Primary Sclerosing Cholangitis, Inflammatory Bowel Disease, and Colon Cancer

ABSTRACT

The prevalence of inflammatory bowel disease (IBD) in patients with PSC differs in various part of the world. Ulcerative colitis (UC) is most common, but 1 to 14% of all primary sclerosing cholangitis (PSC) patients have Crohn disease with colonic involvement. Many PSC patients without clinical symptoms of IBD have colonoscopic and histological findings compatible with IBD, and the subclinical phase may last several years before onset of symptoms of active colitis. The characteristics of UC in patients with PSC are different from those in UC patients without PSC. The colitis is usually substantial, the clinical course of the colitis is quiescent, and rectal sparing is common. Moreover, PSC patients with UC have a higher risk of developing colorectal dysplasia/carcinoma than UC patients without PSC. In patients having an ileal pelvic pouch with ileal anal anastomosis, PSC is a risk factor for development of pouchitis. It is important that all PSC patients with UC are included in colonoscopic surveillance programs.

Crohn disease - ulcerative colitis - colorectal dysplasia - colorectal carcinoma - and pouchitis

REFERENCES

• 1 Smith M, Loe S. Sclerosing cholangitis: review of recent case reports and associated diseases and four new cases.  Am J Surg. 1965;  110 239-246
• 2 Broomé U, Glaumann H, Hellers G et al.. Liver disease in ulcerative colitis: an epidemiological and follow up study in the county of Stockholm.  Gut. 1994;  35 84-89
• 3 Atkinson A J, Carroll W W. Sclerosing cholangitis, association with regional enteritis.  JAMA. 1964;  188 183-184
• 4 Fausa O, Schrumpf E, Elgjo K. Relationship of inflammatory bowel disease and primary sclerosing cholangitis.  Semin Liver Dis. 1991;  11 31-39
• 5 Broomé U, Glaumann H, Hultcrantz R. Liver histology and follow up of 68 patients with ulcerative colitis and normal liver function tests.  Gut. 1990;  31 468-471
• 6 Wiesner R H, LaRusso N F. Clinicopathologic features of the syndrome of primary sclerosing cholangitis.  Gastroenterology. 1980;  79 200-206
• 7 Aadland E, Schrumpf E, Fausa O et al.. Primary sclerosing cholangitis: a long-term follow-up study.  Scand J Gastroenterol. 1987;  22 655-664
• 8 Chapman R WG, Arborgh B AM, Rhodes J M et al.. Primary sclerosing cholangitis: a review of its clinical features, cholangiography and hepatic histology.  Gut. 1980;  21 870-877
• 9 Riley T R, Schoen R E, Lee R G, Rakela J. A case series of transplant recipients who despite immunosuppression developed inflammatory bowel disease.  Am J Gastroenterol. 1997;  92 279-282
• 10 Broomé U, Olsson R, Lööf L et al.. Natural history and prognostic factors in 305 Swedish patients with primary sclerosing cholangitis.  Gut. 1996;  38 610-615
• 11 Farrant J M, Hayllar K M, Wilkinson M L et al.. Natural history and prognostic variables in primary sclerosing cholangitis.  Gastroenterology. 1991;  100 1710-1717
• 12 Wiesner R, Grambsch P, Dickson R et al.. Primary sclerosing cholangitis: natural history, prognostic factors and survival analysis.  Hepatology. 1989;  10 430-436
• 13 Dickson E R, Murtaugh P A, Wiesner R H et al.. Primary sclerosing cholangitis: refinement and validation of survival models.  Gastroenterology. 1992;  103 1893-1899
• 14 Shetty K, Rybicki L, Carey W D. The Child-Pugh classification as a prognostic indicator for survival in primary sclerosing cholangitis.  Hepatology. 1997;  25 1049-1053
• 15 Boberg K M, Rocca G, Egeland T et al.. Time-dependent Cox regression model is superior in prediction of prognosis in primary sclerosing cholangitis.  Hepatology. 2002;  35 652-657
• 16 Boberg K M, Bergquist A, Mitchell S et al.. Cholangiocarcinoma in primary sclerosing cholangitis: risk factors and clinical presentation.  Scand J Gastroenterol. 2002;  37 1205-1211
