DOES COLECTOMY AFFECT THE PROGRESSION OF PRIMARY SCLEROSING CHOLANGITIS? A SYSTEMATIC REVIEW AND META-ANALYSIS
Gastroenterology and Hepatology from Bed to Bench,
2 September 2018
Aim: The aim of this systematic review was to determine if the human colon, through the lower gut-liver axis, drives PSC activity by assessing the progression of the disease in patients with and without colectomy for colonic disease.
Background: The gut-liver axis is involved in the pathogenesis of liver disease. Abnormal immune-mediated responses to intestinal
microbiome are implicated in primary sclerosing cholangitis (PSC) however the mechanisms remain poorly understood. Currently, no
single animal model recapitulates all attributes of PSC in humans and this limits further studies of gut-liver interactions.
Methods: A systematic search of PubMed, Medline, and Scopus was performed for articles that contained the terms “colectomy” or
“bowel resection” AND “primary sclerosing cholangitis” up to 15th April 2018. Articles were reviewed by 2 reviewers and raw data
collated. A Forest plot was used to illustrate the effect of colectomy on subsequent liver transplantation for PSC. Linear regression was
used to estimate mortality risk.
Results: Colectomy appeared to have no effect on PSC progression, although high-quality studies were lacking. Rates of liver
transplantation or transjugular intrahepatic portosystemic shunt for PSC were not affected by colectomy (OR 0.59, 95% CI 0.14 - 2.53,
p=0.48). Mortality risk following colectomy in patients with PSC is 2.11% per year (95% CI 0.03% - 4.18%, p=0.032, R2 = 0.722).
Conclusion: Current evidence is limited but suggests colectomy does not affect the progression of PSC in patients with colonic disease.
Pathogenic micro-organisms or antigens that drive PSC may not be limited to the lower gut.
Keywords: Primary sclerosing cholangitis, Inflammatory bowel disease, Colectomy, Procto-colectomy.
(Please cite as: Ong J, Bath MF, Swift C, Al-Naeeb Y. Does colectomy affect the progression of primary sclerosing
cholangitis? A systematic review and meta-analysis. Gastroenterol Hepatol Bed Bench 2018;11(4):277-283).
- Primary sclerosing cholangitis
- inflammatory bowel disease
Volta U, Bonazzi C, Bianchi FB, Baldoni AM, Zoli M and Pisi E. IgA antibodies to dietary antigens in liver cirrhosis. Ric Clin Lab 1987;17, 235–242.
Vajro P, Paolella G & Fasano A. Microbiota And Gut-Liver Axis: A Mini-Review On Their Influences On Obesity And Obesity Related Liver Disease. J Pediatr Gastroenterol Nutr 2013;56, 461–468. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3637398/
Tripathi A, Debelius J, Brenner DA, Karin M, Loomba R, Schnabi, et al. The gut-liver axis and the intersection with the microbiome. Nat Rev Gastroenterol Hepatol 2018; 15(7):397-411. Available at: https://www.nature.com/articles/s41575-018-0011-z
Boonstra K, Beuers U & Ponsioen CY. Epidemiology of primary sclerosing cholangitis and primary biliary cirrhosis: A systematic review. Journal of Hepatology 2012;56, 1181–1188. Available at: https://www.journal-of-hepatology.eu/article/S0168-8278(12)00043-8/fulltext
Olsson R & Hulten L. Concurrence of ulcerative colitis and chronic active hepatitis: clinical courses and results of colectomy. Stand J Gastroenterol 1975;10:331-5.
