Effect of ursodeoxycholic acid use on the risk of colorectal neoplasia in patients with primary sclerosing cholangitis and inflammatory bowel disease: A systematic review and meta-analysis

Inflammatory Bowel Diseases

Volumn 19, Issue 8, 2013, Pages 1631-1638

  Singh, Siddharth ^a   Khanna, Sahil ^a   Pardi, Darrell S ^a   Loftus Jr , Edward V ^a   Talwalkar, Jayant A ^a  

^a MAYO CLINIC   (United States)

Author keywords

Chemoprevention; Dysplasia; Inflammatory bowel disease; Primary sclerosing cholangitis

Indexed keywords

URSODEOXYCHOLIC ACID;

ARTICLE; CANCER GRADING; CANCER RISK; CHEMOPROPHYLAXIS; COLORECTAL TUMOR; DISEASE ASSOCIATION; DRUG MEGADOSE; ENTERITIS; HUMAN; LOW DRUG DOSE; META ANALYSIS; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; QUALITY CONTROL; RISK FACTOR; RISK REDUCTION; SYSTEMATIC REVIEW;

CHOLAGOGUES AND CHOLERETICS; CHOLANGITIS, SCLEROSING; COLORECTAL NEOPLASMS; HUMANS; INFLAMMATORY BOWEL DISEASES; META-ANALYSIS AS TOPIC; PROGNOSIS; URSODEOXYCHOLIC ACID;

EID: 84882451856     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0b013e318286fa61     Document Type: Article

References (57)

