Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 29, Number 6—June 2023
CME ACTIVITY - Synopsis

Case Studies and Literature Review of Francisella tularensis–Related Prosthetic Joint Infection

Léa Ponderand, Thomas Guimard, Estibaliz Lazaro, Henry Dupuy, Olivia Peuchant, Nathalie Roch, Philippe Deroche, Tristan Ferry, Max Maurin, Aurélie Hennebique, Sandrine Boisset, Isabelle Pelloux, and Yvan CasparComments to Author 
Author affiliations: Grenoble Alpes University Hospital Center, Grenoble, France (L. Ponderand, M. Maurin, A. Hennebique, S. Boisset, I. Pelloux, Y. Caspar); Univ. Grenoble Alpes, CNRS, CEA, IBS, Grenoble, France (L. Ponderand, S. Boisset, Y. Caspar); Departmental Hospital Center of Vendée, La Roche sur Yon, France (T. Guimard); University Hospital Center of Haut-Lévêque, Pessac, France (E. Lazaro, H. Dupuy); University Hospital Center of Bordeaux, Bordeaux, France (O. Peuchant); William Morey Hospital Center, Chalon-sur-Saône, France (N. Roch); Dracy-le-Fort Orthopedic Center, Dracy-le-Fort, France (P. Deroche); Claude Bernard University Lyon 1, CNRS ENS Lyon, INSERM, Lyon, France (T. Ferry); Croix-Rousse University Hospital Center, Hospices Civils de Lyon, Lyon (T. Ferry); Univ. Grenoble Alpes, CNRS, Grenoble INP, TIMC-IMAG, Grenoble (M. Maurin, A. Hennebique)

Main Article

Table 1

Clinical and biologic characteristics of patients with Francisella tularensis–related prosthetic joint infection*

Characteristic Case
1 2 3 4 (10) 5 (11) 6 (11) 7 (12) 8 (13)
Country France France France United States Switzerland Czech Republic United States Canada
Region
 Vendée
 Gironde
 Aube
 Colorado
 NS
 NS
 Illinois
 Ontario
Age, y
 49
 70
 68
 58
 84
 84
 77
 68
Sex
 M
 M
 M
 M
 F
 M
 M
 M
Exposure factors
 Rural residence, dog
 Hunter
 Retired butcher, cooking with wild game
 Farmer, possible rabbit carcass handling
 Airborne transmission (rabbit barn in neighbor’s house)
 Walk in tularemia- endemic area
 Hunter
 Hunter, tick bite 6 mo before surgery
Type of surgery
 Left THR
 Left TKA
 Left THR
 Left TKA
 Right knee prosthesis
 Right TKA
 Right THR
 Right TKA
Delay between diagnosis and prosthesis implantation
 35 d
 12 y
 19 y
 9 mo
 12 y
 8 y
 7 d
 6 mo
Clinical symptoms
 Infected scar, fever
 Feverish confusion, bilateral mediastinal and hilar lymphadenopathy, knee swelling
 Joint pain
 Repeated joint effusion
 Erythema, joint pain
 Fever, abdominal pain, confusion, painful knee effusion
 Fever, joint pain and swelling, bullous skin lesion with itching
 Joint pain, warm and swollen knee
CRP, mg/L
 21
 100
 58
 NA
 81
 98
 16
 NA
Leukocytes, G/L
 4.45
 4
 NA
 NA
 NA
 NA
 NA
 NA
Sample type
 Abscess
 Joint aspiration
 3 tissues
 Joint aspiration
 7 tissues
 Joint aspiration
 Joint aspiration
 Joint aspiration
No. positive samples/total
 1/1
 1/1
 2/3
 1/1
 6/7
 1/1
 1/1
 1/1
Delay to positivity
 NA
 7 d
 5 d
 24 h–48 h
 12 d
 4 d
 7 d
 3 d
Identification
 Vitek 2 GN Biochemical assay; ISFtu2 PCR +; specific F. tularensis subspeciesholarctica PCR
 Specific Francisella PCR; ISFtu2 PCR +; 16S-23S PCR + sequencing
 MALDI-TOF MS (Microflex LT); ISFtu2 PCR +; specific F. tularensis subspecies holarctica PCR
 Sequencing
 16S rRNA gene sequencing
 16 S rRNA gene sequencing
 MALDI-TOF MS
 Sequencing
Serologic results MAT 640; IFA IgG 1,280; IgM 640 ELISA IgG 1.5; IgM 3.58; IFA IgG 640; IgM 640 MAT 160 ND IgM 232.6 U/mL; IgG 126.4 U/mL MAT 80 Positive (titers NA) MAT 320

