Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-28T15:30:42.445Z Has data issue: false hasContentIssue false

Probiotics and inflammatory bowel disease: from fads and fantasy to facts and future

Published online by Cambridge University Press:  09 March 2007

Fergus Shanahan*
Affiliation:
Department of Medicine, Clinical Sciences Building, Cork University Hospital, Wilton, Cork, Ireland
*
*Corresponding author: Professor Fergus Shanahan, fax +353 21 4345300, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Probiotic therapy is attracting the renewed interest of clinicians and basic investigators from a variety of traditional research disciplines. While the theoretical rationale for modifying the commensal flora of the gastrointestinal tract in specific circumstances appears sound and requires scientific pursuit, the field of probiotics has been clouded by exaggerated claims from some quarters. In general, many of the claims for therapeutic efficacy have not been well substantiated, but the field is now poised for evaluation within the realm of evidence-based medicine. Alterations in commensal bacterial flora within the gastrointestinal tract are associated with susceptibility to pathogens such as Clostridium difficile and there is persuasive evidence that the normal flora may participate in the pathogenesis of inflammatory bowel disease and other chronic diseases in genetically susceptible individuals. This has prompted various strategies to fortify or otherwise modify the enteric flora by dietary supplements containing probiotic formulations. Detailed comparisons of probiotic performance amongst different bacterial strains have not been performed in vivo in man or under clinical trial conditions, and the level of scientific characterisation of individual organisms has been variable. In addition, it cannot be assumed that the same probiotic is equally suitable for all individuals. Moreover, the heterogeneity of clinical disorders such as Crohn's disease and ulcerative colitis implies that strain-specific properties may be required for subset-specific categories of patients. While cocktails of probiotics offer convenience, therapeutic progress may require clarification of the mechanism of probiotic action and may be delayed until individual bacterial components have been rigorously studied. More importantly, the full potential of therapeutic manipulation of the enteric flora with probiotics or other strategies may not be optimally realised until the composition and metabolic activities of the normal flora are better understood.

