Review article: Probiotics for the treatment of irritable bowel syndrome - Focus on lactic acid bacteria

Alimentary Pharmacology and Therapeutics

Volumn 35, Issue 4, 2012, Pages 403-413

  Clarke, G ^a,b   Cryan, J F ^a,b   Dinan, T G ^a,b   Quigley, E M ^a,b  

^a UNIVERSITY COLLEGE CORK   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

PLACEBO; PROBIOTIC AGENT;

BACILLUS COAGULANS; BIFIDOBACTERIUM ANIMALIS; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE; BIFIDOBACTERIUM LONGUM; BIFIDOBACTERIUM LONGUM INFANTIS; DEFECATION; DOSE RESPONSE; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; ENTEROCOCCUS FAECIUM; HUMAN; INTESTINE FLORA; IRRITABLE COLON; LACTIC ACID BACTERIUM; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CASEI; LACTOBACILLUS HELVETICUS; LACTOBACILLUS PARACASEI; LACTOBACILLUS PLANTARUM; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SALIVARIUS; MICROBIOME; NONHUMAN; OPTIMAL DRUG DOSE; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME; UNSPECIFIED SIDE EFFECT;

ANIMALS; HUMANS; IRRITABLE BOWEL SYNDROME; LACTIC ACID; LACTOBACILLUS; PROBIOTICS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TREATMENT OUTCOME;

EID: 84856033373     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2011.04965.x     Document Type: Review

References (103)

