Systematic review: Probiotics in the management of lower gastrointestinal symptoms in clinical practice - An evidence-based international guide

Alimentary Pharmacology and Therapeutics

Volumn 38, Issue 8, 2013, Pages 864-886

  Hungin, A P S ^a   Mulligan, C ^a,b   Pot, B ^c,d   Whorwell, P ^e   Agreus L ^f   Fracasso, P ^g   Lionis, C ^h   Mendive, J ⁱ   Philippart De Foy, J M ^j   Rubin, G ^a   Winchester, C ^b   De Wit, N ^k  

^a DURHAM UNIVERSITY   (United Kingdom)

^b OXFORD PHARMAGENESIS LTD   (United Kingdom)

^c INSERM U1019   (France)

^d UNIV LILLE   (France)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

^f KAROLINSKA INSTITUTE   (Sweden)

^g Don Bosco Outpatient Clinic   (Italy)

^h UNIVERSITY OF CRETE   (Greece)

ⁱ La Mina Primary Health Care Centre   (Spain)

^j Nutrition Committee of the Scientific Society of General Practice (SSMG Belgium)   (Belgium)

^k UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

AB100 JIANNENG; ABT 21 CULTURE; ACTIMEL; ACTIVIA; ALIGN; ANTIBIOTIC AGENT; BIFANTIS; BIO K CL1285; CH; CODEX; CULTURA; DIGESTIVE ADVANTAGE GAS DEFENSE FORMULA; DR10; DUOLAC7; ENTEROGERMINA; GEFILUS MAX; GIFLOREX; GOL12; GOL6; HOWARU BIFIDO; LAB4; LACIDOFIL CAP; LACTIBIANE; PLACEBO; PROBIOTIC AGENT; REFLOR; REUTERIN; SDC; SYMBIOFLOR 2; UNCLASSIFIED DRUG; VALIO BB99; VSL3; YOGHURT; YOSA;

ABDOMINAL DISCOMFORT; ABDOMINAL PAIN; ADULT; ANTIBIOTIC ASSOCIATED DIARRHEA; ANTIBIOTIC THERAPY; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM LONGUM INFANTIS; BLOATING; CLINICAL PRACTICE; DIARRHEA; DISEASE DURATION; DISEASE SEVERITY; DRUG EFFICACY; DRUG INDICATION; DRUG SAFETY; ERADICATION THERAPY; ESCHERICHIA COLI; EVIDENCE BASED MEDICINE; FERMENTED PRODUCT; FLATULENCE; GASTROINTESTINAL SYMPTOM; HELICOBACTER INFECTION; HUMAN; INTERNATIONAL COOPERATION; IRRITABLE COLON; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS PARACASEI; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOSE INTOLERANCE; MAJOR CLINICAL STUDY; MILK; NONHUMAN; PATIENT COMPLIANCE; PRACTICE GUIDELINE; PRIORITY JOURNAL; PROPIONIBACTERIUM FREUDENREICHII; QUALITY OF LIFE; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SACCHAROMYCES BOULARDII; STREPTOCOCCUS SALIVARIUS; SYSTEMATIC REVIEW;

ABDOMINAL PAIN; ANTI-BACTERIAL AGENTS; DELPHI TECHNIQUE; DIARRHEA; HUMANS; IRRITABLE BOWEL SYNDROME; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC;

EID: 84884906412     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/apt.12460     Document Type: Review

References (83)

