Advertisement

Infection

pp 1–13 | Cite as

Tularemia: an experience of 13 cases including a rare myocarditis in a referral center in Eastern Switzerland (Central Europe) and a review of the literature

  • Manuel Frischknecht
  • Angelina Meier
  • Bernhard Mani
  • Lucas Joerg
  • Olaf Chan-Hi Kim
  • Katia Boggian
  • Carol StrahmEmail author
Review

Abstract

Background

Tularemia, a zoonotic disease caused by Francisella tularensis, can cause a broad spectrum of disease in humans including six major clinical presentations: the ulceroglandular, glandular, oculoglandular, oropharyngeal, typhoidal and pneumonic form. The epidemiology and ecology and thus transmission of tularemia are complex, depending on conditions unique to specific locations.

Case series and methods

Thirteen cases with different forms of the disease and one very rare case of a myocarditis are reported, discussed, and reviewed within the scope of current literature.

Conclusion

Tularemia is a rare, but emerging disease in Central Europe with glandular and ulceroglandular disease as its predominant forms. Transmission is mainly caused by contact with lagomorphs, rodents and tick bites. However, domestic cats may play an important role in transmission too. Myocarditis is probably a worldwide, but very rare manifestation of tularemia.

Keywords

Tularemia Francisella tularensis Myocarditis Oculoglandular tularemia Glandular tularemia Pulmonary tularemia 

Abbreviations

GP

General practitioner

ER

Emergency room

CRP

C-reactive protein

WBC

White blood cells

AST

Aspartate aminotransferase

ALT

Alanine aminotransferase

LDH

Lactate dehydrogenase

CK

Creatine kinase

U/ml

Units per milliliter

U/l

Units per liter

G/l

Giga per liter

mg/l

Milligram per liter

ng/l

Nanogram per liter

PCR

Polymerase chain reaction

ECG

Electrocardiogram

CT

Computed tomography

MRI

Magnetic resonance imaging

PET

Positron emissions tomography

I.V.

Intravenous

ELISA

Enzyme-linked immunosorbent assay

Bid

Twice a day

NSAID

Nonsteroidal anti-inflammatory drugs

Ssp.

Subspecies

DNA

Deoxyribonucleic acid

RNA

Ribonucleic acid

Notes

Acknowledgements

In particular, we would like to thank Nancy Landes and Carol Idone for the language editing.

Compliance with ethical standards

Conflict of interest

We received no financial support for this work. We state that there is no conflict of interest.

Informed consent

Written informed consent for publication of the cases and images was obtained from all the patients.

