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 28, Number 3—March 2022

Case–Control Study of Clostridium innocuum Infection, Taiwan

Yi-Ching Chen1, Yi-Chun Kuo1, Mi-Chi Chen, Young-Da Zhang, Chyi-Liang Chen, Puo-Hsien Le, and Cheng-Hsun ChiuComments to Author 
Author affiliations: Chang Gung University, Taoyuan, Taiwan (Y.-C. Chen, Y.-C. Kuo, C.-H. Chiu); Chang Gung Memorial Hospital, Taoyuan (Y.-C. Chen, M.-C. Chen, Y.-D. Zhang, C.-L. Chen, P.-H. Le, C.-H. Chiu)

Main Article

Table 4

Reported cases of extraintestinal Clostridium innocuum infection, 2000–2020, Taiwan*

Characteristic Castiglioni et al. (10) Crum-Cianflone et al. (29) Hung et al. (30) Mutoh et al. (31) Aroca-Ferri et al. (32)
Year and country
2003 United States
2009 United States
2014 Taiwan
2015 Japan
2019 Spain
Age, y/sex
Underlying conditions
Chronic HCV, interstitial nephritis after renal transplant
DM with CDAD and CMV colitis
Takayasu arteritis, ESRD under PD
Isolation site
Blood, BM
Peritoneal fluid
Vancomycin MIC
16 μg/mL
>32 μg/mL
8 μg/mL
8 μg/mL
Bacteremia secondary to infectious hematoma
Pelvic osteomyelitis complicated with iliac muscle abscess
PD peritonitis complicated with sigmoid colon perforation
11 days and surgery
2 weeks
8 weeks
15 days
Outcome Recovered Recovered Recovered Recovered Died

*ALL, acute lymphoblastic leukemia; AMP, ampicillin; BM, bone marrow; CDAD, C. difficile–associated diarrhea; CLI, clindamycin; CMV, cytomegalovirus; CTX, cefotaxime; DAP, daptomycin; ERY, erythromycin; ESRD, end stage renal disease; HCV, hepatitis C virus; IP, intraperitoneal route; IV, intravenous route; MIC, minimum inhibitory concentration; MTZ, metronidazole; NA, not available; PD, peritoneal dialysis; PO, oral route; TZP, piperacillin/tazobactam.

