The potential of probiotic fermented milk products in reducing risk of antibiotic-associated diarrhoea and Clostridium difficile disease

International Journal of Dairy Technology

Volumn 62, Issue 4, 2009, Pages 461-471

  Lewis, Jonathan D N ^a   Thomas, Linda V ^a,b   Weir, William ^c  

^a UK   (United Kingdom)

^b Artemis   (United Kingdom)

^c WEST HERTFORDSHIRE HOSPITALS NHS TRUST   (United Kingdom)

Author keywords

Antibiotic associated diarrhoea; Clostridium difficile; Fermented milk products; Lactobacillus; Probiotic

Indexed keywords

CLOSTRIDIUM DIFFICILE; LACTOBACILLUS;

EID: 70350141567     PISSN: 1364727X     EISSN: 14710307     Source Type: Journal    
DOI: 10.1111/j.1471-0307.2009.00518.x     Document Type: Review

References (77)

1. Aggett P J, Antoine J-M, Asp N-G et al. (2005) PASSCLAIM: process for the assessment of scientific support for claims on foods, consensus on criteria. The European Journal of Nutrition 44 1 30.
2. Asha N J, Tompkins D Wilcox M H (2006) Comparative analysis of prevalence, risk factors, and molecular epidemiology of antibiotic-associated diarrhea due to Clostridium difficile, Clostridium perfringens, and Staphylococcus aureus. Journal of Clinical Microbiology 44 2785 2791.
3. Baker H Day B (2008) Probiotics: where are they going next? New and emerging areas of research. Nutrition Bulletin 33 359 363.
4. Bartlett J G, Chang T W, Gurwith M, Gorbach S L Onderdonk A B (1978) Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. The New England Journal of Medicine 298 531 534. (Pubitemid 8295586)
5. Beausoleil M, Fortier N, Guénette S, L'Ecuyer A, Savoie M, Franco M Lachaîne J (2007) Effect of a fermented milk combining Lactobacillus acidophilus CL1285 and Lactobacillus casei in the prevention of antibiotic-associated diarrhoea: a randomized, double-blind, placebo-controlled trial. Canadian Journal of Gastroenterology 21 732 736.
6. Borriello S P (1998) Pathogenesis of Clostridium difficile infection. The Journal of Antimicrobial Chemotherapy 41 (Suppl C) 13 19.
7. Brazier J S (2008) Clostridium difficile: from obscurity to superbug. British Journal of Biomedical Science 65 39 44.
8. Candy D C A, Heath S J, Lewis J D N Thomas L V (2008) Probiotics for the young and not so young. International Journal of Dairy Technology 61 215 221.
9. Canny G O McCormick B A (2008) Bacteria in the intestines, helpful residents or enemies from within. Infection and Immunity 76 3360 3373.
10. Cohendy M (1906a) Essais d'acclimatation microbienne dans la cavité intestinale. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 60 364 366.
11. Cohendy M (1906b) Description du ferment lactique puissant capable de s'acclimater dans l'intestine de l'homme. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 60 558 560.
12. Conway S, Hart A, Clark A Harvey I (2007) Does eating yogurt prevent antibiotic-associated diarrhoea? A placebo-controlled randomised trial in general practice. British Journal of General Practice 57 953 959.
13. Cunningham R Dial S (2008) Is over-use of proton pump inhibitors fuelling the current epidemic of Clostridium difficile-associated diarrhoea? The Journal of Hospital Infection 70 1 6.
14. D'Souza A, Rajkumar C, Cooke J Bulpitt C J (2002) Probiotics in prevention of antibiotic-associated diarrhoea: meta-analysis. British Medical Journal 324 1361.
15. Del Campo R, Bravo D, Canton R, Ruiz-Garbajosa P, Garcia-Albiach R, Montesi-Libois A, Yuste F-J, Abraira V Baquero F (2005) Scarce evidence of yogurt lactic acid bacteria in human feces after daily yogurt consumption by healthy volunteers. Applied and Environmental Microbiology 71 547 549.
16. Dendukuri N Brophy J (2007) Inappropriate use of meta-analysis to estimate efficacy of probiotics. American Journal of Gastroenterology 102 201.