Type
Research Article
Copyright
Copyright © The Nutrition Society 2002

References

Akkermans, ADL, Zoetendal, EG, Favier, CF, Heilig, HGHJ, Akkermans-van Vliet, WM & de Vos, WM (2000) Temperature and denaturing gradient gel electrophoresis analysis of 16S rRNA from human faecal samples. Bioscience Microflora 19, 9398.Google Scholar
Atlas, RM (1999) Probiotics – snake oil for the new millennium? Environmental Microbiology 1, 375382.CrossRefGoogle ScholarPubMed
Bengmark, S (1998) Ecological control of the gastrointestinal tract. The role of probiotic flora. Gut 42, 27.Google Scholar
Berg, RD (1996) The indigenous gastrointestinal microflora. Trends in Microbiology 4, 430435.CrossRefGoogle ScholarPubMed
Berg, RD (1998) Probiotics, prebiotics or conbiotics? Trends in Microbiology 6, 8992.CrossRefGoogle ScholarPubMed
Blumberg, RS, Saubermann, LJ & Strober, W (1999) Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Current Opinion in Immunology 11, 648656.Google Scholar
Bocci, V (1992) The neglected organ: bacterial flora has a crucial immunostimulatory role. Perspectives in Biological Medicine 35, 251260.CrossRefGoogle Scholar
Cong, Y, Brandwein, SL, McCabe, RP, Lazenby, A, Birkenmeier, EH, Sundberg, JP & Elson, CO (1998) CD4+ T-cells reactive to enteric bacterial antigens in spontaneously colitic C3H/HeJBir mice: increased T-helper cell type 1 response and ability to transfer disease. Journal of Experimental Medicine 187, 855864.Google Scholar
D'Haens, GR, Geboes, K, Peeters, M, Baert, F, Penninckx, F & Rutgeerts, P (1998) Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum. Gastroenterology 114, 262267.Google Scholar
Diplock, AT, Aggett, P, Ashwell, M, Bornet, F, Fern, E & Roberfroid, M (1999) Scientific concepts of functional food science in Europe: consensus document. British Journal of Nutrition 81, Suppl. 1, 128.Google Scholar
Dugas, B, Mercenier, A, Lenoir-Wijnkoop, I, Arnaud, C, Dugas, N & Postaire, E (1999) Immunity and probiotics. Immunology Today 20, 387390.Google Scholar
Dunne, C, Murphy, L, Flynn, S, O'Mahony, L, O'Halloran, S, Feeney, M, Morrissey, D, Thornton, G, Fitzgerald, G, Daly, C, Kiely, B, Quigley, EMM, O'Sullivan, GC, Shanahan, F & Collins, JK (1999) Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie von Leeuwenhoek 76, 279292.Google Scholar
Dunne, C, O'Mahony, L, Murphy, L, Thornton, G, Morrissey, D, O'Halloran, S, Feeney, M, Flynn, S, Fitzgerald, G, Daly, C, Kiely, B, O'Sullivan, GC, Shanahan, F & Collins, JK (2001) In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. American Journal of Clinical Nutrition 73, Suppl. 2, 386S392S.Google Scholar
Elson, CO, Sartor, RB, Tennyson, GS & Riddell, RH (1995) Experimental models of inflammatory bowel disease. Gastroenterology 109, 13441367.Google Scholar
Erman, J & Fathman, CG (2001) Autoimmune diseases: genes, bugs and failed regulation. Nature Immunology 2, 759761.CrossRefGoogle Scholar
Feagan, B (1997) Antibiotics are not effective therapy for Crohn's disease (time to remove the rose-coloured glasses). Inflammatory Bowel Diseases 3, 314317.CrossRefGoogle Scholar
Fuss, IJ & Strober, W (1998) Animal models of inflammatory bowel disease: insights into the immunopathogenesis of Crohn's disease and ulcerative colitis. Current Opinion in Gastroenterology 14, 476482.Google Scholar
Gionchietti, P, Rizzello, F, Venturi, A, Brigidi, P, Matteuzzi, D, Bazzocchi, G, Poggioli, G, Migioli, M & Campieri, M (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double blind, placebo-controlled trial. Gastroenterology 119, 305309.Google Scholar
Hamilton-Miller, JMT (2001) A review of clinical trials of probiotics in the management of inflammatory bowel disease. Infectious Disease Reviews 3, 8387.Google Scholar
Harper, PH, Lee, ECG, Kettlewell, MGW, Bennett, MK & Jewell, DP (1985) Role of the faecal stream in the maintenance of Crohn's colitis. Gut 26, 279284.Google Scholar
Hooper, LV, Wong, MH, Thelin, A, Hansson, L, Falk, PG & Gordon, JI (2001) Molecular analysis of commensal host–microbial relationships in the intestine. Science 291, 881884.Google Scholar
Isolauri, E, Majamaa, H, Arvola, T, Rantala, I, Virtanen, E & Arvilommi, H (1993) Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in suckling rats. Gastroenterology 105, 16431650.Google Scholar
Konings, WN, Kok, J, Kuipers, OP & Poolman, B (2000) Lactic acid bacteria: the bugs of the new millennium. Current Opinion in Microbiology 3, 276282.Google Scholar
Kronenberg, M & Cheroutre, H (2000) Do mucosal T-cells prevent intestinal inflammation? Gastroenterology 118, 974977.CrossRefGoogle ScholarPubMed
Kruis, W, Schütz, E, Fric, P, Fixa, B, Judmaiers, G & Stolte, M (1997) Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Alimentary Pharmacology and Therapeutics 11, 853858.CrossRefGoogle ScholarPubMed
Leenhouts, K, Buist, G & Kok, J (1999) Anchoring of proteins to lactic acid bacteria. Antonie von Leeuwenhoek 76, 367376.CrossRefGoogle ScholarPubMed
McNaught, CE & Mac Fie, J (2001) Probiotics in clinical practice: a critical review of the evidence. Nutrition Research 21, 343353.CrossRefGoogle Scholar
MacPherson, A, Khoo, UY, Forgacs, I, Philpott-Howard, J & Bjarnason, I (1996) Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut 38, 365375.CrossRefGoogle ScholarPubMed
Madsen, KL, Doyle, JS, Jewell, LD, Tavernini, MM & Fedorak, RN (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116, 11071114.CrossRefGoogle ScholarPubMed
Midtvedt, T (1999) Microbial functional activities. In Intestinal Microflora Nestle Nutrition Workshop Series 42, pp. 7996 [Hanson, LA and Yolken, RH, editors]. Philadelphia: Lippincott-Raven.Google Scholar
Murch, SH (2001) Toll of allergy reduced by probiotics. Lancet 357, 10571059.Google Scholar
Neish, AS, Gewirtz, AT, Zeng, H, Young, AN, Hobert, ME, Karmali, V, Rao, AS & Madara, JL (2000) Prokaryotic regulation of epithelial responses by inhibition of IκB-α ubiquitination. Science 289, 15601563.Google Scholar
O'Mahony, L, Feeney, M, O'Halloran, S, Murphy, L, Kiely, B, Fitzgibbon, J, Lee, G, O'Sullivan, G, Shanahan, F & Collins, JK (2001) Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Alimentary Pharmacology and Therapeutics 15, 12191225.Google Scholar
Powrie, F (1995) T-cells in inflammatory bowel disease: protective and pathogenic roles. Immunity 3, 171174.CrossRefGoogle ScholarPubMed
Present, DH (1998) Ciprofloxacin as a treatment for ulcerative colitis – not yet. Gastroenterology 115, 12891291.Google Scholar
Rembacken, BJ, Snelling, AM, Hawkey, PM, Chalmers, DM & Axon, ATR (1999) Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 354, 635639.CrossRefGoogle ScholarPubMed
Rook, GA & Stanford, JL (1998) Give us this day our daily germs. Immunology Today 19, 113116.Google Scholar
Shanahan, F (2000) Probiotics and inflammatory bowel disease: is there a scientific rationale? Inflammatory Bowel Disease 6, 107115.CrossRefGoogle Scholar
Shanahan, F (2001) Inflammatory bowel disease: immunodiagnostics, immunotherapeutic, and ecotherapeutics. Gastroenterology 120, 622635.CrossRefGoogle ScholarPubMed
Shanahan, F & McCarthy, J (2000) Functional foods and probiotics: time for gastroenterologists to embrace the concept. Current Gastroenterology Reports 2, 345346.CrossRefGoogle ScholarPubMed
Steidler, L, Hans, W, Schotte, L, Neirynck, S, Obermeier, F, Falk, W, Fiers, W & Remaut, E (2000) Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289, 13521355.CrossRefGoogle ScholarPubMed
Vaughan, EE, Schut, F, Hellig, HGHJ, Zoetendal, EG, de Vos, WM & Akkermans, ADL (2000) A molecular view of the intestinal ecosystem. Current Issues in Intestinal Microbiology 1, 112.Google ScholarPubMed
Zubillaga, M, Weill, R, Postaire, E, Goldman, C, Caro, R, & Boccio, J (2001) Effect of probiotics and functional foods and their use in different diseases. Nutrition Research 21, 569579.CrossRefGoogle Scholar