Recent evidence suggests that the composition of colonic flora plays a role in intestinal inflammation in inflammatory bowel disease (IBO). This review examines the evidence that altering the concentrations of colonic bacteria might benefit patients with this condition. (Journal of Parenteral and Enteral Nutrition24:189-195, 2000)
Get full access to this article
View all access options for this article.
References
1.
Sartor RB: Microbial factors in the pathogenesis of Crohn's disease, ulcerative colitis and experimental intestinal inflammation. IN Inflammatory Bowel Disease, Kirsner JB, Shorter RG (eds). Williams and Wilkins , Baltimore, 1995, pp 96-124
2.
Sartor RB: Review article: Role of the enteric microflora in the pathogenesis of intestinal inflammation and arthritis. Aliment Pharmacol Ther11:17-23, 1997
3.
Harper PH, Truelove SC, Lee ECG, et al: Split ileostomy and ileocolostomy for Crohn's disease of the colon and ulcerative colitis: A twenty year survey. Gut23:106-113, 1983
4.
D'Haens GR, Geboes K., Peeters M., et al: Early lesions of recurrent Crohn's disease caused by infusion of intestinal contents in excluded ileum. Gastroenterology114:262-267, 1998
5.
Sundberg JP, Elson CO, Bedigian H., et al: Spontaneous, heritable colitis in a new substrain of C3H/HeJ mice. Gastroenterology107:1726-1735, 1994
6.
Taurog JD, Richardson JA, Croft JT, et al: The germfree state prevents development of gut and joint inflammatory disease of HLA-B27 transgenic rats. J Exp Med180:2359-2364, 1994
7.
Sadlack B., Merz H., Schorle H., et al: Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell75:253-261, 1993
8.
Kühn R., Löhler J., Rennick D., et al: Interleukin-10-deficient mice develop chronic enterocolitis . Cell75:263-274, 1993
9.
Duchmann R., Kaiser I., Hermann E., et al: Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease. Clin Exp Immunol102:448-455, 1995
10.
MacDonald TT : Breakdown of tolerance to the intestinal bacterial flora in inflammatory bowel disease (IBD). Clin Exp Immunol102:445-447, 1995
11.
Macpherson A., Khoo UY, Forgacs I., et al: Mucosal antibodies in inflammatory bowel disease are directed against intestinal bacteria. Gut38:365-375, 1996
12.
Strober W., Kelsall B., Marth T.: Oral Tolerance. J Clin Immunol18:1-30, 1998
13.
Brown WR: Listeria: The latest putative pathogenic micro-organism in Crohn's disease . Gastroenterology108:1589-1590, 1995
14.
Thomas GAO , Swift GL, Green JT, et al: Controlled trial of antituberculous chemotherapy in Crohn's disease: A five year follow up study. Gut42:497-500, 1998
15.
Warren JB, Rees HC, Cox TM: Remission of Crohn's disease with tuberculosis chemotherapy. N Engl J Med314:182, 1986
16.
Schultz MG, Reider HLHersh T. et al: Remission of Crohn's disease with anti-mycobacterial chemotherapy . Lancetii:1391-1392, 1987
17.
Picciotto A.Gesu GP, Schito GC et al: Antimycobacterial chemotherapy in 2 cases of inflammatory bowel disease. Lancetii: 536-537. 1998
18.
Elliot PR, Burnham WRBerghouse LM, et al: Sulphadoxinepyrimethamine therapy in Crohn's disease. Digestion23:132-134, 1982
19.
Swift GL, Srivastava ED, Stone R., et al: Controlled trial of anti-tuberculous chemotherapy for two years in Crohn's disease. Gut35:363-368, 1994
20.
Graham DY, Al-Assi MT, Robinson M.: Prolonged remission in Crohn's disease following therapy for Mycobacterium paratuberculosis (Abstr). Gastroenterology108:A826, 1995
21.
Seneca H., Henderson E.: Normal intestinal bacteria in ulcerative colitis. Gastroenterology15:34-39, 1950
22.
Keighley MRB , Arabi Y., Dimock F., et al: Influence of inflammatory bowel disease on the intestinal microflora. Gut19:1099-1104, 1978
23.
Dickinson RJ , Varian SA, Axon ATR, et al: Increased incidence of faecal coliforms with in-vitro adhesive and invasive properties in patients with ulcerative colitis. Gut21:787-792, 1980
24.
Bourgault A-M. , Rosenblatt JE, Fitzgerald RH: Peptococcus magnus: a significant human pathogen . Ann Intern Med93:244-248, 1980
25.