• 17 Okada H, Mizuno M, Yamamoto K, Tsuji T. Primary sclerosing cholangitis in Japanese patients: association with inflammatory bowel disease.  Acta Med Okayama. 1996;  50 227-235
• 18 Takikawa H, Manabe T. Primary sclerosing cholangitis in Japan-analysis of 192 cases.  J Gastroenterol. 1997;  32 134-137
• 19 Escorsell A, Pares A, Rodes J et al.. Epidemiology of primary sclerosing cholangitis in Spain.  J Hepatol. 1994;  21 787-791
• 20 Kochhar R, Goenka M K, Das K et al.. Primary sclerosing cholangitis: an experience from India.  J Gastroenterol Hepatol. 1996;  11 429-433
• 21 Kingham J GC, Kochar N, Gravenor M B. Incidence, clinical patterns, and outcomes of primary sclerosing cholangitis in South Wales, United Kingdom.  Gastroenterology. 2004;  126 1929-1930
• 22 Bergquist A, Ekbom A, Olsson R et al.. Hepatic and extrahepatic malignancies in primary sclerosing cholangitis.  J Hepatol. 2002;  36 321-327
• 23 Lundqvist K, Broomé U. Differences in colonic disease activity in patients with ulcerative colitis with and without primary sclerosing cholangitis: a case control study.  Dis Colon Rectum. 1997;  40 451-456
• 24 Olsson R, Danielsson A, Järnerot G et al.. Prevalence of primary sclerosing cholangitis in patients with ulcerative colitis.  Gastroenterology. 1991;  100 1319-1323
• 25 Rasmussen H H, Fallingborg J F, Mortensen P B et al.. Hepatobiliary dysfunction and primary sclerosing cholangitis in patients with Crohn’s disease.  Scand J Gastroenterol. 1997;  32 604-610
• 26 McGarity B, Bansi D S, Robertsson D AF, Millward-Sadler G H, Shepherd H A. Primary sclerosing cholangitis: an important and prevalent complication of Crohn’s disease.  Eur J Gastroenterol Hepatol. 1991;  3 361-364
• 27 Faubion Jr W A, Loftus E V, Sandborn W J, Freese D K, Perrault J. Pediatric “PSC-IBD”: a descriptive report of associated inflammatory bowel disease among pediatric patients with PSC.  J Pediatr Gastroenterol Nutr. 2001;  33 296-300
• 28 Loftus Jr E V, Harewood G C, Loftus C G et al.. PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis.  Gut. 2005;  54 91-96
• 29 Loftus E V, Sandborn W J, Lindor K D, LaRusso N F. Interactions between chronic liver disease and inflammatory bowel disease.  Inflamm Bowel Dis. 1997;  3 288-302
• 30 Broomé U, Glaumann H, Hellers G et al.. Liver disease in ulcerative colitis. An epidemiological and follow-up study in the county of Stockholm.  Gut. 1994;  35 84-89
• 31 Outwater E, Kaplan M M, Bankoff M S. Lymphadenopathy in sclerosing cholangitis: pitfall in the diagnosis of malignant biliary obstruction.  Gastrointest Radiol. 1992;  17 157-160
• 32 Hirche T O, Russler J, Braden B et al.. Sonographic detection of perihepatic lymphadenopathy is an indicator for primary sclerosing cholangitis in patients with inflammatory bowel disease.  Int J Colorectal Dis. 2004;  19 586-594
• 33 Ludwig J, Barham S S, La Russo N F et al.. Morphologic features of chronic hepatitis associated with primary sclerosing cholangitis and chronic ulcerative colitis.  Hepatology. 1981;  1 632-640
• 34 MacCarty R L, La Russo N F, May G R et al.. Cholangiocarcinoma complicating primary sclerosing cholangitis: cholangiographic appearances.  Radiology. 1985;  156 43-46
• 35 Rabinovitz M, Gavaler J S, Schade R R et al.. Does primary sclerosing cholangitis occurring in association with inflammatory bowel disease differ from that occurring in the absence of inflammatory bowel disease? A study of sixty-six subjects.  Hepatology. 1990;  11 7-11
• 36 Moayyeri A, Daryani N E, Bahrami H et al.. Clinical course of ulcerative colitis in patients with and without primary sclerosing cholangitis.  J Gastroenterol Hepatol. 2005;  20 366-370