17. Dendukuri N, Costa V, McGregor M Brophy J M (2005) Probiotic therapy for the prevention and treatment of Clostridium difficile-associated diarrhea: a systematic review. Canadian Medical Association Journal 173 167 170.
18. Department of Health and Health Protection Agency (2009) Clostridium difficile infection: how to deal with the problem. http://www.orderline.dh.gov. uk.
19. Dial S, Alrasadi K, Manoukian C, Huang A Menzies D (2004) Risk of Clostridium difficile diarrhoea among hospital inpatients prescribed proton pump inhibitors: cohort and case-control studies. Canadian Medical Association Journal 171 33 38.
20. Doron S I, Hibberd P L Gorbach S L (2008) Probiotics for prevention of antibiotic-associated diarrhoea. Journal of Clinical Gastroenterology 42 (suppl. 2) S58 S63.
21. Dubberke E R, Reske K A, Olsen M A, McMullen K M, Mayfield J L, McDonald L C Fraser V J (2007) Evaluation of Clostridium difficile associated disease pressure as a risk factor for C. difficile-associated disease. Archives of Internal Medicine 167 1092 1097.
22. Durai R (2007) Epidemiology, pathogenesis, and management of Clostridium difficile infection. Digestive Diseases and Sciences 52 2958 2962.
23. Farnworth E F (ed 2008) Handbook of Fermented Functional Foods, 2nd edn. Boca Raton, FL : CRC Press, Taylor & Francis Group.
24. Fenner L, Widmer A F, Goy G, Rudin S Frei R (2008) Rapid and reliable diagnostic algorithm for detection of Clostridium difficile. Journal of Clinical Microbiology 46 328 330.
25. Flemming K Ackermann G (2007) Prevalence of enterotoxin producing Staphylococcus aureus in stools of patients with nosocomial diarrhoea. Infection 35 356 358.
26. Friedman G (ed 2005) Probiotics, prebiotics, and commensal bacteria: perspectives and clinical applications in gastroenterology. Gastroenterology Clinics of North America 34.
27. Gibson G R Wang X (1994) Regulatory effects of bifidobacteria on the growth of other colonic bacteria. The Journal of Applied Bacteriology 77 412 420.
28. Goldin B R, Gorbach S L, Saxelin L, Barakat S, Gualtieri L Salminen S (1992) Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Digestive and Liver Diseases 37 121 128.
29. Gougoulias C, Tuohy K M Gibson G R (2007) Dietary-based gut flora modulation against Clostridium difficile onset. Food Science and Technology Bulletin: Functional Foods 4 31 41.
30. Gravet A, Rondeau M, Harf-Montell C, Grunenberger F, Monteil H, Jean-Michel Scheftel J-M Prévost G (1999) Predominant Staphylococcus aureus isolated from antibiotic-associated diarrhoea is clinically relevant and produces enterotoxin A and the bicomponent toxin LukE-LukD. Journal of Clinical Microbiology 37 4012 4019.
31. Hall I C O'Toole E (1935) Intestinal flora in newborn infants with a description of a new pathogenic anaerobe, Bacillus difficilis. American Journal of Diseases of Children 49 390 402.
32. Hamilton-Miller J M (2008) Elie Metchnikoff and his probiotic legacy. Medical Science History 24 1 5.
33. Hancock P (1997) Antibiotic-associated diarrhoea: Clostridium difficile or Clostridium perfringens? Reviews in Medical Microbiology 8 (suppl. 1) 66 67.
34. Hawrelak J A, Whitten D L Myers S P (2005) Is Lactobacillus rhamnosus GG effective in preventing the onset of antibiotic-associated diarrhoea: a systematic review. Digestion 72 51 56.
35. Hickson M, D'Souza A L, Muthu N, Rogers T R, Want S, Rajkumar C Bulpitt C J (2007) Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. British Medical Journal 335 80.
36. Hopkins M J Macfarlane G T (2002) Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. Journal of Medical Microbiology 51 448 454.
37. Hopkins M J, Sharp R Macfarlane G T (2002) Variation in human intestinal microbiota with age. Digestive and Liver Disease 34 (suppl. 2) S12 S18.
