for Francisella tularensis Following Outbreaks of Human Tularemia in Georgia. Vector Borne Zoonotic Dis. 2015;15(10):633–6. doi: 10.1089/vbz.2015.1781.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Gyuranecz M, Reiczigel J, Krisztalovics K, et al. Factors influencing emergence of tularemia, Hungary, 1984–2010. Emerg Infect Dis. 2012;18(8):1379–81. doi: 10.3201/eid1808.111826.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Luque-Larena JJ, Mougeot F, Roig DV, et al. Tularemia Outbreaks and Common Vole (Microtus arvalis) Irruptive Population Dynamics in Northwestern Spain, 1997–2014. Vector Borne Zoonotic Dis. 2015;15(9):568–70. doi: 10.1089/vbz.2015.1770.CrossRefPubMedGoogle Scholar
  51. 51.
    Ryden P, Bjork R, Schafer ML, et al. Outbreaks of tularemia in a boreal forest region depends on mosquito prevalence. J Infect Dis. 2012;205(2):297–304. doi: 10.1093/infdis/jir732.CrossRefPubMedGoogle Scholar
  52. 52.
    Hanke CA, Otten JE, Berner R, et al. Ulceroglandular tularemia in a toddler in Germany after a mosquito bite. Eur J Pediatr. 2009;168(8):937–40. doi: 10.1007/s00431-008-0862-3.CrossRefPubMedGoogle Scholar
  53. 53.
    Forminska K, Zasada AA, Rastawicki W, et al. Increasing role of arthropod bites in tularaemia transmission in Poland - case reports and diagnostic methods. Ann Agric Environ Med. 2015;22(3):443–6. doi: 10.5604/12321966.1167711.CrossRefPubMedGoogle Scholar
  54. 54.
    • Thelaus J, Andersson A, Broman T, et al. Francisella tularensis subspecies holarctica occurs in Swedish mosquitoes, persists through the developmental stages of laboratory-infected mosquitoes and is transmissible during blood feeding. Microb Ecol. 2014;67(1):96–107. doi: 10.1007/s00248-013-0285-1. Transmission of F. tularensis by insects.CrossRefPubMedGoogle Scholar
  55. 55.
    Genchi M, Prati P, Vicari N, et al. Francisella tularensis: No Evidence for Transovarial Transmission in the Tularemia Tick Vectors Dermacentor reticulatus and Ixodes ricinus. PLoS One. 2015;10(8), e0133593. doi: 10.1371/journal.pone.0133593.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Klock LE, Olsen PF, Fukushima T. Tularemia epidemic associated with the deerfly. JAMA. 1973;226(2):149–52.CrossRefPubMedGoogle Scholar
  57. 57.
    Ryden P, Sjostedt A, Johansson A. Effects of climate change on tularaemia disease activity in Sweden. Glob Health Action. 2009. doi: 10.3402/gha.v2i0.2063.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Aktas D, Celebi B, Isik ME, et al. Oropharyngeal Tularemia Outbreak Associated with Drinking Contaminated Tap Water, Turkey, July–September 2013. Emerg Infect Dis. 2015;21(12):2194–6. doi: 10.3201/eid2112.142032.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Kilic S, Birdsell DN, Karagoz A, et al. Water as Source of Francisella tularensis Infection in Humans. Turkey Emerg Infect Dis. 2015;21(12):2213–6. doi: 10.3201/eid2112.150634.CrossRefPubMedGoogle Scholar
  60. 60.
    Ughetto E, Hery-Arnaud G, Cariou ME, et al. An original case of Francisella tularensis subsp. holarctica bacteremia after a near-drowning accident. Infect Dis (Lond). 2015;47(8):588–90. doi: 10.3109/23744235.2015.1028099.CrossRefGoogle Scholar
  61. 61.
    •• Desvars A, Furberg M, Hjertqvist M, et al. Epidemiology and ecology of tularemia in Sweden, 1984–2012. Emerg Infect Dis. 2015;21(1):32–9. doi: 10.3201/eid2101.140916. Summarizes eopidemiological situation concerning tularemia over many years.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Broman T, Thelaus J, Andersson AC, et al. Molecular Detection of Persistent Francisella tularensis Subspecies holarctica in Natural Waters. Int J Microbiol. 2011. doi: 10.1155/2011/851946.PubMedGoogle Scholar
  63. 63.
