Volume 78, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645


Specific polymerase chain reaction (PCR) protocols were used to determine the prevalence of toxigenic in Vhembe, South Africa. Of 322 stool samples collected, toxigenic was found in 23 (7.1%) cases and was significantly associated with diarrhea 20 (11.4%) compared with 3 (2%) in non-diarrheal samples (χ = 426, = 0.001), intestinal inflammation in 18 (12.1%) compared with 5 (2.9%) in lactoferrin-negative samples (χ = 10.194, = 0.001), and occult blood in 19 (16%) compared with 4 (2%) in occult blood–negative samples (χ = 22.157, < 0.001). Toxigenic was more common among individuals > 50 years of age (20%), followed by those between 30 and 39 years of age (19%) and was not associated with HIV infections (χ = 0.289, = 0.591). Co-infection with other pathogens was common. Multivariate analysis indicated that toxigenic was associated with ( = 0.028), ( = 0.007), and Enteroaggregative (EAEC) ( = 0.007) in diarrheal samples. This study confirms the usefulness of PCR methodologies in the detection of toxigenic and suggests that is responsible for a small, but underappreciated, proportion of diarrheal cases in the region, and further study is warranted in this area.


Article metrics loading...

The graphs shown below represent data from March 2017
Loading full text...

Full text loading...