1. McCormick A, Fleming D, Charlton J., Morbidity Statistics from General Practice: Fourth National Study 1991-1992. London: Office of Population Censuses and Surveys, 1995. Available at: http://www.statistics.gov.uk/downloads/theme- health/MB5No3.pdf. Accessed February 28, 2005.
2. Quigley E, Fried M, Gwee KA, et al,. Irritable bowel syndrome: a global perspective. 2009. Available at: http://www.worldgastroenterology.org/assets/ downloads/en/pdf/guidelines/20-irritable-bowel-syndrome.pdf. Accessed December 2012.
3. Birtwhistle RV,. Irritable bowel syndrome: are complementary and alternative medicine treatments useful? Can Fam Physician 2009; 55: 126-7, 8-9.
4. Moynihan NT, Callahan MJ, Kalsmith B, Moses PL,. How do you spell relief for irritable bowel syndrome? J Fam Pract 2008; 57: 100-8.
5. Simrén M, Barbara G, Flint HJ, et al,. Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut 2013; 62: 159-76.
6. Thabane M, Kottachchi DT, Marshall JK,. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther 2007; 26: 535-44.
7. Porter CK, Gormley R, Tribble DR, Cash BD, Riddle MS,. The incidence and gastrointestinal infectious risk of functional gastrointestinal disorders in a healthy US adult population. Am J Gastroenterol 2011; 106: 130-8.
8. Whelan K,. Probiotics and prebiotics in the management of irritable bowel syndrome: a review of recent clinical trials and systematic reviews. Curr Opin Clin Nutr Metab Care 2011; 14: 581-7.
9. FAO/WHO Working Group. Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food. London, Ontario, Canada, 2002. Available at: ftp://ftp.fao.org/es/esn/food/wgreport2.pdf. Accessed 21 February 2013.
10. Guarner F, Khan AG, Garisch J, et al,. Probiotics and prebiotics. 2011. Available at: http://www.worldgastroenterology.org/probiotics-prebiotics.html. Accessed March 6, 2013.
11. FAO/WHO Expert Consultation., Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria, 2001. Cõrdoba, Argentina. Available at: http://www.who.int/ foodsafety/publications/fs-management/en/probiotics.pdf. Accessed July 11, 2012.
12. Gardiner GE, O'Sullivan E, Kelly J, et al,. Comparative survival rates of human-derived probiotic Lactobacillus paracasei and L. salivarius strains during heat treatment and spray drying. Appl Environ Microbiol 2000; 66: 2605-12.
13. Corcoran BM, Ross RP, Fitzgerald GF, Stanton C,. Comparative survival of probiotic lactobacilli spray-dried in the presence of prebiotic substances. J Appl Microbiol 2004; 96: 1024-39.
14. Hopkins MJ, Sharp R, Macfarlane GT,. Age and disease related changes in intestinal bacterial populations assessed by cell culture, 16S rRNA abundance, and community cellular fatty acid profiles. Gut 2001; 48: 198-205.
15. Sanders ME,. How do we know when something called "probiotic" is really a probiotic? A guideline for consumers and health care professionals. Funct Food Rev 2009; 1: 3-12.
16. Williams MD, Ha CY, Ciorba MA,. Probiotics as therapy in gastroenterology: a study of physician opinions and recommendations. J Clin Gastroenterol 2010; 44: 631-6.
17. Cordina C, Shaikh I, Shrestha S, Camilleri-Brennan J,. Probiotics in the management of gastrointestinal disease: analysis of the attitudes and prescribing practices of gastroenterologists and surgeons. J Dig Dis 2011; 12: 489-96.
18. Sharp RR, Achkar JP, Brinich MA, Farrell RM,. Helping patients make informed choices about probiotics: a need for research. Am J Gastroenterol 2009; 104: 809-13.
19. Schultz M, Baranchi A, Thurston L, et al,. Consumer demographics and expectations of probiotic therapy in New Zealand: results of a large telephone survey. N Z Med J 2011; 124: 36-43.
20. Drossman DA,. The functional gastrointestinal disorders and the Rome III process. Gastroenterology 2006; 130: 1377-90.
21. Brouwers MC, Kho ME, Browman GP, et al,. AGREE II: advancing guideline development, reporting and evaluation in health care. CMAJ 2010; 182: E839-42.
22. Thompson M,. Considering the implication of variations within Delphi research. Fam Pract 2009; 26: 420-4.