*CRP, C-reactive protein; IFA, immunofluorescence assay; MALDI-TOF MS, matrix-assisted laser desorption/ionization time-of-flight mass spectrometry; MAT, microagglutination test; Microflex LT, Bruker Daltonics; NA, not available; ND, not done; NS, not specified; THR, total hip replacement; TKA, total knee arthroplasty; +, positive.

Main Article

References
  1. Oyston  PCF, Sjostedt  A, Titball  RW. Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol. 2004;2:967–78. DOIPubMedGoogle Scholar
  2. Boisset  S, Caspar  Y, Sutera  V, Maurin  M. New therapeutic approaches for treatment of tularaemia: a review. Front Cell Infect Microbiol. 2014;4:40. DOIPubMedGoogle Scholar
  3. Maurin  M, Mersali  NF, Raoult  D. Bactericidal activities of antibiotics against intracellular Francisella tularensis. Antimicrob Agents Chemother. 2000;44:3428–31. DOIPubMedGoogle Scholar
  4. Hennebique  A, Boisset  S, Maurin  M. Tularemia as a waterborne disease: a review. Emerg Microbes Infect. 2019;8:1027–42. DOIPubMedGoogle Scholar
  5. Burckhardt  F, Hoffmann  D, Jahn  K, Heuner  K, Jacob  D, Vogt  M, et al. Oropharyngeal tularemia from freshly pressed grape must. N Engl J Med. 2018;379:197–9. DOIPubMedGoogle Scholar
  6. Eren Gok  S, Kocagul Celikbas  A, Baykam  N, Atay Buyukdemirci  A, Eroglu  MN, Evren Kemer  O, et al. Evaluation of tularemia cases focusing on the oculoglandular form. J Infect Dev Ctries. 2014;8:1277–84. DOIPubMedGoogle Scholar
  7. Maurin  M, Gyuranecz  M. Tularaemia: clinical aspects in Europe. Lancet Infect Dis. 2016;16:113–24. DOIPubMedGoogle Scholar
  8. Petersen  JM, Molins  CR. Subpopulations of Francisella tularensis ssp. tularensis and holarctica: identification and associated epidemiology. Future Microbiol. 2010;5:649–61. DOIPubMedGoogle Scholar
  9. Mailles  A, Vaillant  V. 10 years of surveillance of human tularaemia in France. Euro Surveill. 2014;19:20956. DOIPubMedGoogle Scholar
  10. Azua  EN, Voss  LA. Tularemia in a prosthetic joint infection. Orthopedics. 2020;43:e54–6. DOIPubMedGoogle Scholar
  11. Chrdle  A, Trnka  T, Musil  D, Fucentese  SF, Bode  P, Keller  PM, et al. Francisella tularensis periprosthetic joint infections diagnosed with growth in cultures. J Clin Microbiol. 2019;57:e00339–19. DOIPubMedGoogle Scholar
  12. Rawal  H, Patel  A, Moran  M. Unusual case of prosthetic joint infection caused by Francisella tularensis. BMJ Case Rep. 2017;2017:2017.
  13. Cooper  CL, Van Caeseele  P, Canvin  J, Nicolle  LE. Chronic prosthetic device infection with Francisella tularensis. Clin Infect Dis. 1999;29:1589–91. DOIPubMedGoogle Scholar
  14. French Infectious Diseases Society (SPILF). Clinical recommendations for prosthetic joint infection by the Société de pathologie infectieuse de langue française [in French] [cited 2021 Jan 12]. https://www.infectiologie.com/fr/recommandations.html
  15. Beam  E, Osmon  D. Prosthetic joint infection update. Infect Dis Clin North Am. 2018;32:843–59. DOIPubMedGoogle Scholar