• 37 Broomé U, Löfberg R, Lundqvist K, Veress B. Subclinical time span of inflammatory bowel disease in patients with primary sclerosing cholangitis.  Dis Colon Rectum. 1995;  38 1301-1305
• 38 Perdigoto R, Wiesner R H, La Russo N, Dozois R. Inflammatory bowel disease associated with primary sclerosing cholangitis: incidence, severity and relationship to liver disease.  Gastroenterology. 1991;  100 A238
• 39 Penna C, Dozois R, Tremaine W et al.. Pouchitis after ileal pouch-anal anastomosis for ulcerative colitis occurs with increased frequency in patients with associated primary sclerosing cholangitis.  Gut. 1996;  38 234-239
• 40 Zins B J, Sandborn W J, Penna C R et al.. Pouchitis disease course after orthotopic liver transplantation in patients with primary sclerosing cholangitis and an ileal pouch-anal anastomosis.  Am J Gastroenterol. 1995;  90 2177-2181
• 41 Tobias R, Wright J P, Kottler R E. Primary sclerosing cholangitis associated with inflammatory bowel disease in Cape Town, 1975-1981.  S Afr Med J. 1983;  63 229-235
• 42 Askling J, Dickman P W, Karlen P et al.. Family history as a risk factor for colorectal cancer in inflammatory bowel disease.  Gastroenterology. 2001;  120 1356-1362
• 43 Rutter M, Saunders B, Wilkinson K et al.. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis.  Gastroenterology. 2004;  126 451-459
• 44 Broomé U, Lindberg G, Löfberg R. Primary sclerosing cholangitis in ulcerative colitis-a risk factor for the development of dysplasia and DNA aneuploidy?.  Gastroenterology. 1992;  102 1877-1880
• 45 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
• 46 Brentnall T A, Haggitt R C, Rabinovitch P S et al.. Risk and natural history of colonic neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis.  Gastroenterology. 1996;  110 331-338
• 47 D'Haens G R, Lashner B A, Hanauer S B. Pericholangitis and sclerosing cholangitis are risk factors for dysplasia and cancer in ulcerative colitis.  Am J Gastroenterol. 1993;  88 1174-1178
• 48 Leidenius M H, Farkkila M A, Karkkainen P et al.. Colorectal dysplasia and carcinoma in patients with ulcerative colitis and primary sclerosing cholangitis.  Scand J Gastroenterol. 1997;  32 706-711
• 49 Eaden J A, Abrams K, Mayberry J F. The risk of colorectal cancer in ulcerative colitis: a meta analysis.  Gut. 2001;  48 526-535
• 50 Broomé U, Löfberg R, Veress B, Eriksson L S. Primary sclerosing cholangitis and ulcerative colitis: evidence for increased neoplastic potential.  Hepatology. 1995;  22 1404-1408
• 51 Choi P M, Nugent F W, Rossi R L. Relationship between colorectal neoplasia and primary sclerosing cholangitis in ulcerative colitis.  Gastroenterology. 1992;  103 1707-1709
• 52 Gurbuz A K, Giardiello F M, Bayless T M. Colorectal neoplasia in patients with ulcerative colitis and primary sclerosing cholangitis.  Dis Colon Rectum. 1995;  38 37-41
• 53 Loftus Jr E V, Sandborn W J, Tremaine W J et al.. Risk of colorectal neoplasia in patients with primary sclerosing cholangitis.  Gastroenterology. 1996;  110 432-440
• 54 Nuako K W, Ahlquist D A, Sandborn W J et al.. Primary sclerosing cholangitis and colorectal carcinoma in patients with chronic ulcerative colitis: a case-control study.  Cancer. 1998;  82 822-826
• 55 Ekbom A, Helmick C, Zack M, Adami H O. Ulcerative colitis and colorectal cancer. A population based study.  N Engl J Med. 1990;  323 1228-1233
• 56 Soetikno R M, Lin O S, Heidenreich P A, Young H S, Blackstone M O. Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: a meta-analysis.  Gastrointest Endosc. 2002;  56 48-54
• 57 Bleday R, Lee E, Jessurun J, Heine J, Wong W D. Increased risk of early colorectal neoplasms after hepatic transplant in patients with inflammatory bowel disease.  Dis Colon Rectum. 1993;  36 908-912