38. Jayatilaka S, Shakov R, Eddi R, Bakaj G, Baddoura W J DeBari V A (2007) Clostridium difficile infection in an urban medical center: five year analysis of infection rates among adult admissions and association with the use of proton pump inhibitors. Annals of Clinical and Laboratory Science 37 241 247.
39. Joint FAO/WHO Expert Consultation (2001) Evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, October 2001, Argentina.
40. Joint FAO/WHO Working Group (2002) Report on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada; April 30 and May 1, 2002.
41. Khedkar C D Ouwehand A C (2006) Modifying the gastrointestinal microbiota with probiotics. in Gastrointestinal Microbiology, pp 315 333. Ouwehand A C, Vaughan E E, eds. New York : Taylor & Francis Group, LLC.
42. Larson H E, Price A B, Honour P Borriello S P (1978) Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1 1063 1066.
43. Martinez C O, Paz V S O'Donnell A (2003) Lactobacillus casei Shirota prevention approach for healthy children with mild acute infection treated with antibiotics. Pediatric Research 4 (suppl. 2) 174A.
44. McCartney A L (2002) Application of molecular biological methods for studying probiotics and the gut flora. The British Journal of Nutrition 88 (suppl. 1) S29 S37.
45. McFarland L V (2006) Meta-analysis of probiotics for the prevention of antibiotic associated diarrhoea and the treatment of Clostridium difficile disease. American Journal of Gastroenterology 101 812 822.
46. McFarland L V (2008a) Renewed interest in a difficult disease: Clostridium difficile infections - epidemiology and current treatment strategies. Current Opinion in Gastroenterology 25 24 35.
47. McFarland L V (2008b) Antibiotic-associated diarrhoea: epidemiology, trends and treatment. Future Microbiology 3 563 578.
48. McFarland L V (2008c) Updates on the changing epidemiology of Clostridium difficile-associated disease. Nature Clinical Practice Gastroenterology and Hepatology 5 40 48.
49. Meier R F (2005) Probiotics: a new treatment for antibiotic-associated diarrhea? Digestion 72 49 50.
50. Metchnikoff E (1907) The Prolongation of Life: Optimistic Studies. London : William Heinemann.
51. Mitsuoka T (1992) Intestinal flora and aging. Nutrition Reviews 50 438 446.
52. Muto C A, Pokrywka M, Shutt K et al. (2005) A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infection Control and Hospital Epidemiology 26 273 280.
53. Owens R C Jr., Donskey C J, Gaynes R P, Loo V G Muto C A (2008) Antimicrobial-associated risk factors for Clostridium difficile infection. Clinical Infectious Diseases 46 (suppl. 1) S19 S31.
54. Pituch H, Obuch-Woszczatyski P, Wultaska D, van Belkum A, Meisel-Mikoajczyk F Uczak M (2007) Laboratory diagnosis of antibiotic-associated diarrhoea: a Polish pilot study into the clinical relevance of Clostridium difficile and Clostridium perfringens toxins. Diagnostic Microbiology and Infectious Disease 51 71 75.
55. Reller M E, Lema C A, Perl T M, Cai M, Ross T L, Speck K A Carroll K C (2007) Yield of stool culture with isolate toxin testing versus a two-step algorithm including stool toxin testing for detection of toxigenic Clostridium difficile. Journal of Clinical Microbiology 45 3601 3605.
56. Rettger L F Cheplin H A (1921) 'A Treatise on the Transformation of the Intestinal Flora with Special Reference to the Implantation of Bacillus Acidophilus'. New Haven, CT : Yale University Press.
57. Saxelin M (1997) Lactobacillus GG - a human probiotic strain with thorough clinical documentation. Food Reviews International 13 293 313. (Pubitemid 127338465)
58. Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S Black R E (2006) Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo controlled trials. Lancet Infectious Diseases 6 374 382.