23. Linstone HA, Turoff M,. The Delphi method: techniques and applications, 2002. Available at: http://is.njit.edu/pubs/delphibook/. Accessed December 2012.
24. Dalkey N,. An experimental study of group opinion: the Delphi method. Futures 1969; 1: 408-26.
25. Atkins D, Best D, Briss PA, et al,. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490.
26. Drouault-Holowacz S, Bieuvelet S, Burckel A, Cazaubiel M, Dray X, Marteau P,. A double blind randomized controlled trial of a probiotic combination in 100 patients with irritable bowel syndrome. Gastroenterol Clin Biol 2008; 32: 147-52.
27. Enck P, Zimmermann K, Menke G, Klosterhalfen S,. Randomized controlled treatment trial of irritable bowel syndrome with a probiotic E. coli preparation (DSM17252) compared to placebo. Z Gastroenterol 2009; 47: 209-14.
28. Kajander K, Myllyluoma E, Rajilic-Stojanovic M, et al,. Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota. Aliment Pharmacol Ther 2008; 27: 48-57.
29. Kim HJ, Vazquez Roque MI, Camilleri M, et al,. A randomized controlled trial of a probiotic combination VSL# 3 and placebo in irritable bowel syndrome with bloating. Neurogastroenterol Motil 2005; 17: 687-96.
30. Sen S, Mullan MM, Parker TJ, Woolner JT, Tarry SA, Hunter JO,. Effect of Lactobacillus plantarum 299v on colonic fermentation and symptoms of irritable bowel syndrome. Dig Dis Sci 2002; 47: 2615-20.
31. Simrén M, Ohman L, Olsson J, et al,. Clinical trial: the effects of a fermented milk containing three probiotic bacteria in patients with irritable bowel syndrome-a randomized, double-blind, controlled study. Aliment Pharmacol Ther 2010; 31: 218-27.
32. Sondergaard B, Olsson J, Ohlson K, Svensson U, Bytzer P, Ekesbo R,. Effects of probiotic fermented milk on symptoms and intestinal flora in patients with irritable bowel syndrome: a randomized, placebo-controlled trial. Scand J Gastroenterol 2011; 46: 663-72.
33. Whorwell PJ, Altringer L, Morel J, et al,. Efficacy of an encapsulated probiotic Bifidobacterium infantis 35624 in women with irritable bowel syndrome. Am J Gastroenterol 2006; 101: 1581-90.
34. Williams EA, Stimpson J, Wang D, et al,. Clinical trial: a multistrain probiotic preparation significantly reduces symptoms of irritable bowel syndrome in a double-blind placebo-controlled study. Aliment Pharmacol Ther 2009; 29: 97-103.
35. Agrawal A, Houghton LA, Morris J, et al,. Clinical trial: the effects of a fermented milk product containing Bifidobacterium lactis DN-173 010 on abdominal distension and gastrointestinal transit in irritable bowel syndrome with constipation. Aliment Pharmacol Ther 2009; 29: 104-14.
36. Guyonnet D, Chassany O, Ducrotte P, et al,. Effect of a fermented milk containing Bifidobacterium animalis DN-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial. Aliment Pharmacol Ther 2007; 26: 475-86.
37. Ki Cha B, Mun Jung S, Hwan Choi C, et al,. The effect of a multispecies probiotic mixture on the symptoms and fecal microbiota in diarrhea-dominant irritable bowel syndrome: a randomized, double-blind, placebo-controlled trial. J Clin Gastroenterol 2012; 46: 220-7.
38. Kim HJ, Camilleri M, McKinzie S, et al,. A randomized controlled trial of a probiotic, VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2003; 17: 895-904.
39. Zeng J, Li YQ, Zuo XL, Zhen YB, Yang J, Liu CH,. Clinical trial: effect of active lactic acid bacteria on mucosal barrier function in patients with diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2008; 28: 994-1002.
40. Beausoleil M, Fortier N, Guenette S, et al,. Effect of a fermented milk combining Lactobacillus acidophilus Cl1285 and Lactobacillus casei in the prevention of antibiotic-associated diarrhea: a randomized, double-blind, placebo-controlled trial. Can J Gastroenterol 2007; 21: 732-6.
41. Gao XW, Mubasher M, Fang CY, Reifer C, Miller LE,. Dose-response efficacy of a proprietary probiotic formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for antibiotic-associated diarrhea and Clostridium difficile-associated diarrhea prophylaxis in adult patients. Am J Gastroenterol 2010; 105: 1636-41.