Wensinck F. , Custers-van Lieshout LMC, Poppelaars-Kustermans PAJ, et al: The faecal flora of patients with Crohn's disease. J Hyg87:1-12, 1981
26.
Ambrose NS, Young D., Burdon DW, et al: Changes in intestinal flora in Crohn's disease. Br J Surg69:681, 1982
27.
Giaffer MH, Holdsworth CD, Duerden BI: The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol35:238-243, 1991
28.
Favier C., Neut C., Mizon C., et al: Fecal β-D-galactosidase production and bifidobacteria are decreased in Crohn's disease. Dig Dis Sci42:817-822, 1997
29.
Gorbach SL, Nahas L., Plaut AG, et al: Studies of intestinal microflora. V. Fecal microbial ecology in ulcerative colitis and regional enteritis: Relationship to severity of disease and chemotherapy. Gastroenterology54:575-587, 1968
Cartun RW, Van Kruiningen HJ, Pedersen CA, et al: An immunocyctochemical search for infectious agents in Crohn's disease. Mod Pathol6:212-219, 1993
32.
Turunen U., Färkkilä M., Valtonen V., et al: Long-term outcome of ciprofloxacin treatment in severe perianal or fistulous Crohn's disease (Abstr). Gastroenterology104:A793, 1993
33.
Silva M., Jacobus NV, Deneke C., et al: Antimicrobial substance from a human lactobacillus strain. Antimicrob Agents Chemother31:1231-1233, 1987
34.
Fernandes CF , Shahami KM, Am MA: Therapeutic role of dietary lactobacilli and lactobacilli fermented dairy products. FEMS Microbiol Rev46:343-356, 1987
35.
Salminen S., Deighton M., Gorbach SL: Lactic acid bacteria in health and disease. IN Lactic Acid Bacteria, Salminen S, von Wright A (eds). Dekker, New York, 1993, pp 531-537
36.
van der Waiij D.: Colonisation resistance of the digestive tract: Mechanisms and clinical consequences. Die Nahrung31:507-517,1987
37.
Greenberg GR : Nutritional management of inflammatory bowel disease. Semin Gast Dis4:69-85, 1993
38.
Wellmann W. , Fink PC, Schmidt FW: Whole-gut irrigation as anti-endotoxinaemic therapy in inflammatory bowel disease. Hepatogastroenterology31:91-93. 1988
39.
Prantera C. , Scribano MLBerto E. et al: Antibiotic use in Crohn's disease. Why and how?Biodrugs8:293-306. 1997
40.
Krook A.Lindstrom B., Kjelland J. et al: Relation between concentrations of metronidazole and Bacteroides spp. in faeces of patients with Crohn's disease and healthy individuals. J Clin Pathol34:645-650, 1981
41.
Ursing B., Alm T.Barany F. et al: A comparative study of metronidazole and sulfasalazine for active Crohn's disease: The cooperative Crohn's disease study in Sweden: II. Result . Gastroenterology83:550-562, 1982
42.
Sutherland L. , Singleton L., Sessions J., et al: Double blind, placebo controlled trial of metronidazole in Crohn's disease. Gut32:1071-1075, 1991
43.
Prantera C., Zannoni F., Scribano ML, et al: An antibiotic regimen for the treatment of active Crohn's disease: A randomised, controlled clinical trial of metronidazole plus ciprofloxacin . Am J Gastroenterol91:328-332, 1996
44.
Saverymuttu S. , Hodgson HJF, Chadwick VS: Controlled trial comparing prednisolone with an elemental diet plus non-absorbable antibiotics in active Crohn's disease . Gut26:994-998, 1985
45.
Blichfeldt P. , Blomhoff JP, Myhre E., et al: Metronidazole in Crohn's disease. A double blind cross-over clinical trial. Scand J Gastroenterol13:123-127, 1978
46.
Ambrose NS, Allan RN, Keighley MRB, et al: Antibiotic therapy for treatment in relapse of intestinal Crohn's disease. Dis Colon Rectum28:81-85, 1985
47.
Burke DA, Axon ATR, Clayden SA, et al: The efficacy of tobramycin in the treatment of ulcerative colitis . Aliment Pharmacol Ther4:123-129, 1990
48.
Lobo AJ, Burke DA, Sobala GM, et al: Oral tobramycin in ulcerative colitis: Effect on the maintenance of remission. Aliment Pharmacol Ther7:155-158, 1993
49.
Mantzaris GJ , Hatzis A., Konogiannis P., et al: Intravenous tobramycin and metronidazole as an adjunct to corticosteroids in acute, severe ulcerative colitis. Am J Gastroenterol89:43-46, 1994
50.
