Probiotics in irritable bowel syndrome the science and the evidence

Journal of Clinical Gastroenterology

Volumn 49, Issue , 2015, Pages S60-S64

  Quigley, Eamonn M M ^a,b  

^a HOUSTON METHODIST HOSPITAL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Irritable bowel syndrome; Microbiome; Probiotics; Small intestinal bacterial overgrowth

Indexed keywords

PROBIOTIC AGENT;

ARTICLE; COMMENSAL; DRUG EFFICACY; GASTROINTESTINAL MOTILITY; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; IRRITABLE COLON; MICROBIOME; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SENSATION; GASTROINTESTINAL TRACT; IMMUNOLOGY; INTESTINE FLORA; IRRITABLE BOWEL SYNDROME; MICROBIOLOGY;

GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL MOTILITY; GASTROINTESTINAL TRACT; HUMANS; IRRITABLE BOWEL SYNDROME; PROBIOTICS;

EID: 84944217494     PISSN: 01920790     EISSN: 15392031     Source Type: Journal    
DOI: 10.1097/MCG.0000000000000348     Document Type: Article

References (93)

1. Quigley EMM, Locke GR, Mueller-Lissner S, et al. Prevalence and management of abdominal cramping and pain: a multinational survey. Aliment Pharmacol Ther. 2006;24:411-419.
2. Longstreth GF, Thompson WG, Chey WD, et al. Functional bowel disorders. Gastroenterology. 2006;130:1480-1491.
3. Saito YA, Schoenfeld P, Locke GR 3rd. The epidemiology of irritable bowel syndrome in North America: a systematic review. Am J Gastroenterol. 2002;97:1910-1915.
4. Quigley EMM, Abdel-Hamid H, Barbara G, et al. A global perspective on irritable bowel syndrome. A consensus statement of the World Gastroenterology Organization (WGO) Summit Task Force on Irritable Bowel Syndrome. J Clin Gastroenterol. 2012;46:356-366.
5. Hussein Z, Quigley EMM. Complementary and alternative medicine in the irritable bowel syndrome. Aliment Pharmacol Ther. 2006;23:465-471.
6. Quigley EM. Bugs on the brain; brain in the gut-seeking explanations for common gastrointestinal symptoms. Ir J Med Sci. 2012;182:1-6.
7. Kamiya T, Wang L, Forsythe P, et al. Inhibitory effects of Lactobacillus reuteri on visceral pain induced by colorectal distension in Sprague-Dawley rats. Gut. 2006;55:191-196.
8. Verdu EF, Bercik P, Verma-Gandhu M, et al. Specific probiotic therapy attenuates antibiotic induced visceral hypersensitivity in mice. Gut. 2006;55:182-190.
9. Ait-Belgnaoui A, Han W, Lamine F, et al. Lactobacillus farciminis treatment suppresses stress-induced visceral hypersensitivity: a possible action through interaction with epithelial cells cytoskeleton contraction. Gut. 2006;55:1090-1094.
10. Eutamene H, Lamine F, Chabo C, et al. Synergy between Lactobacillus paracasei and its bacterial products to counteract stress-induced gut permeability and sensitivity increase in rats. J Nutr. 2007;137:1901-1907.
11. Johnson AC, Greenwood-Van Meerveld B, McRorie J. Effects of Bifidobacterium infantis 35624 on post-inflammatory visceral hypersensitivity in the rat. Dig Dis Sci. 2011;56:3179-3186.
12. Quigley EMM. The role of gas in IBS. In: Camilleri M, Spiller RC, eds. Irritable Bowel Syndrome Diagnosis and Treatment. Philadelphia: WB Saunders Co.; 2002:77-84.
13. Quigley EMM. From comic relief to real understanding; how intestinal gas causes symptoms. Gut. 2003;52:1659-1661.
14. Serra J, Azpiroz F, Malagelada JR. Impaired transit and tolerance of gas in the irritable bowel syndrome. Gut. 2001;48:14-19.
15. 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;29:104-114.
16. Verdu EF, Bercik P, Bergonzelli GE, et al. Lactobacillus paracasei normalizes muscle hypercontractility in a murine model of postinfective gut dysfunction. Gastroenterology. 2004;127:826-837.
17. Jeffrey IB, Quigley EM, Öhman L, et al. The microbiota link to irritable bowel syndrome: an emerging story. Gut Microbes. 2012;3:572-576.
18. Charbonneau D, Gibb RD, Quigley EM. Fecal excretion of Bifidobacterium infantis 35624 and changes in fecal microbiota after eight weeks of oral supplementation with encapsulated probiotic. Gut Microbes. 2013;4:201-211.