References

  1. 1.
    Ellis J, Oyston PCF, Green M, Titball RW. Tularemia. Clin Microbiol Rev. 2002;15:631–46.CrossRefGoogle Scholar
  2. 2.
    Tärnvik A, Berglund L. Tularaemia. Eur Respir J. 2003;21:361–73.  https://doi.org/10.1183/09031936.03.00088903.CrossRefGoogle Scholar
  3. 3.
    Tularämie, Hasenpest—Ein Überblick. Bundesamt für Gesundh. BAG. 2012. https://www.bag.admin.ch/bag/de/home/themen/mensch-gesundheit/uebertragbare-krankheiten/infektionskrankheiten-a-z/tularaemie.html. Accessed 5 Jan 2017.
  4. 4.
    Keim P, Johansson A, Wagner DM. Molecular epidemiology, evolution, and ecology of Francisella. Ann N Y Acad Sci. 2007;1105:30–66.  https://doi.org/10.1196/annals.1409.011.CrossRefGoogle Scholar
  5. 5.
    Penn RL. 229—Francisella tularensis (Tularemia). In: Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. 2015. [cited 2017 Aug 20]. pp. 2590–2602.e3. http://www.sciencedirect.com/science/article/pii/B9781455748013002290.
  6. 6.
    Sjöstedt A. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci. 2007;1105:1–29.  https://doi.org/10.1196/annals.1409.009.CrossRefGoogle Scholar
  7. 7.
    Mailles A, Vaillant V. 10 years of surveillance of human tularaemia in France. Eurosurveillance 2014;19:20956.  https://doi.org/10.2807/1560-7917.ES2014.19.45.20956 CrossRefGoogle Scholar
  8. 8.
    Jackson J, McGregor A, Cooley L, Ng J, Brown M, Ong CW, et al. Francisella tularensis subspecies holarctica, Tasmania, Australia, 2011. Emerg Infect Dis. 2012;18:1484–6.CrossRefGoogle Scholar
  9. 9.
    Maurin M, Gyuranecz M. Tularaemia: clinical aspects in Europe. Lancet Infect Dis. 2016;16:113–24.CrossRefGoogle Scholar
  10. 10.
    Kugeler KJ, Janusz AM, Staples JE, Kubota KA, Chalcraft LG, Petersen JM. Molecular epidemiology of Francisella tularensis in the United States. Clin Infect Dis. 2009;48:863–70.  https://doi.org/10.1086/597261.CrossRefGoogle Scholar
  11. 11.
    Farlow J, Wagner DM, Dukerich M, Stanley M, Chu M, Kubota K, et al. Francisella tularensis in the United States. Emerg Infect Dis. 2005;11:1835–41.CrossRefGoogle Scholar
  12. 12.
    Alias T, Fallahzadeh MK, Berhe M. Tularemia presenting as pulmonary nodules in an immunocompromised patient. Bayl Univ Med Cent Proc. 2017;30:175–6.CrossRefGoogle Scholar
  13. 13.
    Franzen D, Müller F, Bode PK. Lung mass and tularaemia. QJM. 2016;109:417–8.CrossRefGoogle Scholar
  14. 14.
    Odegaard K, Boersma B, Keegan J. Atypical presentations of tularemia. S D Med U S. 2017;70:207–9.Google Scholar
  15. 15.
    Naughton M, Brown R, Adkins D, DiPersio J. Tularemia—an unusual cause of a solitary pulmonary nodule in the post-transplant setting. Bone Marrow Transpl. 1999;24:197–9.CrossRefGoogle Scholar
  16. 16.
    Fachinger P, Tini GM, Grobholz R, Gambazzi F, Fankhauser H, Irani S. Pulmonary tularaemia: all that looks like cancer is not necessarily cancer—case report of four consecutive cases. BMC Pulm Med. 2015;15:1–6.CrossRefGoogle Scholar
  17. 17.
    Genchi M, Prati P, Vicari N, Manfredini A, Sacchi L, Clementi E, et al. Francisella tularensis: no evidence for transovarial transmission in the tularemia tick vectors dermacentor reticulatus and ixodes ricinus. PLoS One. 2015;10:e0133593.CrossRefGoogle Scholar
  18. 18.
    Johansson A, Lärkeryd A, Widerström M, Mörtberg S, Myrtännäs K, Öhrman C, et al. An outbreak of respiratory tularemia caused by diverse clones of Francisella tularensis. Clin Infect Dis. 2014;59:1546–53.CrossRefGoogle Scholar
  19. 19.
    Eliasson H, Lindbäck J, Pekka Nuorti J, Arneborn M, Giesecke J, Tegnell A. The 2000 tularemia outbreak: a case-control study of risk factors in disease-endemic and emergent areas, Sweden. Emerg Infect Dis. 2002;8:956–60.CrossRefGoogle Scholar
  20. 20.