42. Sampalis J, Psaradellis E, Rampakakis E,. Efficacy of BIO K+ CL1285 in the reduction of antibiotic-associated diarrhea-a placebo controlled double-blind randomized, multi-center study. Arch Med Sci 2010; 6: 56-64.
43. Hickson M, D'Souza AL, Muthu N, et al,. Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: randomised double blind placebo controlled trial. BMJ 2007; 335: 80.
44. Plummer S, Weaver MA, Harris JC, Dee P, Hunter J,. Clostridium difficile pilot study: effects of probiotic supplementation on the incidence of C. difficile diarrhoea. Int Microbiol 2004; 7: 59-62.
45. ® cap) for the prevention of antibiotic-associated diarrhea: a prospective, randomized, double-blind, multicenter study. J Korean Med Sci 2010; 25: 1784-91.
46. Cindoruk M, Erkan G, Karakan T, Dursun A, Unal S,. Efficacy and safety of Saccharomyces boulardii in the 14-day triple anti-Helicobacter pylori therapy: a prospective randomized placebo-controlled double-blind study. Helicobacter 2007; 12: 309-16.
47. Cremonini F, Di Caro S, Covino M, et al,. Effect of different probiotic preparations on anti-Helicobacter pylori therapy-related side effects: a parallel group, triple blind, placebo-controlled study. Am J Gastroenterol 2002; 97: 2744-9.
48. de Vrese M, Kristen H, Rautenberg P, Laue C, Schrezenmeir J,. Probiotic lactobacilli and bifidobacteria in a fermented milk product with added fruit preparation reduce antibiotic associated diarrhea and Helicobacter pylori activity. J Dairy Res 2011; 78: 396-403.
49. Nista EC, Candelli M, Cremonini F, et al,. Bacillus clausii therapy to reduce side-effects of anti-Helicobacter pylori treatment: randomized, double-blind, placebo controlled trial. Aliment Pharmacol Ther 2004; 20: 1181-8.
50. Waller PA, Gopal PK, Leyer GJ, et al,. Dose-response effect of Bifidobacterium lactis HN019 on whole gut transit time and functional gastrointestinal symptoms in adults. Scand J Gastroenterol 2011; 46: 1057-64.
51. Guyonnet D, Schlumberger A, Mhamdi L, Jakob S, Chassany O,. Fermented milk containing Bifidobacterium lactis DN-173 010 improves gastrointestinal well-being and digestive symptoms in women reporting minor digestive symptoms: a randomised, double-blind, parallel, controlled study. Br J Nutr 2009; 102: 1654-62.
52. Kalman DS, Schwartz HI, Alvarez P, Feldman S, Pezzullo JC, Krieger DR,. A prospective, randomized, double-blind, placebo-controlled parallel-group dual site trial to evaluate the effects of a Bacillus coagulans-based product on functional intestinal gas symptoms. BMC Gastroenterol 2009; 9: 85.
53. Ojetti V, Gigante G, Gabrielli M, et al,. The effect of oral supplementation with Lactobacillus reuteri or tilactase in lactose intolerant patients: randomized trial. Eur Rev Med Pharmacol Sci 2010; 14: 163-70.
54. Pitkala KH, Strandberg TE, Finne Soveri UH, Ouwehand AC, Poussa T, Salminen S,. Fermented cereal with specific bifidobacteria normalizes bowel movements in elderly nursing home residents. A randomized, controlled trial. J Nutr Health Aging 2007; 11: 305-11.
55. ®) supplementation and gastrointestinal and respiratory-tract illness symptoms: a randomised control trial in athletes. Nutr J 2011; 10: 30.
56. Guglielmetti S, Mora D, Gschwender M, Popp K,. Randomised clinical trial: Bifidobacterium bifidum MIMBb75 significantly alleviates irritable bowel syndrome and improves quality of life-a double-blind, placebo-controlled study. Aliment Pharmacol Ther 2011; 33: 1123-32.
57. Hong KS, Kang HW, Im JP, et al,. Effect of probiotics on symptoms in Korean adults with irritable bowel syndrome. Gut Liver 2009; 3: 101-7.
58. Kajander K, Hatakka K, Poussa T, Farkkila M, Korpela R,. A probiotic mixture alleviates symptoms in irritable bowel syndrome patients: a controlled 6-month intervention. Aliment Pharmacol Ther 2005; 22: 387-94.
59. Ligaarden SC, Axelsson L, Naterstad K, Lydersen S, Farup PG,. A candidate probiotic with unfavourable effects in subjects with irritable bowel syndrome: a randomised controlled trial. BMC Gastroenterol 2010; 10: 16.
60. Sinn DH, Song JH, Kim HJ, et al,. Therapeutic effect of Lactobacillus acidophilus-SDC 2012, 2013 in patients with irritable bowel syndrome. Dig Dis Sci 2008; 53: 2714-8.
