A clinical and epidemiological review of non-toxigenic clostridium difficile

Anaerobe

Volumn 22, Issue , 2013, Pages 1-5

  Natarajan, Mukil ^a   Walk, Seth T ^a,b   Young, Vincent B ^a   Aronoff, David M ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

Clostridium difficile; Hamsters; Humans; Non toxigenic Clostridium difficile; NTCD; Probiotic

Indexed keywords

CEFTRIAXONE; CLINDAMYCIN; CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; PROBIOTIC AGENT; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL COLONIZATION; BACTERIUM CARRIER; BACTERIUM CULTURE; BACTERIUM ISOLATE; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; DISEASE MODEL; ENZYME IMMUNOASSAY; FECES ANALYSIS; HAMSTER; HUMAN; NON TOXICOGENIC CLOSTRIDIUM DIFFICILE; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); POLYMERASE CHAIN REACTION; PREVALENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RISK REDUCTION; STRAIN DIFFERENCE; SURVIVAL RATE; SYSTEMATIC REVIEW; TOXIN SYNTHESIS;

CLOSTRIDIUM DIFFICILE; HAMSTERS; HUMANS; NON-TOXIGENIC CLOSTRIDIUM DIFFICILE; NTCD; PROBIOTIC;

ANIMALS; BACTERIAL TOXINS; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; CRICETINAE; CROSS INFECTION; DIARRHEA; DISEASE MODELS, ANIMAL; ENTEROTOXINS; HUMANS; PROTECTIVE AGENTS; SPECIES SPECIFICITY;

ANIMALIA; CLOSTRIDIUM DIFFICILE; CRICETINAE;

EID: 84880755047     PISSN: 10759964     EISSN: 10958274     Source Type: Journal    
DOI: 10.1016/j.anaerobe.2013.05.005     Document Type: Review

References (49)