  1. Cleary RK, 1998. Clostridium difficile-associated diarrhea and colitis: clinical manifestations, diagnosis, and treatment. Dis Colon Rectum 41 : 1435–1449. [Google Scholar]
  2. Wilcox MH, 1996. Cleaning up Clostridium difficile infection. Lancet 348 : 767–768. [Google Scholar]
  3. Surawicz CM, McFarland LV, 1999. Pseudomembranous colitis: causes and cures. Digestion 60 : 91–100. [Google Scholar]
  4. Karlström O, Fryklund B, Tullus K, Burman LG, 1998. A prospective nationwide study of Clostridium difficile-associated diarrhea in Sweden. The Swedish C. difficile Study Group. Clin Infect Dis 26 : 141–145. [Google Scholar]
  5. Kuijper EJ, Coignard B, Tull P, the ESCMID Study Group for Clostridium difficile (ESGCD)*, EU Member States and the European Centre for Disease Prevention and Control (ECDC), 2006. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 6 : 2–18. [Google Scholar]
  6. Reichardt C, Chaberny IF, Kola A, Mattner F, Vonberg RP, Gastmeier P, 2007. Dramatic increase of diarrhea associated with Clostridium difficile in Germany: has the new strain PCR-ribotype 027 reached us? Dtsch Med Wochenschr 132 : 223–228. [Google Scholar]
  7. Lyerly DM, Lockwood DE, Richardson SH, Wilkins TD, 1982. Biological activities of toxins A and B of Clostridium difficile. Infect Immun 35 : 1147–1150. [Google Scholar]
  8. Borriello SP, 1998. Pathogenesis of Clostridium difficile infection. J Antimicrob Chemother 41 : 13–19. [Google Scholar]
  9. Riegler M, Sedivy R, Pothoulakis C, Hamilton G, Zacherl J, Bischof G, Cosentini E, Feil W, Schiessel R, LaMont JT, Wenzl E, 1995. Clostridium difficile toxin B is more potent than toxin A in damaging human colonic epithelium in vitro. J Clin Invest 95 : 2004–2011. [Google Scholar]
  10. Barbut F, Decre D, Lalande V, Burghoffer B, Noussair L, Gigandon A, Espinasse F, Raskine L, Robert J, Mangeol A, Branger C, Petit JC, 2005. Clinical features of Clostridium difficile-associated diarrhea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J Med Microbiol 54 : 181–185. [Google Scholar]
  11. Johnson S, Kent SA, O’Leary KJ, Merrigan MM, Sambol SP, Peterson LR, Gerding DN, 2001. Fatal pseudomembranous colitis associated with a variant Clostridium difficile strain not detected by toxin A immunoassay. Ann Intern Med 135 : 434–438. [Google Scholar]
  12. Moncrief JS, Zheng L, Neville LM, Lyerly DM, 2000. Genetic characterization of toxin A-negative, toxin B-positive Clostridium difficile isolates by PCR. J Clin Microbiol 38 : 3072–3075. [Google Scholar]
  13. Spigaglia P, Mastrantonio P, 2002. Molecular analysis of the pathogenicity locus and polymorphism in the putative negative regulator of toxin production (TcdC) among Clostridium difficile clinical isolates. J Clin Microbiol 40 : 3470–3475. [Google Scholar]
  14. Geric B, Carman RJ, Rupnik M, Genheimer CW, Sambol SP, Lyerly DM, Gerding DN, Johnson S, 2006. Binary toxin-producing, large clostridial toxin-negative Clostridium difficile strains are enterotoxic but do not cause disease in hamsters. J Infect Dis 193 : 1143–1150. [Google Scholar]
  15. Poilane I, Karjalainen T, Barc MC, Bourlioux P, Collignon A, 1998. Protease activity of Clostridium difficile strains. Can J Microbiol 44 : 157–161. [Google Scholar]
  16. Eveillard M, Fourel V, Barc MC, Kerneis S, Coconnier MH, Karjalainen T, Bourlioux P, Servin AL, 1993. Identification and characterization of adhesive factors of Clostridium difficile involved in adhesion to human colonic enterocyte-like Caco-2 and mucus-secreting HT 29 cells in culture. Mol Microbiol 7 : 371–381. [Google Scholar]
  17. Karjalainen T, Barc MC, Collignon A, Trolle S, Boureau H, Cotte-Laffitte J, Bourlioux P, 1994. Cloning of a genetic determinant from Clostridium difficile involved in adherence to tissue culture cells and mucus. Infect Immun 62 : 4347–4355. [Google Scholar]
  18. Bartlett JG, 2006. Narrative review: the new epidemic of Clostridium difficile-associated enteric disease. Ann Intern Med 145 : 758–764. [Google Scholar]
  19. Johal SS, Hammond J, Solomon K, James PD, Mahida YR, 2004. Clostridium difficile associated diarrhea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut 53 : 673–677. [Google Scholar]
  20. Rupnik M, Avesani V, Janc M, von Eichel-Streiber C, Delmee M, 1998. A novel toxinotyping scheme and correlation of toxino-types with serogroups of Clostridium difficile isolates. J Clin Microbiol 36 : 2240–2247. [Google Scholar]
  21. Rahmati A, Gal M, Northey G, Brazier JS, 2005. Subtyping of Clostridium difficile polymerase chain reaction (PCR) ribotype 001 by repetitive extragenic palindromic PCR genomic fingerprinting. J Hosp Infect 60 : 56–60. [Google Scholar]
  22. Silletti RP, Lee G, Ailey E, 1996. Role of stool screening tests in diagnosis of inflammatory bacterial enteritis and in selection of specimens likely to yield invasive enteric pathogens. J Clin Microbiol 34 : 1161–1165. [Google Scholar]
  23. Ruiz-Pelaez JG, Mattar S, 1999. Accuracy of fecal lactoferrin and other stool tests for diagnosis of invasive diarrhea at a Colombian pediatric hospital. Pediatr Infect Dis J 18 : 342–346. [Google Scholar]
  24. Vaishnavi C, Thapa BR, Thennarasu K, Singh K, 2002. Faecal lactoferrin assay as an adjunct to Clostridium difficile diarrhea. Indian J Pathol Microbiol 45 : 69–73. [Google Scholar]