    Grunow R, Kalaveshi A, Kuhn A et al. Surveillance of tularaemia in Kosovo, 2001 to 2010. Euro Surveill. 2012;17(28).Google Scholar
  64. 64.
    Djordjevic-Spasic M, Potkonjak A, Kostic V, et al. Oropharyngeal tularemia in father and son after consumption of under-cooked rabbit meat. Scand J Infect Dis. 2011;43(11–12):977–81. doi: 10.3109/00365548.2011.592988.CrossRefPubMedGoogle Scholar
  65. 65.
    Komitova R, Nenova R, Padeshki P, et al. Tularemia in bulgaria 2003–2004. J Infect Dev Ctries. 2010;4(11):689–94.CrossRefPubMedGoogle Scholar
  66. 66.
    Hristovski KD, Pacemska-Atanasova T, Olson LW, et al. Potential health implications of water resources depletion and sewage discharges in the Republic of Macedonia. J Water Health. 2016;14(4):682–91. doi: 10.2166/wh.2016.274.CrossRefPubMedGoogle Scholar
  67. 67.
    RKI. SurvStat@RKI 2.0. Robert Koch Institut, Berlin, Germany. 2016.
  68. 68.
    Padeshki PI, Ivanov IN, Popov B, et al. The role of birds in dissemination of Francisella tularensis: first direct molecular evidence for bird-to-human transmission. Epidemiol Infect. 2010;138(3):376–9. doi: 10.1017/S0950268809990513.CrossRefPubMedGoogle Scholar
  69. 69.
    Hildebrandt A, Franke J, Schmoock G, et al. Diversity and coexistence of tick-borne pathogens in central Germany. J Med Entomol. 2011;48(3):651–5.CrossRefPubMedGoogle Scholar
  70. 70.
    Toma L, Mancini F, Di Luca M, et al. Detection of microbial agents in ticks collected from migratory birds in central Italy. Vector Borne Zoonotic Dis. 2014;14(3):199–205. doi: 10.1089/vbz.2013.1458.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Nordstoga A, Handeland K, Johansen TB, et al. Tularaemia in Norwegian dogs. Vet Microbiol. 2014;173(3–4):318–22. doi: 10.1016/j.vetmic.2014.06.031.CrossRefPubMedGoogle Scholar
  72. 72.
    Larson MA, Fey PD, Hinrichs SH, et al. Francisella tularensis bacteria associated with feline tularemia in the United States. Emerg Infect Dis. 2014;20(12):2068–71. doi: 10.3201/eid2012.131101.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Pennisi MG, Egberink H, Hartmann K, et al. Francisella tularensis infection in cats: ABCD guidelines on prevention and management. J Feline Med Surg. 2013;15(7):585–7. doi: 10.1177/1098612X13489219.CrossRefPubMedGoogle Scholar
  74. 74.
    Eliasson H, Lindback J, Nuorti JP, et al. The 2000 tularemia outbreak: a case-control study of risk factors in disease-endemic and emergent areas. Sweden Emerg Infect Dis. 2002;8(9):956–60. doi: 10.3201/eid0809.020051.CrossRefPubMedGoogle Scholar
  75. 75.
    Karlsson E, Svensson K, Lindgren P, et al. The phylogeographic pattern of Francisella tularensis in Sweden indicates a Scandinavian origin of Eurosiberian tularaemia. Environ Microbiol. 2013;15(2):634–45. doi: 10.1111/1462-2920.12052.CrossRefPubMedGoogle Scholar
  76. 76.
    Afset JE, Larssen KW, Bergh K, et al. Phylogeographical pattern of Francisella tularensis in a nationwide outbreak of tularaemia in Norway, 2011. Euro Surveill. 2015;20(19):9–14.CrossRefPubMedGoogle Scholar
  77. 77.
    Lu Y, Yu Y, Feng L, et al. Phylogeography of Francisella tularensis from Tibet, China: Evidence for an asian origin and radiation of holarctica-type Tularemia. Ticks Tick Borne Dis. 2016. doi: 10.1016/j.ttbdis.2016.04.001.PubMedGoogle Scholar
  78. 78.