1. Forbes AL, Hunter JO,. Irritable bowel syndrome. Medicine 2007; 35: 267-71. (Pubitemid 46666790)
2. Spiller R, Aziz Q, Creed F, et al,. Guidelines on the irritable bowel syndrome: mechanisms and practical management. Gut 2007; 56: 1770-98. (Pubitemid 350206308)
3. Maxion-Bergemann S, Thielecke F, Abel F, Bergemann R,. Costs of irritable bowel syndrome in the UK and US. Pharmacoeconomics 2006; 24: 21-37. (Pubitemid 43197228)
4. Drossman DA,. The functional gastrointestinal disorders and the Rome III process. Gastroenterology 2006; 130: 1377-90.
5. Talley NJ,. Irritable bowel syndrome. Intern Med J 2006; 36: 724-8. (Pubitemid 44563434)
6. Ohman L, Simren M,. New insights into the pathogenesis and pathophysiology of irritable bowel syndrome. Dig Liver Dis 2007; 39: 201-15. (Pubitemid 46196435)
7. Cryan JF, O'Mahony SM,. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil 2011; 23: 187-92.
8. Clarke G, Quigley EM, Cryan JF, Dinan TG,. Irritable bowel syndrome: towards biomarker identification. Trends Mol Med 2009; 15: 478-89.
9. Snelling N,. Do any treatments work for irritable bowel syndrome? Int J Osteopath Med 2006; 9: 137-42. (Pubitemid 46049151)
10. Camilleri M, Chang L,. Challenges to the therapeutic pipeline for irritable bowel syndrome: end points and regulatory hurdles. Gastroenterology 2008; 135: 1877-91.
11. Quigley EM,. Changing face of irritable bowel syndrome. World J Gastroenterol 2006; 12: 1-5. (Pubitemid 43126074)
12. Quigley EM,. Antibiotics for irritable bowel syndrome: hitting the target, but what is it? Gastroenterology 2011; 141: 391-3.
13. Quigley EM,. Bacterial flora in irritable bowel syndrome: role in pathophysiology, implications for management. J Dig Dis 2007; 8: 2-7. (Pubitemid 46189203)
14. Quigley EM, Flourie B,. Probiotics and irritable bowel syndrome: a rationale for their use and an assessment of the evidence to date. Neurogastroenterol Motil 2007; 19: 166-72. (Pubitemid 46239427)
15. Parvez S, Malik KA, Ah Kang S, Kim HY,. Probiotics and their fermented food products are beneficial for health. J Appl Microbiol 2006; 100: 1171-85. (Pubitemid 43739184)
16. Kleerebezem M, Vaughan EE,. Probiotic and gut lactobacilli and bifidobacteria: molecular approaches to study diversity and activity. Annu Rev Microbiol 2009; 63: 269-90.
17. Holzapfel WH, Haberer P, Geisen R, Bjorkroth J, Schillinger U,. Taxonomy and important features of probiotic microorganisms in food and nutrition. Am J Clin Nutr 2001; 73 (2 Suppl.): 365S-73S. (Pubitemid 32113257)
18. Adlerberth I, Wold AE,. Establishment of the gut microbiota in Western infants. Acta Paediatr 2009; 98: 229-38.
19. Mackie RI, Sghir A, Gaskins HR,. Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 1999; 69: 1035S-45S. (Pubitemid 29205082)
20. O'Hara AM, Shanahan F,. The gut flora as a forgotten organ. EMBO Rep 2006; 7: 688-93. (Pubitemid 43986264)
21. Quigley EM,. Probiotics in functional bowel disorders getting it right. J Clin Gastroenterol 2011; 45: 481-2.
22. Shanahan F,. Probiotics in perspective. Gastroenterology 2010; 139: 1808-12.
23. Rhee SH, Pothoulakis C, Mayer EA,. Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 2009; 6: 306-14.
24. Heijtz RD, Wang S, Anuar F, et al,. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A 2011; 108: 3047-52.
25. Neufeld KM, Kang N, Bienenstock J, Foster JA,. Reduced anxiety-like behavior and central neurochemical change in germ-free mice. Neurogastroenterol Motil 2010; 23: 255-64, e119.
26. Sudo N, Chida Y, Aiba Y, et al,. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol 2004; 558: 263-75. (Pubitemid 39077406)
27. Kennedy P, Clarke G, Quigley EM, Groeger J, Dinan T, Cryan JF,. Gut memories: towards a cognitive neurobiology of irritable bowel syndrome. Neurosci Biobehav Rev 2012; 36: 310-40.
28. Quigley EM,. Probiotics in functional gastrointestinal disorders: what are the facts? Curr Opin Pharmacol 2008; 8: 704-8.
29. Quigley EM,. Do patients with functional gastrointestinal disorders have an altered gut flora? Therap Adv Gastroenterol 2009; 2: 23-30.
30. Whorwell PJ,. Do probiotics improve symptoms in patients with irritable bowel syndrome? Therap Adv Gastroenterol 2009; 2: 37-44.
31. Verdu EF,. Probiotics effects on gastrointestinal function: beyond the gut? Neurogastroenterol Motil 2009; 21: 477-80.
32. O'Mahony L, McCarthy J, Kelly P, et al,. Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005; 128: 541-51. (Pubitemid 40585355)
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. (Pubitemid 43980633)
34. Konieczna P, Groeger D, Ziegler M, et al,. Bifidobacterium infantis 35624 administration induces Foxp3 T regulatory cells in human peripheral blood: potential role for myeloid and plasmacytoid dendritic cells. Gut 2011 [Epub ahead of print].
35. McKernan DP, Fitzgerald P, Dinan TG, Cryan JF,. The probiotic Bifidobacterium infantis 35624 displays visceral antinociceptive effects in the rat. Neurogastroenterol Motil 2010; 22: 1029-35, e268.
36. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG,. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res 2008; 43: 164-74.
37. 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.
38. 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.
39. Andriulli A, Neri M, Loguercio C, et al,. Clinical trial on the efficacy of a new symbiotic formulation, Flortec, in patients with irritable bowel syndrome: a multicenter, randomized study. J Clin Gastroenterol 2008; 42 (Suppl. 3 Pt 2): S218-23.
40. Niedzielin K, Kordecki H, Birkenfeld B,. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol 2001; 13: 1143-7. (Pubitemid 33015878)
41. Rousseaux C, Thuru X, Gelot A, et al,. Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 2007; 13: 35-7. (Pubitemid 46067383)
42. Verdu EF, Bercik P, Verma-Gandhu M, et al,. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut 2006; 55: 182-90. (Pubitemid 43117275)
43. Gawronska A, Dziechciarz P, Horvath A, Szajewska H,. A randomized double-blind placebo-controlled trial of Lactobacillus GG for abdominal pain disorders in children. Aliment Pharmacol Ther 2007; 25: 177-84. (Pubitemid 46046374)
44. Francavilla R, Miniello V, Magista AM, et al,. A randomized controlled trial of Lactobacillus GG in children with functional abdominal pain. Pediatrics 2010; 126: e1445-52.
45. Bausserman M, Michail S,. The use of Lactobacillus GG in irritable bowel syndrome in children: a double-blind randomized control trial. J Pediatr 2005; 147: 197-201. (Pubitemid 41207833)
46. Horvath A, Dziechciarz P, Szajewska H,. Meta-analysis: Lactobacillus rhamnosus GG for abdominal pain-related functional gastrointestinal disorders in childhood. Aliment Pharmacol Ther 2011; 33: 1302-10.
47. O'Sullivan MA, O'Morain CA,. Bacterial supplementation in the irritable bowel syndrome. A randomised double-blind placebo-controlled crossover study. Dig Liver Dis 2000; 32: 294-301. (Pubitemid 30445067)
48. Nobaek S, Johansson ML, Molin G, Ahrne S, Jeppsson B,. Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am J Gastroenterol 2000; 95: 1231-8. (Pubitemid 30263518)
49. Enck P, Zimmermann K, Menke G, Muller-Lissner S, Martens U, Klosterhalfen S,. A mixture of Escherichia coli (DSM 17252) and Enterococcus faecalis (DSM 16440) for treatment of the irritable bowel syndrome-a randomized controlled trial with primary care physicians. Neurogastroenterol Motil 2008; 20: 1103-9.
50. Guandalini S, Magazzu G, Chiaro A, et al,. VSL#3 improves symptoms in children with irritable bowel syndrome: a multicenter, randomized, placebo-controlled, double-blind, crossover study. J Pediatr Gastroenterol Nutr 2010; 51: 24-30.
51. 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. (Pubitemid 351637577)
52. Kim YG, Moon JT, Lee KM, Chon NR, Park H,. The effects of probiotics on symptoms of irritable bowel syndrome. Korean J Gastroenterol 2006; 47: 413-9.
53. Saggioro A,. Probiotics in the treatment of irritable bowel syndrome. J Clin Gastroenterol 2004; 38 (6 Suppl.): S104-6.
54. Choi SC, Kim BJ, Rhee PL, et al,. Probiotic fermented milk containing dietary fiber has additive effects in IBS with constipation compared to plain probiotic fermented milk. Gut Liver 2011; 5: 22-8.
55. 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.
56. 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. (Pubitemid 36459602)
57. 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. (Pubitemid 41400717)
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. (Pubitemid 41248105)
59. 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. (Pubitemid 350212625)
60. 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.
61. Simren 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.
62. 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.
63. 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.
64. Ringel-Kulka T, Palsson OS, Maier D, et al,. Probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium lactis Bi-07 versus placebo for the symptoms of bloating in patients with functional bowel disorders: a double-blind study. J Clin Gastroenterol 2011; 45: 518-25.
65. 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. (Pubitemid 47063138)
66. Dolin BJ,. Effects of a proprietary Bacillus coagulans preparation on symptoms of diarrhea-predominant irritable bowel syndrome. Methods Find Exp Clin Pharmacol 2009; 31: 655-9.
67. 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. (Pubitemid 35305475)
68. Barrett JS, Canale KE, Gearry RB, Irving PM, Gibson PR,. Probiotic effects on intestinal fermentation patterns in patients with irritable bowel syndrome. World J Gastroenterol 2008; 14: 5020-4.
69. Long ZR, Yu CH, Yang Y, Wang HN, Chi XX,. Clinical observation on acupuncture combined with microorganism pharmaceutical preparations for treatment of irritable bowel syndrome of constipation type. Zhongguo Zhen Jiu 2006; 26: 403-5.
70. Gade J, Thorn P,. Paraghurt for patients with irritable bowel syndrome. A controlled clinical investigation from general practice. Scand J Prim Health Care 1989; 7: 23-6. (Pubitemid 19096834)