19. Scully P, Macsharry J, O'Mahony D, et al. Bifidobacterium infantis suppression of Peyer's patch MIP-1a and MIP-1b secretion during Salmonella infection correlates with increased local CD4+ CD25+ T cell numbers. Cell Immunol. 2013;281:134-140.
20. Joyce SA, MacSharry J, Casey PG, et al. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc Natl Acad Sci USA. 2014;111:7421-7426.
21. King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet. 1998;352:1187-1189.
22. Joyce SA, Shanahan F, Hill C, et al. Bacterial bile salt hydrolase in host metabolism: potential for influencing gastrointestinal microbe-host crosstalk. Gut Microbes. 2014;5:669-674.
23. Sipka S, Bruckner G. The immunomodulatory role of bile acids. Int Arch Allergy Immunol. 2014;165:1-8.
24. Weston AP, Biddle WL, Bhatia PS, et al. Terminal ileal mucosal mast cells in irritable bowel syndrome. Dig Dis Sci. 1993;38:1590-1595.
25. Talley NJ, Butterfield J. Mast cell infiltration and degranulation in colonic mucosa in the irritable bowel syndrome. Am J Gastroenterol. 1996;91:1675-1676.
26. O'Sullivan M, Clayton N, Breslin NP, et al. Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Motil. 2000;12:449-457.
27. Spiller RC, Jenkins D, Thornley JP, et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in postdysenteric irritable bowel syndrome. Gut. 2000;47:804-811.
28. Chadwick VS, Chen W, Shu D, et al. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology. 2002;122:1778-1783.
29. Barbara G, Stanghellini V, De Giorgio R, et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syndrome. Gastroenterology. 2004;126:693-702.
30. Crowell MD, Shetzline MA, Moses PL, et al. Enterochromaffin cells and 5-HT signaling in the pathophysiology of disorders of gastrointestinal function. Curr Opin Investig Drugs. 2004;5:55-60.
31. Piche T, Saint-Paul MC, Dainese R, et al. Mast cells and cellularity of the colonic mucosa correlated with fatigue and depression in irritable bowel syndrome. Gut. 2008;57:468-473.
32. Barbara G, Cremon C. Serine proteases: new players in diarrhoea-predominant irritable bowel syndrome. Gut. 2008;57:1035-1037.
33. 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;128:541-551.
34. Dinan TG, Quigley EM, Ahmed SM, et al. Hypothalamicpituitarygut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology. 2006;130:304-311.
35. Scully P, McKernan DP, Keohane J, et al. Plasma cytokine profiles in females with irritable bowel syndrome and extraintestinal co-morbidity. Am J Gastroenterol. 2010;105:2235-2243.
36. Brint EK, MacSharry J, Fanning A, et al. Differential expression of toll-like receptors in patients with irritable bowel syndrome. Am J Gastroenterol. 2011;106:329-336.
37. McCarthy J, O'Mahony L, O'Callaghan L, et al. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut. 2003;52:975-980.
38. Rachmilewitz D, Kayatura K, Karmeli F, et al. Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology. 2004;126:520-528.
39. Jijon H, Backer J, Diaz H, et al. DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology. 2004;126:1358-1373.
40. Hart AL, Lammers K, Brigidi P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut. 2004;53:1602-1609.
41. O'Mahony L, O'Callaghan L, McCarthy J, et al. Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans. Am J Physiol. 2006;290:G839-G845.
42. Konieczna P, Groeger D, Ziegler M, et al. Bifidobacterium infantis 35624 administration induces Foxp3+ 1 T regulatory cells in human peripheral blood - potential role for myeloid and plasmacytoid dendritic cells. Gut. 2012;61:354-366.
43. Gionchetti P, Rizzello F, Helwig U, et al. Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology. 2003;124:1202-1209.
44. Mimura T, Rizzello F, Helwig U, et al. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut. 2004;53:108-114.
45. Camilleri M. Peripheral mechanisms in irritable bowel syndrome. N Engl J Med. 2012;367:1626-1635.
