Probiotic Agents for Ulcerative Colitis: A Systematic Review_Chinese Journal of Evidence-Based Medicine

Authors：

WU Qiurong ¹ , ZHOU Jun ¹ , HE Jidong ¹ ,  WANG Yiping ² , YANG Xiurong ¹ , ZHANG Lan ¹

1. Department of Gastroenterology,The Second People Hospital of Ya’an,Ya’an 625000, China;2. Department of Gastroenterology, West China Hospital, Sichuan University, Chengdu 610041, China;

Corresponding author：

WANG Yiping, Email: wqr0835@163.com

Keywords：

Probiotic agents; Ulcerative colitis; Meta analysis; Systematic review; Randomized controlled trial

DOI：

10.7507/1672-2531.20080071

Video：

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Objective 　To evaluate the effectiveness and safety of probiotic agents for ulcerative colitis.
Methods 　We searched electronically the Cochrane Central Register of Controlled Trials (Issue 1, 2007), MEDLINE (1978 to 2007), EMBASE (1978 to 2007), OVID Database (1978 to 2007), Chinese Biological Medicine Database (CBM Disc) (1978 to 2007), CNKI (1979 to 2007), Chinese VIP Database (1989 to 2007) and Wanfang Database (1978 to 2007). We also checked the reference lists of retrieved articles and hand-searched 4 kinds of important journals to identify randomized controlled trials of probiotic agents for ulcerative colitis. Meta-analyses were conducted with The Cochrane Collaboration’s RevMan 4.2 software.
Results 　Thirteen trials involving 1146 patients were included. Meta-analyses showed that probiotic agents were not superior to aminosalicylates for the clinical remission rate (OR 0.93, 95% CI 0.53 to 1.66; P=0.82); but the combination of probiotic agents and aminosalicylates were superior to aminosalicylates alone (OR 2.69, 95% CI 1.57 to 4.61; P=0.0003). In terms of the clinical relapse, the rate for probiotic agents was superior to that for placebo (OR 0.03, 95% CI 0.00 to 0.15; P lt;0.0001); but not superior to aminosalicylates (OR 0.95, 95% CI 0.65 to 1.38; P=0.79). The combination of probiotic agents and aminosalicylates was not superior to aminosalicylates alone (OR 0.57, 95% CI 0.24 to 1.32; P=0.19). As for the incidence of adverse effects, probiotic agents were not superior to aminosalicylates (OR 0.85, 95% CI 0.43 to 1.70; P=0.65); and the combination of probiotic agents and aminosalicylates was not superior to aminosalicylates alone (OR 0.30, 95% CI 0.06 to 1.54; P=0.15).
Conclusion 　Probiotic agents are not superior to aminosalicylates based on the evidence in this review, but the combination of probiotic agents and aminosalicylates is superior to aminosalicylates alone in maintaining remission. Probiotic agents are superior to placebo but not superior to aminosalicylates, and the combination of probiotic agents and aminosalicylates is not superior to aminosalicylates alone in preventing relapse. Probiotic agents have good tolerability. However, all these findings should be interpreted with caution and more clinical trials are needed.

Citation： WU Qiurong,ZHOU Jun,HE Jidong,WANG Yiping,YANG Xiurong,ZHANG Lan. Probiotic Agents for Ulcerative Colitis: A Systematic Review. Chinese Journal of Evidence-Based Medicine, 2008, 08(5): 315-321. doi: 10.7507/1672-2531.20080071 Copy

1.	Fedorak RN, Madsen KL. Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis, 2004, 10(3): 286-299.
2.	Shanahan F. Probiotics and inflammatory bowel disease: is there a scientific rationale? Inflamm Bowel Dis, 2000, 6(2): 107-115.
3.	Guslandi M, Giollo P, Testoni PA. A pilot trial of Saccharomyces boulardii in ulcerative colitis. Eur J Gastroenterol Hapatol, 2003, 15(6): 697-698.
4.	Leong RW, Lau JY, Sung JJ. The epidemiology and phenotype of Crohn’s disease in the Chinese population. Inflamm Bowel Dis, 2004, 10(5): 646-651.
5.	Heriasm V, Koninkx JF, Vos JG, et al. Probiotic effects of Lactobacillus caseion DSS - induced ulcerative colitis in mice. Int J Food Microbiol, 2005, 103(2): 143-155.
6.	Venturi A, Gionchetti P, Rizzello F, et al. Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther, 1999, 13(9): 1103-1108.
7.	Cui HH, Chen CL, Wang JD, et al. Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J Gastroenterol, 2004, 10(10): 1521-1525.
8.	Kato K, Mizuno S, Umesaki Y, et al. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther, 2004, 20(9): 1133-1141.
9.	Hideki I, Ikuko A, Yoshinori U, et al. Randomized Controlled Trial of the Effect of Bifidobacteria-Fermented Milk on Ulcerative Colitis. Journal of the American College of Nutrition, 2002, 22(1): 56-63.
10.	Antonio T, Giovanni B, Gian Marco G, et al. Low-dose balsalazide plus a high-potency probiotic preparation is more effective than balsalazide alone or mesalazine in the treatment of acute mild-to-moderate ulcerative colitis. Med Sci Monit, 2004, 10(11): 126-131.
11.	Kruis W, Fric P, Pokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut, 2004, 53(11): 1617-1623.
12.	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 Ther, 1997, 23(11): 853-858.
13.	Furrie E, Macfarlane S, Kennedy A, et al. Synbiotic therapy (Bifidobacterium longum/Synergy 1)initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut, 2005, 54(9): 242-249.
14.	Rembacken BJ, Snelling AM, Hawkey PM, et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomized trial. Lancet, 1999, 35(4): 635-639.
15.	Zocco M A, ZileridavermeIL, Cremonini F, et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther, 2006, 23(11): 1567-1574.
16.	李国恩, 杨爱云, 谢明菊. 贝飞达治疗溃疡性结肠炎的疗效观察. 河南大学学报: 医学科学版, 2003, 22(3): 40.
17.	向军英, 冯迎春. 美常安联合柳氮磺吡啶治疗溃疡性结肠炎22例. 世界华人消化杂志, 2006, 14(17): 1742-1744.
18.	李松财, 曹春宇, 汤武亨. 联合应用美沙拉嗪和美常安胶囊治疗溃疡性结肠炎的临床观察. 现代中西医结合杂志, 2006, 15(7): 900-901.
19.	姚玉川, 王磊辉, 赵江华, 等. 贝飞达灌肠治疗溃疡性直肠炎的疗效. 中国微生态学志, 2005, 17(5): 378.
20.	Shanahan F. Probiotics and inflammatory bowel disease : from fads and fantasy to facts and future. Br J Nutr, 2002, 88(suppl 1): S5.
21.	McCarthy J, Mahony LO, Callaghan LO, et al. Double blind, placebo controlled trail of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut, 2003, 52(6): 975.
22.	Resta-Lenert S, Barrett KE. Live probiotics protect intestinal epithelial cell from the effects of Infection with enteroin-vasive Escherichia colis. Gut, 2003, 52(7): 988-997.
23.	Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology, 2001, 112(3): 580-591.