    Capellan J, Fong IW. Tularemia from a cat bite: case report and review of feline-associated tularemia. Clin Infect Dis. 1928;16:472–5.CrossRefGoogle Scholar
  21. 21.
    Petersson E, Athlin S. Cat-bite-induced Francisella tularensis infection with a false-positive serological reaction for Bartonella quintana. JMM Case Rep. 2017;4:4–7.  https://doi.org/10.1099/jmmcr.0.005071.Google Scholar
  22. 22.
    Larson MA, Fey PD, Hinrichs SH, Iwen PC. Francisella tularensis bacteria associated with feline tularemia in the United States. Emerg Infect Dis. 2014;20:2068–71.CrossRefGoogle Scholar
  23. 23.
    Shaw SE, Birtles RJ, Day MJ. Arthropod-transmitted infectious diseases of cats. J Feline Med Surg. 2001;3:193–209.CrossRefGoogle Scholar
  24. 24.
    Federal Office of Public Health FOPH Switzerland. https://www.bag.admin.ch/bag/de/home/zahlen-undstatistiken/zahlen-zu-infektionskrankheiten.exturl.html. Accessed 1 Dec 2017.
  25. 25.
    Ernst M, Pilo P, Fleisch F, Glisenti P. Tularemia in the Southeastern Swiss Alps at 1,700 m above sea level. Infection. 2015;43:111–5.CrossRefGoogle Scholar
  26. 26.
    Tärnvik A, Chu MC. New approaches to diagnosis and therapy of tularemia. Ann N Y Acad Sci. 2007;404:378–404.CrossRefGoogle Scholar
  27. 27.
    Lamps LW, Havens JM, Sjostedt A, Page DL, Scott MA Histologic and molecular diagnosis of tularemia: a potential bioterrorism agent endemic to North America. Mod Pathol. 2004;17:489–95.CrossRefGoogle Scholar
  28. 28.
    Erdem H, Ozturk-Engin D, Yesilyurt M, Karabay O, Elaldi N, Celebi G, et al. Evaluation of tularaemia courses: a multicentre study from Turkey. Clin Microbiol Infect. 2014;20:O1042–51.  https://doi.org/10.1111/1469-0691.12741.CrossRefGoogle Scholar
  29. 29.
    Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, et al. Tularemia as a biological weapon: medical and public health management. JAMA U S. 2001;285:2763–73.CrossRefGoogle Scholar
  30. 30.
    WHO guidelines on tularaemia. WHO Libr. Cat. Data. 2007.Google Scholar
  31. 31.
    Caspar Y, Hennebique A, Maurin M. Antibiotic susceptibility of Francisella tularensis subsp. holarctica strains isolated from tularaemia patients in France between 2006 and 2016. J Antimicrob Chemother Engl. 2017;73:687–91.CrossRefGoogle Scholar
  32. 32.
    Tomaso H, Hotzel H, Otto P, Myrtennas K, Forsman M. Antibiotic susceptibility in vitro of Francisella tularensis subsp. holarctica isolates from Germany. J Antimicrob Chemother England. 2017;72:2539–43.CrossRefGoogle Scholar
  33. 33.
    Ulu-Kilic A, Gulen G, Sezen F, Kilic S, Sencan I. Tularemia in central Anatolia. Infect Ger. 2013;41:391–9.CrossRefGoogle Scholar
  34. 34.
    Meric M, Willke A, Finke E-J, Grunow R, Sayan M, Erdogan S, et al. Evaluation of clinical, laboratory, and therapeutic features of 145 tularemia cases: the role of quinolones in oropharyngeal tularemia. APMIS Den. 2008;116:66–73.CrossRefGoogle Scholar
  35. 35.
    Pérez-Castrillón JL, Bachiller-Luque P, Martín-Luquero M, Mena-Martín FJ, Herreros V. Tularemia epidemic in northwestern Spain: clinical description and therapeutic response. Clin Infect Dis U S. 2001;33:573–6.CrossRefGoogle Scholar
  36. 36.
    Enderlin G, Morales L, Jacobs RF, Cross JT. Streptomycin and alternative agents for the treatment of tularemia: review of the literature. Clin Infect Dis. 1994;19:42–7.CrossRefGoogle Scholar
  37. 37.
    Penn RL, Kinasewitz GT. Factors associated with a poor outcome in tularemia. Arch Intern Med U S. 1987;147:265–8.CrossRefGoogle Scholar
  38. 38.
    Eliasson H, Back E. Tularaemia in an emergent area in Sweden: an analysis of 234 cases in five years. Scand J Infect Dis Engl. 2007;39:880–9.CrossRefGoogle Scholar
  39. 39.