• 58 Higashi H, Yanaga K, Marsh J W et al.. Development of colon cancer after liver transplantation for primary sclerosing cholangitis associated with ulcerative colitis.  Hepatology. 1990;  11 477-480
• 59 Vera A, Gunson B K, Ussatoff V et al.. Colorectal cancer in patients with inflammatory bowel disease after liver transplantation for primary sclerosing cholangitis.  Transplantation. 2003;  75 1983-1988
• 60 Dvorchik I, Subotin M, Demetris A J et al.. Effect of liver transplantation on inflammatory bowel disease in patients with primary sclerosing cholangitis.  Hepatology. 2002;  35 380-384
• 61 van de Vrie W, de Man R A, van Buuren H R et al.. Inflammatory bowel disease and liver transplantation for primary sclerosing cholangitis.  Eur J Gastroenterol Hepatol. 2003;  15 657-663
• 62 Eaden J. Review article: colorectal carcinoma and inflammatory bowel disease.  Aliment Pharmacol Ther. 2004;  20 24-30
• 63 Rutter M D, Saunders B P, Wilkinson K H et al.. Cancer surveillance in longstanding ulcerative colitis: endoscopic appearances help predict cancer risk.  Gut. 2004;  53 1813-1816
• 64 Thomas R C, Selinger C, Rutter M D. Adherence to BSG adenoma surveillance guidelines will reduce colonoscopic workload.  Gut. 2005;  54 173 (Lett)
• 65 Nagggengast F, Grubben M, van Munster I. Role of bile acids in colorectal carcinogenesis.  Eur J Cancer. 1995;  31 1067-1070
• 66 Marchesa P, Lashner B A, Lavery I C et al.. The risk of cancer and dysplasia among ulcerative colitis patients with primary sclerosing cholangitis.  Am J Gastroenterol. 1997;  92 1285-1288
• 67 Shetty K, Rybicki L, Brzezinski A, Carey W D, Lashner B A. The risk for cancer or dysplasia in ulcerative colitis patients with primary sclerosing cholangitis.  Am J Gastroenterol. 1999;  94 1643-1649
• 68 Lindberg B U, Broome U, Persson B. Proximal colorectal dysplasia or cancer in ulcerative colitis. The impact of primary sclerosing cholangitis and sulfasalazine: results from a 20-year surveillance study.  Dis Colon Rectum. 2001;  44 77-85
• 69 Pardi D S, Loftus E V, Kremers W K, Keach J, Lindor K D. Ursodeoxycholic acid as a chemopreventive agent in patients with ulcerative colitis and primary sclerosing cholangitis.  Gastroenterology. 2003;  124 889-893
• 70 Tung B Y, Emond M J, Haggitt R C 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
• 71 Rutter M D, Saunders B P, Wilkinson K H, Kamm M A, Williams C B, Forbes A. Most dysplasia in ulcerative colitis is visible at colonoscopy.  Gastrointest Endosc. 2004;  60 334-339
• 72 Eaden J. Review article: the data supporting a role for aminosalicylates in the chemoprevention of colorectal cancer in patients with inflammatory bowel disease.  Aliment Pharmacol Ther. 2003;  2 15-21
• 73 Bernstein C N, Eaden J, Steinhart A H, Munkholm P, Gordon P H. Cancer prevention in inflammatory bowel disease and the chemoprophylactic potential of 5-aminosalicylic acid.  Inflamm Bowel Dis. 2002;  8 356-361
• 74 Ståhlberg D, Veress B, Tribukait B, Broomé U. Atrophy and neoplastic transformation of the ileal pouch mucosa in patients with ulcerative colitis and primary sclerosing cholangitis: a case control study.  Dis Colon Rectum. 2003;  46 770-778
• 75 Hay J E, Wiesner R H, Shorter R G, La Russo N F, Baldus W P. Primary sclerosing cholangitis and celiac disease. A novel association.  Ann Intern Med. 1988;  109 713-717
• 76 Lindström E, Bodemar G, Ryden B O, Ihse I. Pancreatic ductal morphology and exocrine function in primary sclerosing cholangitis.  Acta Chir Scand. 1990;  156 451-456
• 77 Heikius B, Niemela S, Lehtola J, Karttunen T, Lahde S. Hepatobiliary and coexisting pancreatic duct abnormalities in patients with inflammatory bowel disease.  Scand J Gastroenterol. 1997;  32 153-161
• 78 Cangemi J R, Wiesner R W, Beaver S J, LaRusso N. Effect of proctocolectomy for chronic uclerative colitis on the natural history of primary sclerosing cholangitis.  Gastroenterology. 1989;  96 790-794