Stauffer MH, Sauer WG, Dearing WH & Baggenstoss AH. The spectrum of cholestatic hepatic disease. JAMA 1965;191:829-37. Available at: https://jamanetwork.com/journals/jama/article-abstract/655052
Wood RAB & Cuschieri A. Is sclerosing cholangitis complicating ulcerative colitis a reversible condition? Lancet 1980;ii:716-8. Available at: https://www.thelancet.com/journals/lancet/article/PIIS0140-6736(80)91935-2/abstract
Cangemi JR, Weisner RH, Beaver SJ, Ludwig J, MacCarty RL, Dozois RR et al. Effect of proctocolectomy for chronic ulcerative colitis on the natural history of primary sclerosing cholangitis. Gastroenterology 1989;96, 790–794. Available at: https://www.gastrojournal.org/article/0016-5085(89)90903-7/pdf?referrer=https%3A%2F%2Fwww.ncbi.nlm.nih.gov%2F
Goudet P, Dozois RR, Kelly KA, Ilstrup DM & Phillips SF. Characteristics and evolution of extraintestinal manifestations associated with ulcerative colitis after proctocolectomy. Dig Surg 2001;18, 51–55. Available at: https://www.karger.com/Article/Abstract/50097
Grant AJ, Lalor PF, Hubscher SG, Briskin M & Adams DH. MAdCAM-1 expressed in chronic inflammatory liver disease supports mucosal lymphocyte adhesion to hepatic endothelium (MAdCAM-1 in chronic inflammatory liver disease). Hepatology 2001;33:1065-1072. Available at: https://aasldpubs.onlinelibrary.wiley.com/doi/abs/10.1053/jhep.2001.24231
Eksteen B, Grant AJ, Miles A, Curbishley SM, Lalor PF, Hubscher SG, et al. Hepatic endothelial CCL25 mediates the recruitment of CCR9 gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J Exp Med 2004;200:1511-1517. Available at: http://jem.rupress.org/content/200/11/1511.long
Karrar A, Broome U, Sodergren T, Jaksch M, Bergquist A, Bjornstedt M, et al. Biliary epithelial cell antibodies link adaptive and innate immune responses in primary sclerosing cholangitis. Gastroenterology 2007;132, 1504–1514. Available at: https://www.gastrojournal.org/article/S0016-5085(07)00178-3/fulltext?referrer=https%3A%2F%2Fwww.ncbi.nlm.nih.gov%2F
Katt J, Schwinge D, Schoknecht T, Quaas A, Sobotka I, Burandt E, et al. Increased T helper type 17 response to pathogen stimulation in patients with primary sclerosing cholangitis. Hepatology 2013;58, 1084–1093. Available at: https://aasldpubs.onlinelibrary.wiley.com/doi/abs/10.1002/hep.26447
Alabraba E, Nightingale P, Gunson B, Hubscher S, Olliff S, Mirza D, et al. A re-evaluation of the risk factors for the recurrence of primary sclerosing cholangitis in liver allografts. Liver Transpl. 2009;15, 330–340. Available at: https://aasldpubs.onlinelibrary.wiley.com/doi/abs/10.1002/lt.21679
Fickert P, Pollheimer MJ, Beuers U, Lackner C, Hirschfield G, et al. Characterization of animal models for primary sclerosing cholangitis (PSC). Journal of Hepatology 2014;60, 1290–1303. Available at: https://www.journal-of-hepatology.eu/article/S0168-8278(14)00111-1/fulltext
Moher D, Liberati A, Tetzlaff J, Altman DG & PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009;151:264–269,W64. Available at: http://annals.org/aim/fullarticle/744664/preferred-reporting-items-systematic-reviews-meta-analyses-prisma-statement
Aitola PT, Mattila J, Halonen PJ & Matikainen MJ. The effect of colectomy on histological and biochemical liver changes associated with ulcerative colitis. European Journal of Gastroenterology & Hepatology 1994;6, 803.
Mikkola K, Kiviluoto T, Riihelä M, Taavitsainen M & Järvinen HJ. Liver involvement and its course in patients operated on for ulcerative colitis. Hepatogastroenterology 1995;42, 68–72.
Cho CS, Dayton MT, Thompson JS, Koltun WA, Heise CP & Harms BA. Proctocolectomy-ileal pouch-anal anastomosis for ulcerative colitis after liver transplantation for primary sclerosing cholangitis: a multi-institutional analysis. J. Gastrointest. Surg. 2008;12, 1221–1226. Available at: https://link.springer.com/article/10.1007%2Fs11605-008-0528-5
Lepistö A, Kivistö S, Kivisaari L, Arola J & Järvinen HJ. Primary sclerosing cholangitis: outcome of patients undergoing restorative proctocolecetomy for ulcerative colitis. Int J Colorectal Dis 2009;24, 1169–1174. Available at: https://link.springer.com/article/10.1007%2Fs00384-009-0773-4
Poritz LS. & Koltun WA. Surgical management of ulcerative colitis in the presence of primary sclerosing cholangitis. Dis. Colon Rectum 2003;46, 173–178.
Navaneethan U, Venkatesh PGK, Lashner BA, Shen B & Kiran RP. The impact of ulcerative colitis on the long-term outcome of patients with primary sclerosing cholangitis. Aliment. Pharmacol. Ther. 2012;35, 1045–1053. Available at: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-2036.2012.05063.x
Nordenvall C, Olen O, Nilsson PJ, von Seth E, Ekbom A, Bottai M, et al. Colectomy prior to diagnosis of primary sclerosing cholangitis is associated with improved prognosis in a nationwide cohort study of 2594 PSC-IBD patients. Aliment. Pharmacol. Ther. 2018;47, 238–245. Available at: https://onlinelibrary.wiley.com/doi/abs/10.1111/apt.14393
Mathis KL, Benavente-Chenhalls LA, Dozois EJ, Wolff BG & Larson DW. Short- and long-term surgical outcomes in patients undergoing proctocolectomy with ileal pouch-anal anastomosis in the setting of primary sclerosing cholangitis. Dis. Colon Rectum 2011;54, 787–792. Available at: https://journals.lww.com/dcrjournal/Abstract/2011/07000/Short__and_Long_Term_Surgical_Outcomes_in_Patients.5.aspx
Lian L, Menon, KVN, Shen B, Remzi F & Kiran RP. Inflammatory bowel disease complicated by primary sclerosing cholangitis and cirrhosis: is restorative proctocolectomy safe? Dis. Colon Rectum 2012;55, 79–84. Available at: https://journals.lww.com/dcrjournal/Abstract/2012/01000/Inflammatory_Bowel_Disease_Complicated_by_Primary.12.aspx
Post AB, Bozdech JM, Lavery I & Barnes DS. Colectomy in patients with inflammatory bowel disease and primary sclerosing cholangitis. Dis. Colon Rectum 1994;37, 175–178.