  25. Samie A, Obi CL, Barrett LJ, Powell SM, Guerrant RL, 2006. Prevalence of Campylobacter species, Helicobacter pylori and Arcobacter species in stool samples from the Venda region, Limpopo, South Africa: studies using molecular diagnostic methods. J Infect 54 : 558–566. [Google Scholar]
  26. Lemee L, Dhalluin A, Testelin S, Mattrat MA, Maillard K, Lemeland JF, Pons JL, 2004. Multiplex PCR targeting tpi (triose phosphate isomerase), tcdA (Toxin A), and tcdB (Toxin B) genes for toxigenic culture of Clostridium difficile. J Clin Microbiol 42 : 5710–5714. [Google Scholar]
  27. Terhes G, Urbán E, Sóki J, Hamid KA, Nagy E, 2004. Community-acquired Clostridium difficile caused by binary toxin, toxin A, toxin B gene-positive isolates in Hungary. J Clin Microbiol 42 : 4316–4318. [Google Scholar]
  28. Cohen SH, Tang YJ, Silva J Jr, 2000. Analysis of the pathogenicity locus in Clostridium difficile strains. J Infect Dis 181 : 659–663. [Google Scholar]
  29. Stubbs S, Rupnik M, Gibert M, Brazier J, Duerden B, Popoff M, 2000. Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 186 : 307–312. [Google Scholar]
  30. Nataro JP, Mai V, Johnson J, Blackwelder WC, Heimer R, Tirrell S, Edberg SC, Braden CR, Glenn Morris J Jr, Hirshon JM, 2006. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis 43 : 402–407. [Google Scholar]
  31. Kyne L, Merry C, O’Connell B, Keane C, O’Neill D, 1998. Community-acquired Clostridium difficile infection. J Infect 36 : 287–288. [Google Scholar]
  32. Johal SS, Hammond J, Solomon K, James PD, Mahida YR, 2004. Clostridium difficile associated diarrhoea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut 53 : 673–677. [Google Scholar]
  33. Raveh D, Rabinowitz B, Breuer GS, Rudensky B, Yinnon AM, 2006. Risk factors for Clostridium difficile toxin-positive nosocomial diarrhea. Int J Antimicrob Agents 28 : 231–237. [Google Scholar]
  34. Pulvirenti JJ, Mehra T, Hafiz I, DeMarais P, Marsh D, Kocka F, Meyer PM, Fischer SA, Goodman L, Gerding DN, Weinstein RA, 2002. Epidemiology and outcome of Clostridium difficile infection and diarrhea in HIV infected inpatients. Diagn Microbiol Infect Dis 44 : 325–330. [Google Scholar]
  35. Hutin Y, Molina JM, Casin I, Daix V, Sednaoui P, Welker Y, Lagrange P, Decazes JM, Modai J, 1993. Risk factors for Clostridium difficile-associated diarrhea in HIV-infected patients. AIDS 7 : 1441–1447. [Google Scholar]
  36. Colarian J, 1988. Clostridium difficile colitis following antiviral therapy in the acquired immunodeficiency syndrome. Am J Med 84 : 1081. [Google Scholar]
  37. McDonald LC, Coignard B, Dubberke E, Song X, Horan T, Kutty PK, Ad Hoc Clostridium difficile Surveillance Working Group, 2007. Recommendations for surveillance of Clostridium difficile-associated disease. Infect Control Hosp Epidemiol 28 : 140–145. [Google Scholar]
  38. Taha S, Johansson O, Rivera Jonsson S, Heimer D, Krovacek K, 2007. Toxin production by and adhesive properties of Clostridium difficile isolated from humans and horses with antibiotic-associated diarrhea. Comp Immunol Microbiol Infect Dis 30 : 163–174. [Google Scholar]
  39. Songer JG, Anderson MA, 2006. Clostridium difficile: an important pathogen of food animals. Anaerobe 12 : 1–4. [Google Scholar]
  40. Arroyo LG, Staempfli H, Weese JS, 2007. Molecular analysis of Clostridium difficile isolates recovered from horses with diarrhea. Vet Microbiol 120 : 179–183. [Google Scholar]
  41. Rodriguez-Palacios A, Stampfli HR, Duffield T, Peregrine AS, Trotz-Williams LA, Arroyo LG, Brazier JS, Weese JS, 2006. Clostridium difficile PCR ribotypes in calves, Canada. Emerg Infect Dis 12 : 1730–1736. [Google Scholar]
  42. Simango C, 2006. Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Trans R Soc Trop Med Hyg 100 : 1146–1150. [Google Scholar]
  43. Wultanska D, Pituch H, Obuch-Woszczatynski P, Meisel-Mikolajczyk F, Luczak M, 2005. Profile of toxigenicity of Clostridium difficile strains isolated from paediatric patients with clinical diagnosis of antibiotic associated diarrhea (AAD). Med Dosw Mikrobiol 57 : 377–382. [Google Scholar]
  44. Pituch H, Obuch-Woszczatynski P, Luczak M, Meisel-Mikolajczyk F, 2003. Clostridium difficile and enterotoxigenic Bacteroides fragilis strains isolated from patients with antibiotic associated diarrhea. Anaerobe 9 : 161–163. [Google Scholar]
  45. Price MF, Dao-Tran T, Garey KW, Graham G, Gentry LO, Dhungana L, DuPont HL, 2007. Epidemiology and incidence of Clostridium difficile-associated diarrhea diagnosed upon admission to a university hospital. J Hosp Infect 65 : 42–46. [Google Scholar]
  46. Kazakova SV, Ware K, Baughman B, Bilukha O, Paradis A, Sears S, Thompson A, Jensen B, Wiggs L, Bessette J, Martin J, Clukey J, Gensheimer K, Killgore G, McDonald LC, 2006. A hospital outbreak of diarrhea due to an emerging epidemic strain of Clostridium difficile. Arch Intern Med 166 : 2518–2524. [Google Scholar]
  47. Curry SR, Marsh JW, Muto CA, O’Leary MM, Pasculle AW, Harrison LH, 2007. tcdC genotypes associated with severe TcdC truncation in an epidemic clone and other strains of Clostridium difficile. J Clin Microbiol 45 : 215–221. [Google Scholar]
  48. Rexach CE, Tang-Feldman YJ, Cantrell MC, Cohen SH, 2006. Epidemiologic surveillance of Clostridium difficile diarrhea in a freestanding pediatric hospital and a pediatric hospital at a university medical center. Diagn Microbiol Infect Dis 56 : 109–114. [Google Scholar]

Data & Media loading...

  • Received : 06 Aug 2007
  • Accepted : 03 Jan 2008

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error