1. Larson H.E., Price A.B. Pseudomembranous colitis: presence of clostridial toxin. Lancet 1977, 2:1312-1314.
2. Rifkin G.D., Fekety F.R., Silva J., Sack R.B. Antibiotic-induced colitis implication of a toxin neutralised by Clostridium sordellii antitoxin. Lancet 1977, 2:1103-1106.
3. George R.H., Symonds J.M., Dimock F., Brown J.D., Arabi Y., Shinagawa N., et al. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J 1978, 1:695.
4. Bartlett J.G., Onderdonk A.B., Cisneros R.L., Kasper D.L. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. JInfect Dis 1977, 136:701-705.
5. Bartlett J.G. Commentary on "Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters". JInfect Dis 2004, 190:202-209.
6. Shuttleworth R., Taylor M., Jones D.M. Antimicrobial susceptibilities of Clostridium difficile. JClin Pathol 1980, 33:1002-1005.
7. Kuehne S.A., Cartman S.T., Heap J.T., Kelly M.L., Cockayne A., Minton N.P. The role of toxin A and toxin B in Clostridium difficile infection. Nature 2010, 467:711-713.
8. Kuehne S.A., Cartman S.T., Minton N.P. Both, toxin A and toxin B, are important in Clostridium difficile infection. Gut Microbes 2011, 2:252-255.
9. Lyras D., O'Connor J.R., Howarth P.M., Sambol S.P., Carter G.P., Phumoonna T., et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009, 458:1176-1179.
10. Drudy D., Fanning S., Kyne L. Toxin A-negative, toxin B-positive Clostridium difficile. Int J Infect Dis 2007, 11:5-10.
11. Brouwer M.S., Allan E., Mullany P., Roberts A.P. Draft genome sequence of the nontoxigenic Clostridium difficile strain CD37. JBacteriol 2012, 194:2125-2126.
12. Cohen S.H., Tang Y.J., Silva J. Analysis of the pathogenicity locus in Clostridium difficile strains. JInfect Dis 2000, 181:659-663.
13. Fluit A.C., Wolfhagen M.J., Verdonk G.P., Jansze M., Torensma R., Verhoef J. Nontoxigenic strains of Clostridium difficile lack the genes for both toxin A and toxin B. JClin Microbiol 1991, 29:2666-2667.
14. Wren B.W., Heard S.R., al-Saleh A.I., Tabaqchali S. Characterisation of Clostridium difficile strains by polymerase chain reaction with toxin A- and B-specific primers. JMed Microbiol 1993, 38:109-113.
15. Mathis J.N., Pilkinton L., McMillin D.E. Detection and transcription of toxin DNA in a nontoxigenic strain of Clostridium difficile. Curr Microbiol 1999, 38:324-328.
16. Rupnik M., Brazier J.S., Duerden B.I., Grabnar M., Stubbs S.L. Comparison of toxinotyping and PCR ribotyping of Clostridium difficile strains and description of novel toxinotypes. Microbiology 2001, 147:439-447.
17. Corthier G., Muller M.C. Emergence in gnotobiotic mice of nontoxinogenic clones of Clostridium difficile from a toxinogenic one. Infect Immun 1988, 56:1500-1504.
18. Miyajima F., Roberts P., Swale A., Price V., Jones M., Horan M., et al. Characterisation and carriage ratio of Clostridium difficile strains isolated from a community-dwelling elderly population in the United Kingdom. PLoS One 2011, 6:e22804.
19. Kato H., Kita H., Karasawa T., Maegawa T., Koino Y., Takakuwa H., et al. Colonisation and transmission of Clostridium difficile in healthy individuals examined by PCR ribotyping and pulsed-field gel electrophoresis. JMed Microbiol 2001, 50:720-727.
20. Shim J.K., Johnson S., Samore M.H., Bliss D.Z., Gerding D.N. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 1998, 351:633-636.
21. Boone J.H., Goodykoontz M., Rhodes S.J., Price K., Smith J., Gearhart K.N., et al. Clostridium difficile prevalence rates in a large healthcare system stratified according to patient population, age, gender, and specimen consistency. Eur J Clin Microbiol Infect Dis 2012, 31:1551-1559.
22. Kato H., Kato N., Watanabe K., Ueno K., Ushijima H., Hashira S., et al. Application of typing by pulsed-field gel electrophoresis to the study of Clostridium difficile in a neonatal intensive care unit. JClin Microbiol 1994, 32:2067-2070.
23. Rousseau C., Poilane I., De Pontual L., Maherault A.C., Le Monnier A., Collignon A. Clostridium difficile carriage in healthy infants in the community: a potential reservoir for pathogenic strains. Clin Infect Dis 2012, 55:1209-1215.
24. Rousseau C., Levenez F., Fouqueray C., Dore J., Collignon A., Lepage P. Clostridium difficile colonization in early infancy is accompanied by changes in intestinal microbiota composition. JClin Microbiol 2011, 49:858-865.
25. Koene M.G., Mevius D., Wagenaar J.A., Harmanus C., Hensgens M.P., Meetsma A.M., et al. Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin Microbiol Infect 2012, 18:778-784.
26. Clooten J., Kruth S., Arroyo L., Weese J.S. Prevalence and risk factors for Clostridium difficile colonization in dogs and cats hospitalized in an intensive care unit. Vet Microbiol 2008, 129:209-214.