    Vogler AJ, Birdsell D, Price LB, et al. Phylogeography of Francisella tularensis: global expansion of a highly fit clone. J Bacteriol. 2009;191(8):2474–84. doi: 10.1128/JB.01786-08.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Keim PS, Wagner DM. Humans and evolutionary and ecological forces shaped the phylogeography of recently emerged diseases. Nat Rev Microbiol. 2009;7(11):813–21. doi: 10.1038/nrmicro2219.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Pandya GA, Holmes MH, Petersen JM, et al. Whole genome single nucleotide polymorphism based phylogeny of Francisella tularensis and its application to the development of a strain typing assay. BMC Microbiol. 2009;9:213. doi: 10.1186/1471-2180-9-213.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Svensson K, Granberg M, Karlsson L, et al. A real-time PCR array for hierarchical identification of Francisella isolates. PLoS One. 2009;4(12), e8360. doi: 10.1371/journal.pone.0008360.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Chanturia G, Birdsell DN, Kekelidze M, et al. Phylogeography of Francisella tularensis subspecies holarctica from the country of Georgia. BMC Microbiol. 2011;11:139. doi: 10.1186/1471-2180-11-139.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Gyuranecz M, Birdsell DN, Splettstoesser W, et al. Phylogeography of Francisella tularensis subsp. holarctica, Europe. Emerg Infect Dis. 2012;18(2):290–3. doi: 10.3201/eid1802.111305.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Karadenizli A, Forsman M, Simsek H et al. Genomic analyses of Francisella tularensis strains confirm disease transmission from drinking water sources, Turkey, 2008, 2009 and 2012. Euro Surveill. 2015;20(21)Google Scholar
  85. 85.
    Sissonen S, Rossow H, Karlsson E, et al. Phylogeography of Francisella tularensis subspecies holarctica in Finland, 1993–2011. Infect Dis (Lond). 2015;47(10):701–6. doi: 10.3109/23744235.2015.1049657.CrossRefGoogle Scholar
  86. 86.
    Antwerpen MH, Prior K, Mellmann A, et al. Rapid high resolution genotyping of Francisella tularensis by whole genome sequence comparison of annotated genes ("MLST+"). PLoS One. 2015;10(4), e0123298. doi: 10.1371/journal.pone.0123298.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Johansson A, Larkeryd A, Widerstrom M, et al. An outbreak of respiratory tularemia caused by diverse clones of Francisella tularensis. Clin Infect Dis. 2014;59(11):1546–53. doi: 10.1093/cid/ciu621.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    •• Wahab T, Birdsell DN, Hjertqvist M, et al. Insights to genetic characterization tools for epidemiological tracking of Francisella tularensis in Sweden. PLoS One. 2014;9(11):e112167. doi: 10.1371/journal.pone.0112167. Application of different typing methods for epidemiology.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Huber B, Escudero R, Busse HJ, et al. 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 Microbiol. 2010;60(Pt 8):1887–96. doi: 10.1099/ijs.0.015941-0.CrossRefPubMedGoogle Scholar
  90. 90.
    Lopes de Carvalho I, Toledo A, Carvalho CL, et al. Francisella species in ticks and animals Iberian Peninsula. Ticks Tick Borne Dis. 2016;7(1):159–65. doi: 10.1016/j.ttbdis.2015.10.009.CrossRefPubMedGoogle Scholar
  91. 91.
    Aravena-Roman M, Merritt A, Inglis TJ. First case of Francisella bacteraemia in Western Australia. New Microbes New Infect. 2015;8:75–7. doi: 10.1016/j.nmni.2015.10.004.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Qu PH, Chen SY, Scholz HC, et al. Francisella guangzhouensis sp. nov., isolated from air-conditioning systems. Int J Syst Evol Microbiol. 2013;63(Pt 10):3628–35. doi: 10.1099/ijs.0.049916-0.CrossRefPubMedGoogle Scholar
  93. 93.
    Svensson D, Ohrman C, Backman S et al. Complete Genome Sequence of Francisella guangzhouensis Strain 08HL01032T, Isolated from Air-Conditioning Systems in China. Genome Announc. 2015;3(2). doi: 10.1128/genomeA.00024-15.
  94. 94.
    Rydzewski K, Schulz T, Brzuszkiewicz E, et al. Genome sequence and phenotypic analysis of a first German Francisella sp. isolate (W12-1067) not belonging to the species Francisella tularensis. BMC Microbiol. 2014;14:169. doi: 10.1186/1471-2180-14-169.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Institute of Bacterial Infections and Zoonoses, National Reference Laboratory for TularemiaFriedrich-Loeffler-Institut (Federal Research Institute for Animal Health)JenaGermany

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