1. Fedorak RN, Madsen KL. Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis, 2004, 10(3): 286-299.
2. Shanahan F. Probiotics and inflammatory bowel disease: is there a scientific rationale? Inflamm Bowel Dis, 2000, 6(2): 107-115.
3. Guslandi M, Giollo P, Testoni PA. A pilot trial of Saccharomyces boulardii in ulcerative colitis. Eur J Gastroenterol Hapatol, 2003, 15(6): 697-698.
4. Leong RW, Lau JY, Sung JJ. The epidemiology and phenotype of Crohn’s disease in the Chinese population. Inflamm Bowel Dis, 2004, 10(5): 646-651.
5. Heriasm V, Koninkx JF, Vos JG, et al. Probiotic effects of Lactobacillus caseion DSS - induced ulcerative colitis in mice. Int J Food Microbiol, 2005, 103(2): 143-155.
6. Venturi A, Gionchetti P, Rizzello F, et al. Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther, 1999, 13(9): 1103-1108.
7. Cui HH, Chen CL, Wang JD, et al. Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J Gastroenterol, 2004, 10(10): 1521-1525.
8. Kato K, Mizuno S, Umesaki Y, et al. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther, 2004, 20(9): 1133-1141.
9. Hideki I, Ikuko A, Yoshinori U, et al. Randomized Controlled Trial of the Effect of Bifidobacteria-Fermented Milk on Ulcerative Colitis. Journal of the American College of Nutrition, 2002, 22(1): 56-63.
10. Antonio T, Giovanni B, Gian Marco G, et al. Low-dose balsalazide plus a high-potency probiotic preparation is more effective than balsalazide alone or mesalazine in the treatment of acute mild-to-moderate ulcerative colitis. Med Sci Monit, 2004, 10(11): 126-131.
11. Kruis W, Fric P, Pokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut, 2004, 53(11): 1617-1623.
12. 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 Ther, 1997, 23(11): 853-858.
13. Furrie E, Macfarlane S, Kennedy A, et al. Synbiotic therapy (Bifidobacterium longum/Synergy 1)initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut, 2005, 54(9): 242-249.
14. Rembacken BJ, Snelling AM, Hawkey PM, et al. Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomized trial. Lancet, 1999, 35(4): 635-639.
15. Zocco M A, ZileridavermeIL, Cremonini F, et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther, 2006, 23(11): 1567-1574.
16. 李国恩, 杨爱云, 谢明菊. 贝飞达治疗溃疡性结肠炎的疗效观察. 河南大学学报: 医学科学版, 2003, 22(3): 40.
17. 向军英, 冯迎春. 美常安联合柳氮磺吡啶治疗溃疡性结肠炎22例. 世界华人消化杂志, 2006, 14(17): 1742-1744.
18. 李松财, 曹春宇, 汤武亨. 联合应用美沙拉嗪和美常安胶囊治疗溃疡性结肠炎的临床观察. 现代中西医结合杂志, 2006, 15(7): 900-901.
19. 姚玉川, 王磊辉, 赵江华, 等. 贝飞达灌肠治疗溃疡性直肠炎的疗效. 中国微生态学志, 2005, 17(5): 378.
20. Shanahan F. Probiotics and inflammatory bowel disease : from fads and fantasy to facts and future. Br J Nutr, 2002, 88(suppl 1): S5.
21. McCarthy J, Mahony LO, Callaghan LO, et al. Double blind, placebo controlled trail of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut, 2003, 52(6): 975.
22. Resta-Lenert S, Barrett KE. Live probiotics protect intestinal epithelial cell from the effects of Infection with enteroin-vasive Escherichia colis. Gut, 2003, 52(7): 988-997.
23. Madsen K, Cornish A, Soper P, et al. Probiotic bacteria enhance murine and human intestinal epithelial barrier function. Gastroenterology, 2001, 112(3): 580-591.

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