61. Kim LS, Hilli L, Orlowski J, Kupperman JL, Baral M, Waters RF,. Efficacy of probiotics and nutrients in functional gastrointestinal disorders: a preliminary clinical trial. Dig Dis Sci 2006; 51: 2134-44.
62. Larsen CN, Nielsen S, Kaestel P, et al,. Dose-response study of probiotic bacteria Bifidobacterium animalis subsp lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy young adults. Eur J Clin Nutr 2006; 60: 1284-93.
63. D'Souza AL, Rajkumar C, Cooke J, Bulpitt CJ,. Probiotics in prevention of antibiotic associated diarrhoea: meta-analysis. BMJ 2002; 324: 1361.
64. Cremonini F, Di Caro S, Nista EC, et al,. Meta-analysis: the effect of probiotic administration on antibiotic-associated diarrhoea. Aliment Pharmacol Ther 2002; 16: 1461-7.
65. Hempel S, Newberry SJ, Maher AR, et al,. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA 2012; 307: 1959-69.
66. McFarland LV,. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am J Gastroenterol 2006; 101: 812-22.
67. Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD,. Meta-analysis: the effect of supplementation with probiotics on eradication rates and adverse events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2007; 25: 155-68.
68. Malfertheiner P, Megraud F, O'Morain CA, et al,. Management of Helicobacter pylori infection-the Maastricht IV/Florence Consensus Report. Gut 2012; 61: 646-64.
69. Hickson M,. Probiotics in the prevention of antibiotic-associated diarrhoea and Clostridium difficile infection. Therap Adv Gastroenterol 2011; 4: 185-97.
70. McFarland LV,. Meta-analysis of probiotics for the prevention of traveler's diarrhea. Travel Med Infect Dis 2007; 5: 97-105.
71. Sazawal S, Hiremath G, Dhingra U, Malik P, Deb S, Black RE,. Efficacy of probiotics in prevention of acute diarrhoea: a meta-analysis of masked, randomised, placebo-controlled trials. Lancet Infect Dis 2006; 6: 374-82.
72. Moayyedi P, Ford AC, Talley NJ, et al,. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 2010; 59: 325-32.
73. Sanders ME, Akkermans LM, Haller D, et al,. Safety assessment of probiotics for human use. Gut Microbes 2010; 1: 164-85.
74. Salminen MK, Rautelin H, Tynkkynen S, et al,. Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 2004; 38: 62-9.
75. Boyle RJ, Robins-Browne RM, Tang ML,. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr 2006; 83: 1256-64.
76. Hempel S, Newberry S, Ruelaz A, et al,. Safety of probiotics to reduce risk and prevent or treat disease. Evidence Report/Technology Assessment No. 200. (Prepared by the Southern California Evidence-based Practice Center under Contract No. 290-2007-10062-I.) AHRQ Publication No. 11-E007. Rockville, MD: Agency for Healthcare Research and Quality, 2011. Available at: http://www.ahrq.gov/clinic/tp/probiotictp.htm. Accessed July 29, 2013.
77. Brenner DM, Moeller MJ, Chey WD, Schoenfeld PS,. The utility of probiotics in the treatment of irritable bowel syndrome: a systematic review. Am J Gastroenterol 2009; 104: 1033-49.
78. Mercer M, Brinich MA, Geller G, et al,. How patients view probiotics: findings from a multicenter study of patients with inflammatory bowel disease and irritable bowel syndrome. J Clin Gastroenterol 2012; 46: 138-44.
79. Siro I, Kapolna E, Kapolna B, Lugasi A,. Functional food. Product development, marketing and consumer acceptance-a review. Appetite 2008; 51: 456-67.
80. International Scientific Association for Probiotics and Prebiotics. Probiotics: a consumer guide for making smart choices, 11 March 2009. Available at: http://www.isapp.net/docs/Consumer-Guidelines-probiotic.pdf. Accessed September 26, 2012.
81. O'Connell Motherway M, Zomer A, Leahy SC, et al,. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 2011; 108: 11217-22.
82. Kankainen M, Paulin L, Tynkkynen S, et al,. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci U S A 2009; 106: 17193-8.
83. MacKenzie DA, Tailford LE, Hemmings AM, Juge N,. Crystal structure of a mucus-binding protein repeat reveals an unexpected functional immunoglobulin binding activity. J Biol Chem 2009; 284: 32444-53.