59. Segarra-Newnham M (2007) Probiotics for Clostridium difficile-associated diarrhoea: focus on Lactobacillus rhamnosus GG and Saccharomyces boulardii. The Annals of Pharmacotherapy 41 1212 1221.
60. Shortt C (1999) The probiotic century: historical and current perspectives. Trends in Food Science & Technology 10 411 417.
61. Spencer R C (1998) Clinical impact and associated costs of Clostridium difficile-associated disease. The Journal of Antimicrobial Chemotherapy 41 (Suppl. C) 5 12.
62. Stockenhuber A, Kamhube C, Leeb G, Adelmann K, Prager E, Mach K Stockenhuber F (2008) Preventing diarrhoea associated with antibiotics using a probiotic Lactobacillus casei preparation. Gut 57 (Suppl II) A20.
63. Stubbs S L J, Brazier J S, O'Neill G L Duerden B I (1999) PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. Journal of Clinical Microbiology 37 461 463.
64. Sullivan A, Barkholt L Nord C E (2003) Lactobacillus acidophilus, Bifidobacterium lactis and Lactobacillus F19 prevent antibiotic-associated ecological disturbances of Bacteroides fragilis in the intestine. The Journal of Antimicrobial Chemotherapy 52 308 311.
65. Surawicz C M (2008) Role of probiotics in antibiotic-associated diarrhea, Clostridium difficile-associated diarrhea, and recurrent Clostridium difficile-associated diarrhea. Journal of Clinical Gastroenterology 42 (suppl. 2) S64 S70.
66. Szajewska A, Skorka A, Ruszcynki M Gieruszczak-Bialek D (2007) Meta-analysis: Lactobacillus GG for treating acute diarrhoea in children. Alimentary Pharmacology and Therapeutics 25 871 881. (Pubitemid 46525343)
67. Thomas C, Stevenson M Riley T V (2003) Antibiotics and hospital-acquired Clostridium difficile-associated diarrhoea: a systematic review. The Journal of Antimicrobial Chemotherapy 51 1339 1350.
68. Tissier H (1906) Le traitement des infections intestinales par la méthode de transformation de la flore bactérienne de l'intestine. Comptes Rendus Hebdomadaires des Séances et Mémoires de la Société de Biologie 60 359 361.
69. van Tongeren S P, Slaets J P J, Harmsen H J M Welling G W (2005) Fecal microbiota composition and frailty. Applied and Environmental Microbiology 71 6438 6442.
70. Tuohy K M, Likotrafiti E, Manderson K, Gibson G R Rastall R A (2004) Improving gut health in the elderly. In Functional Foods, Ageing and Degenerative Disease, pp 394 415. Remacle C, Reusens B, eds. Cambridge, England : CRC Press, Woodhead Publishing Ltd.
71. Tuohy K M, Pinart-Gilberga M, Jones M, Hoyles L, McCartney A L Gibson G R (2007) Survivability of a probiotic Lactobacillus casei in the gastrointestinal tract of healthy human volunteers and its impact on the faecal flora. Journal of Applied Microbiology 102 1026 1032.
72. Viscidi R, Willey S Bartlett J G (1981) Isolation rate and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology 81 5 9.
73. Wenus C, Goll R, Loken E B, Biong A S, Halvorsen D S Florholmen J (2008) Prevention of antibiotic-associated diarrhoea by a fermented probiotic milk drink. European Journal of Clinical Nutrition 62 299 301.
74. Wilcox M H Sandoe J A (2007) Probiotics and diarrhoea: data are not widely applicable. British Medical Journal 335 171.
75. Wilcox M H, Cunniffe J G, Trundle C Redpath C (1996) Financial burden of hospital acquired Clostridium difficile infection. The Journal of Hospital Infection 34 23 30.
76. Wistrom J, Norrby S R, Myhre E B, Eriksson S, Granström G, Lagergren L, Englund G, Nord C E Svenungsson B (2001) Frequency of antibiotic-associated diarrhoea in 2462 antibiotic-treated hospitalized patients: a prospective study. The Journal of Antimicrobial Chemotherapy 47 43 50.
77. Woodmansey E J, McMurdo M E T, Macfarlane G T Macfarlane S (2004) Comparison of composition and metabolic activities of fecal microbiotas in young adults and in antibiotic-treated and non-antibiotic-treated elderly subjects. Applied and Environmental Microbiology 70 6113 6122.