Dickinson RJ , O'Connor HJ, Pinder I., et al: Double blind controlled trial of oral vancomycin as adjunctive treatment in acute exacerbations of idiopathic colitis . Gut26:1380-1384, 1985
51.
Rutgeerts P. , Peeters M., Hiele M., et al: A placebo controlled trial of metronidazole for recurrence prevention of Crohn's disease after resection of the terminal ileum. Gastroenterology102: A688, 1992
52.
Rutgeerts P. , Hiele M., Geboes K., et al: Controlled trial of metronidazole treatment for prevention of Crohn's recurrence after ileal resection. Gastroenterology108:1617-1621, 1995
53.
Bernstein LH , Frank MS, Brandt LJ, et al: Healing of perineal Crohn's disease with metronidazole. Gastroenterology79:357-365, 1980
54.
Brandt LJ, Bernstein LH, Boley SJ, et al: Metronidazole therapy for perineal Crohn's disease: A follow-up study. Gastroenterology83:383-387, 1982
55.
Jakobovits J., Schuster MM: Metronidazole therapy for Crohn's disease and associated fistulae. Am J Gastroenterol79:533-540, 1984
56.
Colombel J-F. , Lémann M., Cassagnou M., et al: A controlled trial comparing ciprofloxacin with mesalazine for the treatment of active Crohn's disease. Am J Gastro94:674-678, 1999
57.
Turunen UM, Färkkilä MA, Hakala K., et al: Long-term treatment of ulcerative colitis with ciprofloxacin: A prospective, double-blind, placebo-controlled study. Gastroenterology115: 1072-1078, 1998
58.
Standing Medical Advisory Committee Sub-Group on Antimicrobial resistance: The path of least resistance. Department of Health, 1988
59.
Gibson GR, Roberfroid MB: Dietary modulation of the human colonic microbiota introducing the concept of prebiotics. J Nutr125:1401-1412, 1995
60.
Royall D., Wolevar TMS, Jeejeebhoy KN: Clinical significance of colonic fermentation. Am J Gastroenterology85:1307-1312, 1990
61.
Cummings JH , McFarlane GT: A Review. The control and consequences of bacterial fermentation in the human colon. J Appl Bacteriol70:443-459, 1991
62.
Spiegel JE, Rose R., Karabell P., et al: Safety and benefits of fructo-oligosaccharides as food ingredients . Food Technol48:85-89, 1994
63.
Muller M., Lier D.: Fermentation of fructans by epiphytic lactic acid bacteria. J Appl Bacteriol76:406-411, 1994
64.
Mitsuoka T. , Hidaka H., Eida T.: Effect of Fructo-oligosaccharides on intestinal microflora. Nahrung5-6:421-436, 1987
65.
Umemoto Y., Tanimura H., Ishimoto K., et al: Trial of a new fructo-oligosaccharide therapy against IBD (Abstr) . Gastroenterology114:A1102, 1998
66.
Fujita K., Hara K., Sakai S., et al: Effect of 4G-66-D-Galactosyl-sucrose (lactosucrose) on intestinal flora and its digestibility in humans [in Japanese with English abstract] . Denpun Kagaku38:249-255, 1991
67.
Yoneyama M. , Mandai T., Aga H., et al: Effects of 4G-66-D-galactosylsucrose (lactosucrose) intake of intestinal flora in healthy humans [in Japanese with English abstract]. J Jpn Soc Nutr Food Sci45:101-107, 1992
68.
Iwagaki H., Fuchimito S., Matsubara N., et al: The influence of lactosucrose (LS-98) on the intestinal microflora of patients with resected colon [in Japanese with English abstract]. J Jpn Soc Colo-Proctol44:462-480, 1991
69.
Iwagaki H., Hizuta A., Kimura Y., et al: The effects of oral lactosucrose administration on the intestinal microflora of a patient undergoing total colectomy for familial polyposis coli [in Japanese with English abstract]. J Jpn Soc Colo-Proctol46:194-197, 1993
70.
Iwagaki H., Hizuta A., Kimura Y., et al: Preoperative lactosucrose administration and its effect on postoperative serum endotoxin levels [in Japanese with English abstract]. J Jpn Soc Clin Surg54:553-558, 1993
71.
Teramoto F. , Rokutan K., Kawakami Y., et al: Effect of 4G-66-D-galactosylsucrose (lactosucrose) on fecal microflora in patients with chronic inflammatory bowel disease. J Gastroenterol31:33-39, 1996
72.