• 79 Martin F M, Rossi R L, Nugent F W et al.. Surgical aspects of sclerosing cholangitis. Results in 178 patients.  Ann Surg. 1990;  212 551-556
• 80 Fucini C, Wolff B G, Dozois R R. Bleeding from peristomal varices: perspectives on prevention and treatment.  Dis Colon Rectum. 1991;  34 1073-1078
• 81 Wiesner R H, La Russo N F, Dozois R R, Beaver S J. Peristomal varices after proctocolectomy in patients with primary sclerosing cholangitis.  Gastroenterology. 1986;  90 316-322
• 82 Peck J J, Boyden A M. Exigent ileostomy hemorrhage. A complication of proctocolectomy in patients with chronic ulcerative colitis and primary sclerosing cholangitis.  Am J Surg. 1985;  150 153-158
• 83 Kartheuser A H, Dozois R R, La Russo N F et al.. Comparison of surgical treatment of ulcerative colitis associated with primary sclerosing cholangitis: ileal pouch-anal anastomosis versus Brooke ileostomy.  Mayo Clin Proc. 1996;  71 748-756
• 84 Vera A, Moledina S, Gunson B. Risk factors for recurrence of primary sclerosing cholangitis of liver allograft.  Lancet. 2002;  360(9349) 1943-1944
• 85 Mac Lean A R, Lilly L, Cohen Z, O'Connor B, McLeod R S. Outcome of patients undergoing liver transplantation for primary sclerosing cholangitis.  Dis Colon Rectum. 2003;  46 1124-1128
• 86 Ginsburg P M, Thuluvath P J. Diarrgea in liver transplant recipients: etiology and management.  Liver Transpl. 2005;  11 881-890
• 87 Stephens J, Goldstein R, Crippin J et al.. Effects of orthotopic liver transplantation and immunosuppression on inflammatory bowel disease in primary sclerosing cholangitis patients.  Transplant Proc. 1993;  25 1122-1123
• 88 Befeler A S, Lissoos T W, Schiano T D et al.. Clinical course and management of inflammatory bowel disease after liver transplantation.  Transplantation. 1998;  65 393-396
• 89 Gavaler J S, Delemos B, Belle S H et al.. Ulcerative colitis disease activity as subjectively assessed by patient-completed questionnaires following orthotopic liver transplantation for sclerosing cholangitis.  Dig Dis Sci. 1991;  36 321-328
• 90 Papatheodoridis G V, Hamilton M, Mistry P K, Davidson B, Rolles K, Burroughs A K. Ulcerative colitis has an aggressive course after orthotopic liver transplantation for primary sclerosing cholangitis.  Gut. 1998;  43 639-644
• 91 Knechtle S J, D’Alessandro A M, Harms B A et al.. Relationships between sclerosing cholangitis, inflammatory bowel disease, and cancer in patients undergoing liver transplantation.  Surgery. 1995;  118 615-619
• 92 Miki C, Harrison J D, Gunson B K et al.. Inflammatory bowel disease in primary sclerosing cholangitis: an analysis of patients undergoing liver transplantation.  Br J Surg. 1995;  82 1114-1117
• 93 Shaked A, Colonna J O, Goldstein L, Busuttil R W. The interrelation between sclerosing cholangitis and ulcerative colitis in patients undergoing liver transplantation.  Ann Surg. 1992;  215 598-603
• 94 Haagsma E B, Van Den Berg A P, Kleibeuker J H, Slooff M J, Dijkstra G. Inflammatory bowel disease after liver transplantation: the effect of different immunosuppressive regimens.  Aliment Pharmacol Ther. 2003;  18 33-44
• 95 Cottone M, Pietrosi G, Martorana G et al.. Prevalence of cytomegalovirus infection in severe refractory ulcerative and Crohn’s colitis.  Am J Gastroenterol. 2001;  96 773-775
• 96 van de Vrie W, de Man R, van Buuren H et al.. Inflammatory bowel disease and liver transplantation for primary sclerosing cholangitis.  Eur J Gastroenterol Hepatol. 2003;  15 657-663
• 97 Saldeen K, Friman S, Olausson M, Olsson R. Follow-up after liver transplantation for primary sclerosing cholangitis: effects on survival, quality of life, and colitis.  Scand J Gastroenterol. 1999;  34 535-540