27. Struble A.L., Tang Y.J., Kass P.H., Gumerlock P.H., Madewell B.R., Silva J. Fecal shedding of Clostridium difficile in dogs: a period prevalence survey in a veterinary medical teaching hospital. JVet Diagn Invest 1994, 6:342-347.
28. Janezic S., Ocepek M., Zidaric V., Rupnik M. Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiol 2012, 12:48.
29. Cohen S.H., Tang Y.J., Muenzer J., Gumerlock P.H., Silva J. Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward. Clin Infect Dis 1997, 24:889-893.
30. Delmee M., Verellen G., Avesani V., Francois G. Clostridium difficile in neonates: serogrouping and epidemiology. Eur J Pediatr 1988, 147:36-40.
31. Pron B., Merckx J., Touzet P., Ferroni A., Poyart C., Berche P., et al. Chronic septic arthritis and osteomyelitis in a prosthetic knee joint due to Clostridium difficile. Eur J Clin Microbiol Infect Dis 1995, 14:599-601.
32. Gravisse J., Barnaud G., Hanau-Bercot B., Raskine L., Riahi J., Gaillard J.L., et al. Clostridium difficile brain empyema after prolonged intestinal carriage. JClin Microbiol 2003, 41:509-511.
33. Martirosian G., Szczesny A., Cohen S.H., Silva J. Isolation of non-toxigenic strains of Clostridium difficile from cases of diarrhea among patients hospitalized in hematology/oncology ward. Pol J Microbiol 2004, 53:197-200.
34. Behroozian A.A., Chludzinski J.P., Lo E.S., Ewing S.A., Waslawski S., Newton D.W., et al. Detection of mixed populations of Clostridium difficile from symptomatic patients using capillary-based PCR ribotyping. Infect Control Hosp Epidemiol 2013, in press.
35. Wilson K.H., Sheagren J.N. Antagonism of toxigenic Clostridium difficile by nontoxigenic C.difficile. JInfect Dis 1983, 147:733-736.
36. Borriello S.P., Barclay F.E. Protection of hamsters against Clostridium difficile ileocaecitis by prior colonisation with non-pathogenic strains. JMed Microbiol 1985, 19:339-350.
37. Sambol S.P., Merrigan M.M., Tang J.K., Johnson S., Gerding D.N. Colonization for the prevention of Clostridium difficile disease in hamsters. JInfect Dis 2002, 186:1781-1789.
38. Merrigan M.M., Sambol S.P., Johnson S., Gerding D.N. Prevention of fatal Clostridium difficile-associated disease during continuous administration of clindamycin in hamsters. JInfect Dis 2003, 188:1922-1927.
39. Merrigan M.M., Sambol S.P., Johnson S., Gerding D.N. New approach to the management of Clostridium difficile infection: colonisation with non-toxigenic C. difficile during daily ampicillin or ceftriaxone administration. Int J Antimicrob Agents 2009, 33(Suppl. 1):S46-S50.
40. Songer J.G., Jones R., Anderson M.A., Barbara A.J., Post K.W., Trinh H.T. Prevention of porcine Clostridium difficile-associated disease by competitive exclusion with nontoxigenic organisms. Vet Microbiol 2007, 124:358-361.
41. Seal D., Borriello S.P., Barclay F., Welch A., Piper M., Bonnycastle M. Treatment of relapsing Clostridium difficile diarrhoea by administration of a non-toxigenic strain. Eur J Clin Microbiol 1987, 6:51-53.
42. Villano S.A., Seiberling M., Tatarowicz W., Monnot-Chase E., Gerding D.N. Evaluation of an oral suspension of VP20621, spores of nontoxigenic Clostridium difficile strain M3, in healthy subjects. Antimicrob Agents Chemother 2012, 56:5224-5229.
43. Villano S.A. Safety and efficacy study of VP20621 for prevention of recurrent Clostridium difficile infection 2010, Online at:, [last accessed: Sept 18, 2012]. http://clinicaltrials.gov/show/NCT01259726.
44. Geric B., Rupnik M., Gerding D.N., Grabnar M., Johnson S. Distribution of Clostridium difficile variant toxinotypes and strains with binary toxin genes among clinical isolates in an American hospital. JMed Microbiol 2004, 53:887-894.
45. Martirosian G., Szczesny A., Cohen S.H., Silva J. Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital. Diagn Microbiol Infect Dis 2005, 52:153-155.
46. Walk S.T., Micic D., Jain R., Lo E.S., Trivedi I., Liu E.W., et al. Clostridium difficile ribotype does not predict severe infection. Clin Infect Dis 2012, 55:1661-1668.
47. Ferreira C.E., Nakano V., Durigon E.L., Avila-Campos M.J. Prevalence of Clostridium spp. and Clostridium difficile in children with acute diarrhea in Sao Paulo city, Brazil. Mem Inst Oswaldo Cruz 2003, 98:451-454.
48. Collignon A., Ticchi L., Depitre C., Gaudelus J., Delmee M., Corthier G. Heterogeneity of Clostridium difficile isolates from infants. Eur J Pediatr 1993, 152:319-322.
49. Rousseau C., Lemee L., Le Monnier A., Poilane I., Pons J.L., Collignon A. Prevalence and diversity of Clostridium difficile strains in infants. JMed Microbiol 2011, 60:1112-1118.