71. Niv E, Naftali T, Hallak R, Vaisman N,. The efficacy of Lactobacillus reuteri ATCC 55730 in the treatment of patients with irritable bowel syndrome-a double blind, placebo-controlled, randomized study. Clin Nutr 2005; 24: 925-31. (Pubitemid 41782449)
72. 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.
73. Brigidi P, Vitali B, Swennen E, Bazzocchi G, Matteuzzi D,. Effects of probiotic administration upon the composition and enzymatic activity of human fecal microbiota in patients with irritable bowel syndrome or functional diarrhea. Res Microbiol 2001; 152: 735-41. (Pubitemid 32905506)
74. 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.
75. Tsuchiya J, Barreto R, Okura R, Kawakita S, Fesce E, Marotta F,. Single-blind follow-up study on the effectiveness of a symbiotic preparation in irritable bowel syndrome. Chin J Dig Dis 2004; 5: 169-74. (Pubitemid 40028569)
76. 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.
77. Ford AC,. Probiotics in irritable bowel syndrome: underachievers or underpowered? Aliment Pharmacol Ther 2010; 31: 922-3; author reply 923-4.
78. Ghoshal UC, Park H, Gwee KA,. Bugs and irritable bowel syndrome: The good, the bad and the ugly. J Gastroenterol Hepatol 2010; 25: 244-51.
79. Parkes GC, Sanderson JD, Whelan K,. Treating irritable bowel syndrome with probiotics: the evidence. Proc Nutr Soc 2010; 69: 187-94.
80. Moayyedi P, Ford AC, Talley NJ, et al,. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 2008; 59: 325-32.
81. Hoveyda N, Heneghan C, Mahtani KR, Perera R, Roberts N, Glasziou P,. A systematic review and meta-analysis: probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterol 2009; 9: 15.
82. Lyra A, Krogius-Kurikka L, Nikkila J, et al,. Effect of a multispecies probiotic supplement on quantity of irritable bowel syndrome-related intestinal microbial phylotypes. BMC Gastroenterol 2010; 10: 110.
83. Hong YS, Hong KS, Park MH, et al,. Metabonomic understanding of probiotic effects in humans with irritable bowel syndrome. J Clin Gastroenterol 2011; 45: 415-25.
84. Desbonnet L, Garrett L, Clarke G, Kiely B, Cryan JF, Dinan TG,. Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience 2010; 170: 1179-88.
85. Bravo JA, Forsythe P, Chew MV, et al,. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A 2011; 108: 16050-5.
86. Messaoudi M, Lalonde R, Violle N, et al,. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr 2011; 105: 755-64.
87. Heuvelin E, Lebreton C, Bichara M, Cerf-Bensussan N, Heyman M,. A Bifidobacterium probiotic strain and its soluble factors alleviate chloride secretion by human intestinal epithelial cells. J Nutr 2009; 140: 7-11.
88. Ewaschuk JB, Diaz H, Meddings L, et al,. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am J Physiol Gastrointest Liver Physiol 2008; 295: G1025-34.
89. Zareie M, Johnson-Henry K, Jury J, et al,. Probiotics prevent bacterial translocation and improve intestinal barrier function in rats following chronic psychological stress. Gut 2006; 55: 1553-60. (Pubitemid 44629200)
90. Mangell P, Nejdfors P, Wang M, et al,. Lactobacillus plantarum 299v inhibits Escherichia coli-induced intestinal permeability. Dig Dis Sci 2002; 47: 511-6. (Pubitemid 34218876)
91. Halpern GM, Prindiville T, Blankenburg M, Hsia T, Gershwin ME,. Treatment of irritable bowel syndrome with Lacteol Fort: a randomized, double-blind, cross-over trial. Am J Gastroenterol 1996; 91: 1579-85. (Pubitemid 26269174)
92. Kopp-Hoolihan L,. Prophylactic and therapeutic uses of probiotics: a review. J Am Diet Assoc 2001; 101: 229-38.
93. van Reenen CA, Dicks LM,. Horizontal gene transfer amongst probiotic lactic acid bacteria and other intestinal microbiota: what are the possibilities? A review Arch Microbiol 2011; 193: 157-68.
94. Boyle RJ, Robins-Browne RM, Tang ML,. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr 2006; 83: 1256-64. (Pubitemid 44713053)
95. Chapman CM, Gibson GR, Rowland I,. Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 2011; 50: 1-17.
96. Shanahan F,. The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 2002; 16: 915-31.
97. Aragon G, Graham DB, Borum M, Doman DB,. Probiotic therapy for irritable bowel syndrome. Gastroenterol Hepatol (N Y) 2010; 6: 39-44.
98. Shanahan F,. Gut microbes: from bugs to drugs. Am J Gastroenterol 2010; 105: 275-9.
99. Bischoff SC,. 'Gut health': a new objective in medicine? BMC Med 2010; 9: 24.
100. Archie E, Theis K,. Animal behaviour meets microbial ecology. Anim Behav 2011; 82: 425-36.
101. Marteau P,. Probiotics in functional intestinal disorders and IBS: proof of action and dissecting the multiple mechanisms. Gut 2010; 59: 285-6.
102. Guarner F, Ellen Sanders M, Gibson G, et al,. Probiotic and prebiotic claims in Europe: seeking a clear roadmap. Br J Nutr 2011; 106: 1765-7.
103. Barbara G, Corinaldesi R,. Probiotics: could they turn out to be ineffective in irritable bowel syndrome? Dig Liver Dis 2000; 32: 302-4. (Pubitemid 30445068)