1. Ferlay J, Shin HR, Bray F, et al. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127:2893-2917.
2. Bernstein CN, Blanchard JF, Kliewer E, et al. Cancer risk in patients with inflammatory bowel disease: a population-based study. Cancer. 2001;91: 854-862.
3. Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol. 2012;10:639-645.
4. Loftus EV Jr. Epidemiology and risk factors for colorectal dysplasia and cancer in ulcerative colitis. Gastroenterol Clin North Am. 2006;35:517-531.
5. Jess T, Simonsen J, Jorgensen KT, et al. Decreasing risk of colorectal cancer in patients with inflammatory bowel disease over 30 years. Gastroenterology. 2012;143:375-381 e371.
6. Soetikno RM, Lin OS, Heidenreich PA, et al. Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: a meta-analysis. Gastrointest Endosc. 2002;56:48-54.
7. Fearon ER, Vogelstein B. A genetic model for colorectal tumorigenesis. Cell. 1990;61:759-767.
8. Ullman TA, Itzkowitz SH. Intestinal inflammation and cancer. Gastroenterology. 2011;140:1807-1816.
9. Leedham SJ, Graham TA, Oukrif D, et al. Clonality, founder mutations, and field cancerization in human ulcerative colitis-associated neoplasia. Gastroenterology. 2009;136:542-550 e546.
10. Ochsenkuhn T, Bayerdorffer E, Meining A, et al. Colonic mucosal proliferation is related to serum deoxycholic acid levels. Cancer. 1999;85: 1664-1669.
11. Bayerdorffer E, Mannes GA, Richter WO, et al. Increased serum deoxycholic acid levels in men with colorectal adenomas. Gastroenterology. 1993;104:145-151.
12. Qiao D, Chen W, Stratagoules ED, et al. Bile acid-induced activation of activator protein-1 requires both extracellular signal-regulated kinase and protein kinase C signaling. J Biol Chem. 2000;275:15090-15098.
13. Martinez JD, Stratagoules ED, LaRue JM, et al. Different bile acids exhibit distinct biological effects: the tumor promoter deoxycholic acid induces apoptosis and the chemopreventive agent ursodeoxycholic acid inhibits cell proliferation. Nutr Cancer. 1998;31: 111-118.
14. Narisawa T, Fukaura Y, Terada K, et al. Prevention of N-methylnitrosourea-induced colon tumorigenesis by ursodeoxycholic acid in F344 rats. Jpn J Cancer Res. 1998;89:1009-1013.
15. Narisawa T, Fukaura Y, Terada K, et al. Inhibitory effects of ursodeoxycholic acid on N-methylnitrosourea-induced colon carcinogenesis and colonic mucosal telomerase activity in F344 rats. J Exp Clin Cancer Res. 1999;18:259-266.
16. Earnest DL, Holubec H, Wali RK, et al. Chemoprevention of azoxymethaneinduced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res. 1994;54:5071-5074.
17. Rigas B, Tsioulias GJ, Allan C, et al. The effect of bile acids and piroxicam on MHC antigen expression in rat colonocytes during colon cancer development. Immunology. 1994;83:319-323.
18. Ikegami T, Matsuzaki Y, Shoda J, et al. The chemopreventive role of ursodeoxycholic acid in azoxymethane-treated rats: suppressive effects on enhanced group II phospholipase A2 expression in colonic tissue. Cancer Lett. 1998;134:129-139.
19. Tung BY, Emond MJ, Haggitt RC, et al. Ursodiol use is associated with lower prevalence of colonic neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis. Ann Intern Med. 2001;134:89-95.
20. Pardi DS, Loftus EV Jr, Kremers WK, et al. Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis. Gastroenterology. 2003;124:889-893.
21. Wolf JM, Rybicki LA, Lashner BA. The impact of ursodeoxycholic acid on cancer, dysplasia and mortality in ulcerative colitis patients with primary sclerosing cholangitis. Aliment Pharmacol Ther. 2005;22:783-788.
22. Eaton JE, Silveira MG, Pardi DS, et al. High-dose ursodeoxycholic acid is associated with the development of colorectal neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis. Am J Gastroenterol. 2011;106:1638-1645.
23. Chapman R, Fevery J, Kalloo A, et al. Diagnosis and management of primary sclerosing cholangitis. Hepatology. 2010;51:660-678.
24. EASL. Clinical Practice Guidelines: management of cholestatic liver diseases. J Hepatol. 2009;51:237-267.
25. Higgins JP, Altman DG, Gotzsche PC, et al. The Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ. 2011;343: d5928.
26. Wells GA SB, O'Connell D, Peterson J, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available at: http://www.ohri.ca/programs/clinical-epidemiology/oxford. htm. Accessed May 5, 2012.
27. Der Simonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177-188.
28. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557-560.
29. Sterne JA, Sutton AJ, Ioannidis JP, et al. Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials. BMJ. 2011;343:d4002.
30. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283:2008-2012.
31. Lindstrom L, Boberg KM, Wikman O, et al. High dose ursodeoxycholic acid in primary sclerosing cholangitis does not prevent colorectal neoplasia. Aliment Pharmacol Ther. 2012;35:451-457.
32. Navaneethan U, Kochhar G, Venkatesh PG, et al. Duration and severity of primary sclerosing cholangitis is not associated with risk of neoplastic changes in the colon in patients with ulcerative colitis. Gastrointest Endosc. 2012;75:1045-1054 e1041.