  16. Maurin  M, Pelloux  I, Brion  JP, Del Banõ  JN, Picard  A. Human tularemia in France, 2006-2010. Clin Infect Dis. 2011;53:e133–41. DOIPubMedGoogle Scholar
  17. World Health Organization. WHO guidelines on tularaemia. Geneva: The Organization: 2007 [cited 2020 Apr 7]. https://apps.who.int/iris/handle/10665/43793
  18. Kugeler  KJ, Pappert  R, Zhou  Y, Petersen  JM. Real-time PCR for Francisella tularensis types A and B. Emerg Infect Dis. 2006;12:1799–801. DOIPubMedGoogle Scholar
  19. Caspar  Y, Maurin  M. Francisella tularensis susceptibility to antibiotics: a comprehensive review of the data obtained In vitro and in animal models. Front Cell Infect Microbiol. 2017;7:122. DOIPubMedGoogle Scholar
  20. Brunet  CD, Hennebique  A, Peyroux  J, Pelloux  I, Caspar  Y, Maurin  M. Presence of Francisella tularensis subsp. holarctica DNA in the Aquatic Environment in France. Microorganisms. 2021;9:1398. DOIPubMedGoogle Scholar
  21. 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. 2018;73:687–91. DOIPubMedGoogle Scholar
  22. Ferguson  RJ, Palmer  AJ, Taylor  A, Porter  ML, Malchau  H, Glyn-Jones  S. Hip replacement. Lancet. 2018;392:1662–71. DOIPubMedGoogle Scholar
  23. Price  AJ, Alvand  A, Troelsen  A, Katz  JN, Hooper  G, Gray  A, et al. Knee replacement. Lancet. 2018;392:1672–82. DOIPubMedGoogle Scholar
  24. Kapadia  BH, Berg  RA, Daley  JA, Fritz  J, Bhave  A, Mont  MA. Periprosthetic joint infection. Lancet. 2016;387:386–94. DOIPubMedGoogle Scholar
  25. Allegranzi  B, Zayed  B, Bischoff  P, Kubilay  NZ, de Jonge  S, de Vries  F, et al.; WHO Guidelines Development Group. New WHO recommendations on intraoperative and postoperative measures for surgical site infection prevention: an evidence-based global perspective. Lancet Infect Dis. 2016;16:e288–303. DOIPubMedGoogle Scholar
  26. Berríos-Torres  SI, Umscheid  CA, Bratzler  DW, Leas  B, Stone  EC, Kelz  RR, et al.; Healthcare Infection Control Practices Advisory Committee. Centers for Disease Control and Prevention guideline for the prevention of surgical site infection, 2017. JAMA Surg. 2017;152:784–91. DOIPubMedGoogle Scholar
  27. Tande  AJ, Patel  R. Prosthetic joint infection. Clin Microbiol Rev. 2014;27:302–45. DOIPubMedGoogle Scholar
  28. Zimmerli  W, Trampuz  A, Ochsner  PE. Prosthetic-joint infections. N Engl J Med. 2004;351:1645–54. DOIPubMedGoogle Scholar
  29. Debarge  R, Nicolle  MC, Pinaroli  A, Ait Si Selmi  T, Neyret  P. [Surgical site infection after total knee arthroplasty: a monocenter analysis of 923 first-intention implantations] [in French]. Rev Chir Orthop Repar Appar Mot. 2007;93:582–7. DOIPubMedGoogle Scholar
  30. Million  M, Bellevegue  L, Labussiere  AS, Dekel  M, Ferry  T, Deroche  P, et al. Culture-negative prosthetic joint arthritis related to Coxiella burnetii. Am J Med. 2014;127:786.e7–10. DOIPubMedGoogle Scholar
  31. van Hoek  ML. Biofilms: an advancement in our understanding of Francisella species. Virulence. 2013;4:833–46. DOIPubMedGoogle Scholar