Buhrer M., Bircher J.: Lactitol, a potential second generation disaccharide drug for the treatment of portal-systemic encephalopathy. IN Hepatic Encephalopathy in Chronic Liver Failure, Capocaccia L, Fischer JE, Rossi-Fanelli F (eds). Plenum Press, New York , London, 1984, pp 275-278
73.
Avery GS, Davies EF, Bragden RN: Lactulose: A review of its therapeutic and and pharmacological properties with particular reference to human metabolism and its mode of action in portal systemic encephalopathy. Drugs4:7-48, 1972
74.
de Groote GH , Schalm SW, Batavier P., et al: Incidence of endotoxaemia in pig with ischaemic hepatic necrosis treated by haemodialysis . Hepatogastroenterol30:240-242, 1983
75.
Pain JA, Bailey MB: Experimental and clinical study of lactulose in obstructive jaundice . Br J Surg73:776-778, 1985
76.
Wang X.: Comparative Aspects of Carbohydrate Fermentation by Colonic Bacteria , University of Cambridge, 1987. PhD thesis
77.
Gardiner KR , Anderson NH, McCaigue MD, et al: Systemic endotoxaemia in experimental colitis and following treatment with oral lactulose (Abstr) . Br J Surg77:1421A, 1990
78.
Liao W., Cui XS, Jin XY: The effect of lactulose on the biological activities of endotoxin . Chin J Microbiol Immunol11:108, 1991
79.
Liao W., Cui XS, Jin XY, et al: Lactulose-A potential drug for the treatment of inflammatory bowel disease. Med Hypoth43:234-238, 1994
80.
Fuller R.: Probiotics in man and animals. J Appl Bacteriol66:365-378, 1989
81.
Metha AM, Patel KA, Dave PJ: Isolation and purification of an inhibitory protein from Lactobacillus acidophilus AC1. Microbios37:37-43, 1983
82.
Atrih A., Rekhif N., Bichel M., et al: Detection of bacteriocins produced by Lactobacillus plantarum strains isolated from different foods. Microbios75:117-123, 1993
83.
Bernet-Camard M-F., Lievin V., Brassart D., et al: The human Lactobacillus acidophilus strain LA1 secretes a non bacteriocin antibacterial substance(s) active in vitro and in vivo. Appl Environ Microbiol63:2747-2753, 1997
84.
Jónsson S., Clausen E., Raa J.: Amino acid degradation by a Lactobacillus plantarum strain from fish . Syst Appl Microbiol4:148-154, 1993
85.
Wright CE, Rees DD, Moncada S.: Protective and pathological role of nitric oxide in endotoxin shock . Cardiovasc Res26:48-57, 1992
86.
Duncan C., Dougall H., Johnston P., et al: Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nat Med1:546-551, 1995
87.
Falkow S., Isberg RR, Portney DA: The interaction of bacteria with mammalian cells. Annu Rev Cell Biology8:333-363, 1992
88.
Elo S., Saxelin M., Salminen S.: Attachment of Lactobacillus casei strain GG to human colon carcinoma cell line Caco-2: Comparison with other dairy strains. Lett Appl Microbiol13:154-156, 1991
89.
Coconnier MH , Bernet MF, Kerneis S., et al: Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by L. acidophilus strain LB decreases bacterial invasion . FEMS Microbiol Lett110:299-306, 1993
90.
Bernet M.-F, Brassart D., Neeser JR, et al: Lactobacillus acidophilus LA1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut35:483-489, 1994
91.
Scheppach W. : Effects of short chain fatty acids on gut morphology and function. Gut1 (Suppl):S35-38, 1994
92.
Scheppach W. , Sommer H., Kirchner T., et al: Effect of Butyrate enemas on the colonic mucosa in distal ulcerative colitis. Gastroenterology103:51-56, 1992
93.
Steinhart AH , Brzezinski A., Baker JP: Treatment of refractory ulcerative proctosigmoiditis with butyrate enemas. Am J Gastroenterol89:179-183, 1994
94.
Perdigon G. , Alvarez S., Rachid M., et al: Immune system stimulation by probiotics . J Dairy Sci78:1597-1606, 1995
95.
Schiffrin EJ , Rochat F., Link-Amster H., et al: Immune modulation of human blood cells following the ingestion of lactic acid bacteria. J Dairy Sci78:491-497, 1995
96.
Havenaar R., Ten Brink B., Huis in't Veld JHJ: Selection of strains for probiotic use. IN Probiotics: The Scientific Basis. Fuller R (ed). Chapman & Hall, London, 1992 , pp 209-224
97.