33. Braden B, Halliday J, Aryasingha S, et al. Risk for colorectal neoplasia in patients with colonic Crohn's disease and concomitant primary sclerosing cholangitis. Clin Gastroenterol Hepatol. 2012;10:303-308.
34. Ullman TA, Croog V, Maratchi L, et al. Ursodeoxycholic acid for chemoprevention in ulcerative colitis and primary sclerosing cholangitis: a retrospective cohort study. Am J Gastroenterol. 2003;98:S258.
35. Rudolph G, Gotthardt D, Kloeters-Plachky P, et al. In PSC with dominant bile duct stenosis, IBD is associated with an increase of carcinomas and reduced survival. J Hepatol. 2010;53:313-317.
36. Rudolph G, Gotthardt DN, Kloeters-Plachky P, et al. In PSC with colitis treated with UDCA, most colonic carcinomas develop in the first years after the start of treatment. Dig Dis Sci. 2011;56:3624-3630.
37. Sokol H, Cosnes J, Chazouilleres O, et al. Disease activity and cancer risk in inflammatory bowel disease associated with primary sclerosing cholangitis. W J Gastroenterol. 2008;14:3497-3503.
38. Claessen MMH, Lutgens M, van Buuren HR, et al. More right-sided IBDassociated colorectal cancer in patients with primary sclerosing cholangitis. Inflamm Bowel Dis. 2009;15:1331-1336.
39. Sjöqvist U, Tribukait B, Öst Å, et al. Ursodeoxycholic acid treatment in IBD-patients with colorectal dysplasia and/or DNA-aneuploidy: a prospective, double-blind, randomized controlled pilot study. Anticancer Res. 2004;24:3121-3127.
40. Shetty K, Rybicki L, Brzezinski A, et al. The risk for cancer or dysplasia in ulcerative colitis patients with primary sclerosing cholangitis. Am J Gastroenterol. 1999;94:1643-1649.
41. Alberts DS, Martinez ME, Hess LM, et al. Phase III trial of ursodeoxycholic acid to prevent colorectal adenoma recurrence. J Natl Cancer Inst. 2005;97:846-853.
42. Larson MV, McLeod RS, Beighley CM, et al. Ursodeoxycholic acid for the prevention of metachronous adenomatous colorectal polyps: The results of a randomized controlled trial. Am J Gastroenterol. 2002;97:S118-S118.
43. Serfaty L, De Leusse A, Rosmorduc O, et al. Ursodeoxycholic acid therapy and the risk of colorectal adenoma in patients with primary biliary cirrhosis: an observational study. Hepatology. 2003;38:203-209.
44. Riddell RH, Goldman H, Ransohoff DF, et al. Dysplasia in inflammatory bowel disease: standardized classification with provisional clinical applications. Hum Pathol. 1983;14:931-968.
45. Ashraf I, Choudhary A, Arif M, et al. Ursodeoxycholic acid in patients with ulcerative colitis and primary sclerosing cholangitis for prevention of colon cancer: a meta-analysis. Indian J Gastroenterol. 2012;31:69-74.
46. Hill MJ, Melville DM, Lennard-Jones JE, et al. Faecal bile acids, dysplasia, and carcinoma in ulcerative colitis. Lancet. 1987;2:185-186.
47. Batta AK, Salen G, Holubec H, et al. Enrichment of the more hydrophilic bile acid ursodeoxycholic acid in the fecal water-soluble fraction after feeding to rats with colon polyps. Cancer Res. 1998;58:1684-1687.
48. Wali RK, Frawley BP Jr, Hartmann S, et al. Mechanism of action of chemoprotective ursodeoxycholate in the azoxymethane model of rat colonic carcinogenesis: potential roles of protein kinase C-alpha, -beta II, and -zeta. Cancer Res. 1995;55:5257-5264.
49. Wali RK, Khare S, Tretiakova M, et al. Ursodeoxycholic acid and F(6)-D (3) inhibit aberrant crypt proliferation in the rat azoxymethane model of colon cancer: roles of cyclin D1 and E-cadherin. Cancer Epidemiol Biomarkers Prev. 2002;11:1653-1662.
50. Khare S, Cerda S, Wali RK, et al. Ursodeoxycholic acid inhibits Ras mutations, wild-type Ras activation, and cyclooxygenase-2 expression in colon cancer. Cancer Res. 2003;63:3517-3523.
51. Mitsuyoshi H, Nakashima T, Sumida Y, et al. Ursodeoxycholic acid protects hepatocytes against oxidative injury via induction of antioxidants. Biochem Biophys Res Commun. 1999;263:537-542.
52. Lindor KD. Ursodiol for primary sclerosing cholangitis. Mayo Primary Sclerosing Cholangitis-Ursodeoxycholic Acid Study Group. N Engl J Med. 1997;336:691-695.
53. Lindor KD, Kowdley KV, Luketic VA, et al. High-dose ursodeoxycholic acid for the treatment of primary sclerosing cholangitis. Hepatology. 2009;50:808-814.
54. Sinakos E, Marschall HU, Kowdley KV, et al. Bile acid changes after high-dose ursodeoxycholic acid treatment in primary sclerosing cholangitis: relation to disease progression. Hepatology. 2010;52:197-203.
55. Wertheim BC, Smith JW, Fang CM, et al. Risk modification of colorectal adenoma by CYP7A1 polymorphisms and the role of bile acid metabolism in carcinogenesis. Cancer Prev Res. 2012;5:197-204.
56. Thompson PA, Wertheim BC, Roe DJ, et al. Gender modifies the effect of ursodeoxycholic acid in a randomized controlled trial in colorectal adenoma patients. Cancer Prev Res. 2009;2:1023-1030.
57. Kornfeld D, Ekbom A, Ihre T. Is there an excess risk for colorectal cancer in patients with ulcerative colitis and concomitant primary sclerosing cholangitis? A population based study. Gut. 1997;41:522-525.