  32. Centers for Disease Control and Prevention, American Society for Microbiology, Association of Public Health Laboratories. Basic protocols for Level A laboratories for the presumptive identification of Francisella tularensis [cited 2021 Jan 12]. https://www.epa.gov/sites/production/files/2015-07/documents/cdc-ftularemia.pdf
  33. Ellis  J, Oyston  PCF, Green  M, Titball  RW. Tularemia. Clin Microbiol Rev. 2002;15:631–46. DOIPubMedGoogle Scholar
  34. Petersen  JM, Schriefer  ME, Gage  KL, Montenieri  JA, Carter  LG, Stanley  M, et al. Methods for enhanced culture recovery of Francisella tularensis. Appl Environ Microbiol. 2004;70:3733–5. DOIPubMedGoogle Scholar
  35. Karatuna  O, Celebi  B, Can  S, Akyar  I, Kilic  S. 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;16:132–8.PubMedGoogle Scholar
  36. López-Ramos  I, Hernández  M, Rodríguez-Lázaro  D, Gutiérrez  MP, Zarzosa  P, Orduña  A, et al. Quick identification and epidemiological characterization of Francisella tularensis by MALDI-TOF mass spectrometry. J Microbiol Methods. 2020;177:106055. DOIPubMedGoogle Scholar
  37. Regoui  S, Hennebique  A, Girard  T, Boisset  S, Caspar  Y, Maurin  M. Optimized MALDI TOF mass spectrometry identification of Francisella tularensis Subsp. holarctica. Microorganisms. 2020;8:1143. DOIPubMedGoogle Scholar
  38. Forsman  M, Sandström  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 Bacteriol. 1994;44:38–46. DOIPubMedGoogle Scholar
  39. Versage  JL, Severin  DDM, Chu  MC, Petersen  JM. Development of a multitarget real-time TaqMan PCR assay for enhanced detection of Francisella tularensis in complex specimens. J Clin Microbiol. 2003;41:5492–9. DOIPubMedGoogle Scholar
  40. Johansson  A, Farlow  J, Larsson  P, Dukerich  M, Chambers  E, Byström  M, et al. Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol. 2004;186:5808–18. DOIPubMedGoogle Scholar
  41. Osmon  DR, Berbari  EF, Berendt  AR, Lew  D, Zimmerli  W, Steckelberg  JM, et al.; Infectious Diseases Society of America. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis. 2013;56:e1–25. DOIPubMedGoogle Scholar
  42. Tande  AJ, Gomez-Urena  EO, Berbari  EF, Osmon  DR. Management of prosthetic joint infection. Infect Dis Clin North Am. 2017;31:237–52. DOIPubMedGoogle Scholar
  43. Hepburn  MJ, Simpson  AJH. Tularemia: current diagnosis and treatment options. Expert Rev Anti Infect Ther. 2008;6:231–40. DOIPubMedGoogle Scholar
  44. Bossi  P, Tegnell  A, Baka  A, van Loock  F, Werner  A, Hendriks  J, et al. Bichat guidelines for the clinical management of tularaemia and bioterrorism-related tularaemia. Euro Surveill. 2004;9:27–8. DOIPubMedGoogle Scholar
  45. Thabit  AK, Fatani  DF, Bamakhrama  MS, Barnawi  OA, Basudan  LO, Alhejaili  SF. Antibiotic penetration into bone and joints: An updated review. Int J Infect Dis. 2019;81:128–36. DOIPubMedGoogle Scholar

Main Article

Page created: March 29, 2023
Page updated: May 18, 2023
Page reviewed: May 18, 2023
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external