Isolauri E. , Majamaa H., Arvola T., et al: Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in sucklings. Gastroenterology105:1643-1650, 1993
98.
Barrow PA, Brooker BE, Fuller R., et al: The attachment of bacteria to gastric epithelium of the pig and its importance for the microecology of the intestine. J Appl Bacteriol48:147-154, 1980
99.
Fabia R., Ar'rajab A., Johannson M-L., et al: The effect of exogenous administration of Lactobacillus reuteri R2LC and oat fiber on acetic acid-induced colitis in the rat. Scand J Gastroenterol28:155-162, 1993
100.
Camarri E. , Belvisi A., Guidoni G., et al: A double-blind comparison of two different treatments for acute enteritis in adults. Chemotherapy27:466-470, 1981
101.
Chapoy P.: Treatment of acute infantile diarrhoea: Controlled trial of Saccharomyces boulardii. Ann Pediatr32:561-563, 1985
102.
Isolauri E. , Juntunen M., Rautanen T., et al: A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhoea in children. Pediatrics88:90-97, 1991
103.
Nakaya R.: Role of bifidobacterium in enteric infection. Bifidobacteria Microflora3:3-9, 1984
104.
Corthier G. , Dubos F., Raibaud P.: Modulation of cytotoxin production by Clostridium difficle in the intestinal tracts of gnotobiotic mice inoculated with various human intestinal bacteria. Appl Environ Microbiol49:250-252, 1985
105.
Antoine JM: Validation of health attributes of yogurt. IN Yoghurt: Nutritional and Health Properties. Chandra RC (ed). McLean VA, National Yoghurt Association , 1989, pp 233-240
106.
Perdigon G.Alvarez S., Nader de Macias ME et al: The oral administration of lactic acid bacteria increases the mucosal intestinal immunity in response to enteropathogens. J Food Protect53:404-410. 1990
107.
Juven BJ, Meinersmann RJStern NJ: Antagonistic effects of lactobacilli and pediococci to control intestinal colonisation by human enteropathogens in live poultry . J Appl Bacteriol70:95-103. 1991
108.
Borgia M., Sepe N., Brancato V. et al: A controlled clinical study on Streptococcus faecium preparation for the prevention of side reactions during long-term antibiotic treatments . Curr Ther Res31:265-271, 1982
109.
Surawicz CM , Elmer GW, Speelman P., et al: Prevention of antibiotic-associated diarrhoea by SaccharoniN,ces boulardii: A prospective study. Gastroenterology96:981-988, 1989
110.
Black FT, Anderson PL, Orskov J., et al: Prophylactic efficacy of lactobacilli on traveller's diarrhoea . Travel Med7:333-335, 1989
111.
Caldrini de Bustos MI, Schiffrin EJ, Ogawa de Furuya K., et al: Prevention of carrageenan-induced ulcerative colitis in the guinea pig by serum of bovine colostrum. Medicina47:273-277, 1987
112.
Madsen KL, Doyle JSG, Jewell LD, Tavernini MM, Fedorak RN: Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice . Gastroenterology116:1107-1114, 1999
113.
Schultz M. , Veltkamp C., Dieleman LA, et al: Continuous feeding of Lactobacillus Plantarum attenuates established colitis in interleukin-10 deficient mice (Abstr). Gastroenterology114:A1081, 1998
114.
Malin M., Suomalainen H., Saxelin M., et al: Promotion of IgA immune response in patients with Crohn's disease by oral bacteriotherapy with lactobacillus GG. Ann Nutr Metab40:137-145, 1996
115.
Malchow HA : Crohn's disease and Escherichia coli. A new approach in therapy to maintain remission of colonic Crohn's disease. J Clin Gastroenterol25:653-658, 1997
116.
Kordecki H. , Niedzielin K.: New conception in the treatment of ulcerative colitis: Probiotics as a modification of the microflora of the colon (Abstr) . IN Proceedings of Falk Symposium No. 105, 1998, 45
117.
Venturi A. , Gionchetti P., Rizzello F., et al: Colonisation of patients with ulcerative colitis in remission by a new probiotic preparation (Abstr). Gastroenterology114:A1109, 1998
118.
Gionchetti P., Rizzello F., Venturi A., et al: Maintenance treatment of chronic pouchitis: A randomised placebo-controlled trial with a new probiotic preparation (Abstr) . Gastroenterology114:A985, 1998
119.
Kruis W., Schutz E., Fric P., et al: Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther11:853-858, 1997
120.
Rembracken BJ, Snelling AM, Hawkey PM, et al: Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: A randomised trial. Lancet354:635-639; 1999