Main Article

  1. Smith  LD, King  E. Clostridium innocuum, sp. n., a sporeforming anaerobe isolated from human infections. J Bacteriol. 1962;83:9389. DOIPubMedGoogle Scholar
  2. Alexander  CJ, Citron  DM, Brazier  JS, Goldstein  EJ. Identification and antimicrobial resistance patterns of clinical isolates of Clostridium clostridioforme, Clostridium innocuum, and Clostridium ramosum compared with those of clinical isolates of Clostridium perfringens. J Clin Microbiol. 1995;33:320915. DOIPubMedGoogle Scholar
  3. Stokes  NA, Hylemon  PB. Characterization of delta 4-3-ketosteroid-5 beta-reductase and 3 beta-hydroxysteroid dehydrogenase in cell extracts of Clostridium innocuum. Biochim Biophys Acta. 1985;836:25561. DOIPubMedGoogle Scholar
  4. Carlier  JP, Sellier  N. Identification by gas chromatography-mass spectrometry of short-chain hydroxy acids produced by Fusobacterium species and Clostridium innocuum. J Chromatogr A. 1987;420:1218. DOIPubMedGoogle Scholar
  5. Johnston  NC, Goldfine  H, Fischer  W. Novel polar lipid composition of Clostridium innocuum as the basis for an assessment of its taxonomic status. Microbiology (Reading). 1994;140:10511. DOIPubMedGoogle Scholar
  6. Li  Y, Shan  M, Zhu  Z, Mao  X, Yan  M, Chen  Y, et al. Application of MALDI-TOF MS to rapid identification of anaerobic bacteria. BMC Infect Dis. 2019;19:941. DOIPubMedGoogle Scholar
  7. Cutrona  AF, Watanakunakorn  C, Schaub  CR, Jagetia  A. Clostridium innocuum endocarditis. Clin Infect Dis. 1995;21:13067. DOIPubMedGoogle Scholar
  8. Chia  JH, Wu  TS, Wu  TL, Chen  CL, Chuang  CH, Su  LH, et al. Clostridium innocuum is a vancomycin-resistant pathogen that may cause antibiotic-associated diarrhoea. Clin Microbiol Infect. 2018;24:11959. DOIPubMedGoogle Scholar
  9. Chia  JH, Feng  Y, Su  LH, Wu  TL, Chen  CL, Liang  YH, et al. Clostridium innocuum is a significant vancomycin-resistant pathogen for extraintestinal clostridial infection. Clin Microbiol Infect. 2017;23:5606. DOIPubMedGoogle Scholar
  10. Castiglioni  B, Gautam  A, Citron  DM, Pasculle  W, Goldstein  EJC, Strollo  D, et al. Clostridium innocuum bacteremia secondary to infected hematoma with gas formation in a kidney transplant recipient. Transpl Infect Dis. 2003;5:199202. DOIPubMedGoogle Scholar
  11. David  V, Bozdogan  B, Mainardi  JL, Legrand  R, Gutmann  L, Leclercq  R. Mechanism of intrinsic resistance to vancomycin in Clostridium innocuum NCIB 10674. J Bacteriol. 2004;186:341522. DOIPubMedGoogle Scholar
  12. Peng  Z, Ling  L, Stratton  CW, Li  C, Polage  CR, Wu  B, et al. Advances in the diagnosis and treatment of Clostridium difficile infections. Emerg Microbes Infect. 2018;7:15. DOIPubMedGoogle Scholar
  13. Jewkes  J, Larson  HE, Price  AB, Sanderson  PJ, Davies  HA. Aetiology of acute diarrhoea in adults. Gut. 1981;22:38892. DOIPubMedGoogle Scholar
  14. McDonald  LC, Gerding  DN, Johnson  S, Bakken  JS, Carroll  KC, Coffin  SE, et al. Clinical Practice Guidelines for Clostridium difficile Infection in Adults and Children: 2017 Update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis. 2018;66:98794. DOIPubMedGoogle Scholar
  15. Shannon  S, Kronemann  D, Patel  R, Schuetz  AN. Routine use of MALDI-TOF MS for anaerobic bacterial identification in clinical microbiology. Anaerobe. 2018;54:1916. DOIPubMedGoogle Scholar
  16. Veloo  AC, de Vries  ED, Jean-Pierre  H, Justesen  US, Morris  T, Urban  E, et al.; ENRIA workgroup. The optimization and validation of the Biotyper MALDI-TOF MS database for the identification of Gram-positive anaerobic cocci. Clin Microbiol Infect. 2016;22:7938. DOIPubMedGoogle Scholar
  17. Li  Y, Shan  M, Zhu  Z, Mao  X, Yan  M, Chen  Y, et al. Application of MALDI-TOF MS to rapid identification of anaerobic bacteria. BMC Infect Dis. 2019;19:941. DOIPubMedGoogle Scholar