    Risi GF, Pombo DJ. Relapse of tularemia after aminoglycoside therapy: case report and discussion of therapeutic options. Clin Infect Dis U S. 1995;20:174–5.CrossRefGoogle Scholar
  40. 40.
    Origgi FC, Frey J, Pilo P. Characterisation of a new group of Francisella tularensis subsp. holarctica in Switzerland with altered antimicrobial susceptibilities, 1996 to 2013. Eurosurveillance 2014;19:1–10.CrossRefGoogle Scholar
  41. 41.
    Borde JP, Zange S, Antwerpen MH, Georgi E, von Buttlar H, Kern WV, et al. Five cases of vector-borne Francisella tularensis holarctica infections in south-western Germany and genetic diversity. Ticks Tick Borne Dis Neth. 2017;8:808–12.CrossRefGoogle Scholar
  42. 42.
    Dentan C, Pavese P, Pelloux I, Boisset S, Brion J-P, Stahl J-P, et al. Treatment of tularemia in pregnant woman. Fr Emerg Infect Dis U S. 2013;19:996–8.CrossRefGoogle Scholar
  43. 43.
    Maurin M, Pelloux I, Brion JP, Del Bano J-N, Picard A. Human tularemia in France, 2006–2010. Clin Infect Dis U S. 2011;53:e133-41.Google Scholar
  44. 44.
    Johansson A, Berglund L, Sjöstedt A, Tärnvik A. Ciprofloxacin for treatment of tularemia. Clin Infect Dis U S. 2001;33:267–8.CrossRefGoogle Scholar
  45. 45.
    Syrjala H, Schildt R, Raisainen S. In vitro susceptibility of Francisella tularensis to fluoroquinolones and treatment of tularemia with norfloxacin and ciprofloxacin. Eur J Clin Microbiol Infect Dis Ger. 1991;10:68–70.CrossRefGoogle Scholar
  46. 46.
    Bloch-Infanger C, Furrer K, Wiese M, Hiebinger A, Bucher CM, Kopp S, et al. An unexpected cause for cavitary pneumonia and empyema. Infect Ger. 2016;44:539–41.CrossRefGoogle Scholar
  47. 47.
    Celebi G, Baruonu F, Ayoglu F, Cinar F, Karadenizli A, Ugur MB, et al. Tularemia, a reemerging disease in northwest Turkey: epidemiological investigation and evaluation of treatment responses. Jpn J Infect Dis Jpn. 2006;59:229–34.Google Scholar
  48. 48.
    Passiouk N, Heininger U. Ulceroglandular tularemia following contact with a boar. Pediatr Infect Dis J U S. 2016;35:453–5.CrossRefGoogle Scholar
  49. 49.
    Franco Hidalgo S, Prieto de Paula JM, Balaguer Zubieta I, Alvarez Ruiz AP. Infection due to Francisella tularensis, myocarditis and dilated myocardiopathy. Enferm Infecc Microbiol Clin. 2010;28:752–3.CrossRefGoogle Scholar
  50. 50.
    Amort J, Karrer U. Zwei Fallbeispiele zur Tularämie: eine typische und eine atypische Verlaufsform. BAG Bull. 2013;(49/13):896Google Scholar
  51. 51.
    Gore I, Saphir O. myocarditis a classification of 1402 cases. Am Heart J. 1947;34(6):827–30.CrossRefGoogle Scholar
  52. 52.
    Saphir O. Myocarditis A general review, with an analysis of two hundred an forty cases. Arch Pathol. 1941.  https://doi.org/10.1179/nhi.1988.24.1.227.Google Scholar
  53. 53.
    Saphir O. Isolated myocarditis. Am Heart J. 1942;24:167–81.CrossRefGoogle Scholar
  54. 54.
    Aaagard GN. Involvement of the heart in tularemia. Minn Med. 1944;27:115–21Google Scholar
  55. 55.
    Miller J. Granulomatous myocarditis. A case for diagnosis. Can Med Assoc J. 1933;29:134–7.Google Scholar
  56. 56.
    Ilback NG, Friman G, Beisel WR, Johnson AJ. Sequential metabolic alterations in the myocardium during influenza and tularemia in mice. Infect Immun. 1984;45:491–7.Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Infectious Diseases and Hospital EpidemiologyCantonal Hospital St. GallenSt. GallenSwitzerland
  2. 2.Division of General Internal MedicineCantonal Hospital St. GallenSt. GallenSwitzerland
  3. 3.Center of Laboratory Medicine (ZLM)St. GallenSwitzerland
  4. 4.Division of CardiologyCantonal Hospital St. GallenSt. GallenSwitzerland
  5. 5.Division of Radiology and Nuclear MedicineCantonal Hospital St. GallenSt. GallenSwitzerland

Personalised recommendations