46. Piche T. Tight junctions and IBS-the link between epithelial permeability, low-grade inflammation, and symptom generation? Neurogastroenterol Motil. 2014;26:296-302.
47. Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology. 2001;121:580-591.
48. Laval L, Martin R, Natividad J, et al. Lactobacillus rhamnosus CNCM I-3690 and the commensal bacterium Faecalibacterium prausnitzii A2-165 exhibit similar protective effects to induced barrier hyper-permeability in mice. Gut Microbes. 2015;6:1-9.
49. Hyland NP, Quigley EM, Brint E. Microbiota-host interactions in irritable bowel syndrome: epithelial barrier, immune regulation and brain-gut interactions. World J Gastroenterol. 2014;20:8859-8866.
50. Persborn M, Gerritsen J, Wallon C, et al. The effects of probiotics on barrier function and mucosal pouch microbiota during maintenance treatment for severe pouchitis in patients with ulcerative colitis. Aliment Pharmacol Ther. 2013;38:772-783.
51. Sheil B, McCarthy J, O'Mahony L, et al. Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut. 2004;53:694-700.
52. Groeger D, O'Mahony L, Murphy EF, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes. 2013;4:325-339.
53. 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 USA. 2011;108:16050-16055.
54. Cryan JF, O'Mahony SM. The microbiome-gut-brain axis: from bowel to behavior. Neurogastroenterol Motil. 2011;23:187-192.
55. Cryan JF, Dinan TG. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci. 2012;13:701-712.
56. Desbonnet L, Clarke G, Shanahan F, et al. Microbiota is essential for social development in the mouse. Mol Psychiatry. 2014;19:146-148.
57. Dinan TG. Inflammatory markers in depression. Curr Opin Psychiatry. 2009;22:32-36.
58. Dennison U, McKernan D, Cryan J, et al. Schizophrenia patients with a history of childhood trauma have a proinflammatory phenotype. Psychol Med. 2012;42:1865-1871.
59. Tillisch K, Labus J, Kilpatrick L, et al. Consumption of fermented milk product with probiotic modulates brain activity. Gastroenterology. 2013;144:1394-1401.
60. Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of postinfectious irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:535-544.
61. Quigley EMM. Therapies aimed at the gut microbiota and inflammation. Antibiotics, probiotics/prebiotics/synbiotics, antiinflammatory therapies. Gastroenterol Clin North Am. 2011;40:207-222.
62. Codling C, O'Mahony L, Shanahan F, et al. A molecular analysis of fecal and mucosal bacterial communities in irritable bowel syndrome. Dig Dis Sci. 2010;55:392-397.
63. Carroll IM, Ringel-Kulka T, Keku TO, et al. Molecular analysis of the luminal- and mucosal-associated intestinal microbiota in diarrhea-predominant irritable bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2011;301:G799-G807.
64. Durbán A, Abellán JJ, Jiménez-Hernández N, et al. Structural alterations of faecal and mucosa-associated bacterial communities in irritable bowel syndrome. Environ Microbiol Rep. 2012;4:242-247.
65. Parkes GC, Rayment NB, Hudspith BN, et al. Distinct microbial populations exist in the mucosa-associated microbiota of sub-groups of irritable bowel syndrome. Neurogastroenterol Motil. 2012;24:31-39.
66. Kassinen A, Krogius-Kurikka L, Mäkivuokko H, et al. The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects. Gastroenterology. 2007;133:24-33.
67. Krogius-Kurikka L, Lyra A, Malinen E, et al. Microbial community analysis reveals high level phylogenetic alterations in the overall gastrointestinal microbiota of diarrhoea-predominant irritable bowel syndrome sufferers. BMC Gastroenterol. 2009;9:95.
68. Rajilić-Stojanović M, Biagi E, Heilig HG, et al. Global and deep molecular analysis of microbiota signatures in fecal samples from patients with irritable bowel syndrome. Gastroenterology. 2011;141:1792-1801.
69. Saulnier DM, Riehle K, Mistretta TA, et al. Gastrointestinal microbiome signatures of pediatric patients with irritable bowel syndrome. Gastroenterology. 2011;141:1782-1791.