  18. Khanna  S, Pardi  DS, Aronson  SL, Kammer  PP, Orenstein  R, St Sauver  JL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol. 2012;107:8995. DOIPubMedGoogle Scholar
  19. Charlson  ME, Pompei  P, Ales  KL, MacKenzie  CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:37383. DOIPubMedGoogle Scholar
  20. Pepin  J, Alary  ME, Valiquette  L, Raiche  E, Ruel  J, Fulop  K, et al. Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clin Infect Dis. 2005;40:15917. DOIPubMedGoogle Scholar
  21. Lee  HY, Hsiao  HL, Chia  CY, Cheng  CW, Tsai  TC, Deng  ST, et al. Risk factors and outcomes of Clostridium difficile infection in hospitalized patients. Biomed J. 2019;42:99106. DOIPubMedGoogle Scholar
  22. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing: 27th edition (M100–S27). Wayne (PA): The Institute; 2017.
  23. Van Daele  E, Van de Putte  D, Ceelen  W, Van Nieuwenhove  Y, Pattyn  P. Risk factors and consequences of anastomotic leakage after Ivor Lewis oesophagectomy. Interact Cardiovasc Thorac Surg. 2016;22:327. DOIPubMedGoogle Scholar
  24. Finegold  SM, Song  Y, Liu  C, Hecht  DW, Summanen  P, Könönen  E, et al. Clostridium clostridioforme: a mixture of three clinically important species. Eur J Clin Microbiol Infect Dis. 2005;24:31924. DOIPubMedGoogle Scholar
  25. Leal  J, Gregson  DB, Ross  T, Church  DL, Laupland  KB. Epidemiology of Clostridium species bacteremia in Calgary, Canada, 2000-2006. J Infect. 2008;57:198203. DOIPubMedGoogle Scholar
  26. Bodey  GP, Rodriguez  S, Fainstein  V, Elting  LS. Clostridial bacteremia in cancer patients. A 12-year experience. Cancer. 1991;67:192842. DOIPubMedGoogle Scholar
  27. Shah  M, Bishburg  E, Baran  DA, Chan  T. Epidemiology and outcomes of clostridial bacteremia at a tertiary-care institution. ScientificWorldJournal. 2009;9:1448. DOIPubMedGoogle Scholar
  28. Ha  CWY, Martin  A, Sepich-Poore  GD, Shi  B, Wang  Y, Gouin  K, et al. Translocation of viable gut microbiota to mesenteric adipose drives formation of creeping fat in humans. Cell. 2020;183:666683.e17. DOIPubMedGoogle Scholar
  29. Crum-Cianflone  N. Clostridium innocuum Bacteremia in a patient with acquired immunodeficiency syndrome. Am J Med Sci. 2009;337:4802. DOIPubMedGoogle Scholar
  30. Hung  YP, Lin  HJ, Wu  CJ, Chen  PL, Lee  JC, Liu  HC, et al. Vancomycin-resistant Clostridium innocuum bacteremia following oral vancomycin for Clostridium difficile infection. Anaerobe. 2014;30:246. DOIPubMedGoogle Scholar
  31. Mutoh  Y, Hirai  R, Tanimura  A, Matono  T, Morino  E, Kutsuna  S, et al. Osteomyelitis due to Clostridium innocuum in a patient with acute lymphoblastic leukemia: case report and literature review. Springerplus. 2015;4:385. DOIPubMedGoogle Scholar
  32. Aroca-Ferri  M, Suárez-Hormiga  L, Bosch-Benitez-Parodi  E, Bolaños-Rivero  M. Peritonitis by Clostridium innocuum associated to peritoneal dialysis [in Spanish]. Rev Esp Quimioter. 2019;32:1923.
  33. Morel  G, Mulier  G, Ghrenassia  E, Abdel Nabey  M, Tandjaoui  Y, Kouatchet  A, et al. Non–C. difficile Clostridioides bacteremia in intensive care patients, France. Emerg Infect Dis. 2021;27:18409. DOIPubMedGoogle Scholar
  34. Cherny  KE, Ozer  EA, Kochan  TJ, Johnson  S, Kociolek  LK. Complete genome sequence of Clostridium innocuum strain LC–LUMC-CI-001, isolated from a patient with recurrent antibiotic-associated diarrhea. Microbiol Resour Announc. 2020;9:e0036520. DOIPubMedGoogle Scholar
  35. Sánchez-Hurtado  K, Poxton  IR. Enhancement of the cytotoxic activity of Clostridium difficile toxin A by surface-associated antigens. J Med Microbiol. 2008;57:73944. DOIPubMedGoogle Scholar

Main Article

1These authors contributed equally to this article.

Page created: January 23, 2022
Page updated: February 21, 2022
Page reviewed: February 21, 2022
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.