70. Rigsbee L, Agans R, Shankar V, et al. Quantitative profiling of gut microbiota of children with diarrhea-predominant irritable bowel syndrome. Am J Gastroenterol. 2012;107:1740-1751.
71. Carroll IM, Ringel-Kulka T, Siddle JP, et al. Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil. 2012;24:521-530.
72. Duboc H, Rainteau D, Rajca S, et al. Increase in fecal primary bile acids and dysbiosis in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroenterol Motil. 2012;24:513-520.
73. Chassard C, Dapoigny M, Scott KP, et al. Functional dysbiosis within the gut microbiota of patients with constipatedirritable bowel syndrome. Aliment Pharmacol Ther. 2012;35:828-838.
74. Jeffery IB, O'Toole PW, Öhman L, et al. An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota. Gut. 2012;61:997-1006.
75. Jalanka-Tuovinen J, Salojärvi J, Salonen A, et al. Faecal microbiota composition and host-microbe cross-talk following gastroenteritis and in postinfectious irritable bowel syndrome. Gut. 2014;63:1737-1745.
76. Durbán A, Abellán JJ, Jiménez-Hernández N, et al. Instability of the faecal microbiota in diarrhoea-predominant irritable bowel syndrome. FEMS Microbiol Ecol. 2013;86:581-589.
77. Pimentel M, Chow EJ, Lin HC. Eradication of small intestinal bacterial overgrowth reduces symptoms of irritable bowel syndrome. Am J Gastroenterol. 2000;95:3503-3506.
78. Pimentel M, Chow EJ, Lin HC. Normalization of lactulose breath testing correlates with symptom improvement in irritable bowel syndrome: a double-blind, randomized, placebocontrolled study. Am J Gastroenterol. 2003;98:412-419.
79. Quigley EMM. A 51-year old with IBS. Test or treat for bacterial overgrowth? Clin Gastroenterol Hepatol. 2007;5:114-1143.
80. Quigley EMM, Abu-Shanab A. The diagnosis of small intestinal bacterial overgrowth. The challenges persist!. Expert Rev Gastroenterol Hepatol. 2009;3:77-87.
81. Ford AC, Spiegel BM, Talley NJ, et al. Small intestinal bacterial overgrowth in irritable bowel syndrome: systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2009;7:1279-1286.
82. Pimentel M, Lembo A, Chey WD, et al. for the TARGET Study Group. Rifaximin therapy for patients with irritable bowel syndrome without constipation. N Engl J Med. 2011;364:22-32.
83. 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;19:166-172.
84. McFarland LV, Dublin S. Meta-analysis of probiotics for the treatment of irritable bowel syndrome. World J Gastroenterol. 2008;14:2650-2661.
85. Nikfar S, Rahimi R, Rahimi F, et al. Efficacy of probiotics in irritable bowel syndrome: a meta-analysis of randomized, controlled trials. Dis Colon Rectum. 2008;51:1775-1780.
86. Brenner DM, Moeller MJ, Chey WD, et al. The utility of probiotics in the treatment of irritable bowel syndrome: a systematic review. Am J Gastroenterol. 2009;104:1033-1049.
87. Hoveyda N, Heneghan C, Mahtani KR, et al. A systematic review and meta-analysis: probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterol. 2009;9:15.
88. Moayyedi P, Ford AC, Talley NJ, et al. The efficacy of probiotics in the therapy of irritable bowel syndrome: a systematic review. Gut. 2010;59:325-332.
89. Hungin AP, Mulligan C, Pot B, et al. European Society for Primary Care Gastroenterology. Systematic review: probiotics in the management of lower gastrointestinal symptoms in clinical practice-an evidence-based international guide. Aliment Pharmacol Ther. 2013;38:864-886.
90. Ford AC, Quigley EM, Lacy BE, et al. Efficacy of prebiotics, probiotics, and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: systematic review and metaanalysis. Am J Gastroenterol. 2014;109:1547-1561.
91. 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.
92. Ringel Y, Ringel-Kulka T, Maier D, et al. Clinical trial: 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;45:518-525.
93. 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;17:687-696.