Penna C, Dozois R, Tremaine W, Sandborn W, LaRusso N, Schlek C, 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. Available at: https://gut.bmj.com/content/38/2/234.long
Gorgun E, Remzi FH, Manilich E, Preen M, Shen B & Fazio VW. Surgical outcome in patients with primary sclerosing cholangitis undergoing ileal pouch-anal anastomosis: a case-control study. Surgery 2005;138, 631–637; discussion 637-639. Available at: https://www.surgjournal.com/article/S0039-6060(05)00408-3/fulltext
Treeprasertsuk S, Björnsson E, Sinakos E, Weeding E & Lindor KD. Outcome of patients with primary sclerosing cholangitis and ulcerative colitis undergoing colectomy. World J Gastrointest Pharmacol Ther 2013;4, 61–68. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3729869/
Lindberg J, Stenling R, Palmqvist R & Rutegård J. Early onset of ulcerative colitis: long-term follow-up with special reference to colorectal cancer and primary sclerosing cholangitis. J. Pediatr. Gastroenterol. Nutr. 2008;46, 534–538. Available at: https://journals.lww.com/jpgn/fulltext/2008/05000/Early_Onset_of_Ulcerative_Colitis__Long_term.9.aspx
Cooperman AM. & Judd ES. The role of colectomy in hepatic disease accompanying ulcerative and granulomatous colitis. Current status of a continuing problem. Mayo Clin. Proc. 1972;47, 36–38.
Eade MN, Cooke WT & Brooke BN. Liver disease in ulcerative colitis. II. The long-term effect of colectomy. Ann. Intern. Med. 1970;72, 489–497. Available at: http://annals.org/aim/article-abstract/684195/liver-disease-ulcerative-colitis-ii-long-term-effect-colectomy?volume=72&issue=4&page=489
Kartheuser AH, Dozois RR, LaRusso NF, Weisner RH, Ilstrup DM & Schlek CD. 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 (1996). Available at: https://www.mayoclinicproceedings.org/article/S0025-6196(11)64839-8/fulltext
Dirks E & Singer MV. [Ulcerative colitis and primary sclerosing cholangitis-does proctocolectomy have a therapeutic effect?]. Z Gastroenterol 1990;28, 222–224.
Card TR, Solaymani-Dodaran M & West J. Incidence and mortality of primary sclerosing cholangitis in the UK: a population-based cohort study. J. Hepatol. 2008;48, 939–944. Available at: https://www.journal-of-hepatology.eu/article/S0168-8278(08)00206-7/fulltext
Broomé U, Olsson R, Loof L, Bodemar G, Hultcrantz R, Danielsson A, et al. Natural history and prognostic factors in 305 Swedish patients with primary sclerosing cholangitis. Gut 1996;38, 610–615. Available at: https://gut.bmj.com/content/38/4/610.long
Kingham JGC, Kochar N & Gravenor M. B. Incidence, clinical patterns, and outcomes of primary sclerosing cholangitis in South Wales, United Kingdom. Gastroenterology 2004;126, 1929–1930. Available at: https://www.gastrojournal.org/article/S0016-5085(04)00757-7/fulltext?referrer=https%3A%2F%2Fwww.ncbi.nlm.nih.gov%2F
Ueda Y, Kaido T, Okajima H, Hata K, Anazawa T, Yoshizawa A, et al. Long-term Prognosis and Recurrence of Primary Sclerosing Cholangitis After Liver Transplantation: A Single-Center Experience. Transplant Direct 2017;3, e334. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5828688/
Tischendorf JJW, Hecker H, Krüger M, Manns MP & Meier PN. Characterization, outcome, and prognosis in 273 patients with primary sclerosing cholangitis: A single center study. Am. J. Gastroenterol. 2007;102, 107–114. Available at: https://www.nature.com/articles/ajg200719
Sampaziotis F, de Brito MC, Madrigal P, Bertero A, Saeb-Parsy K, Soares FAC, et al. Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation. Nature Biotechnology 2015;33, 845–852. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4768345/
Sampaziotis F, Justin AW, Tysoe OC, Sawiak S, Godfrey EM, Upponi SS, et al. Reconstruction of the mouse extrahepatic biliary tree using primary human extrahepatic cholangiocyte organoids. Nature Medicine 2017;23, 954–963. Available at: https://www.nature.com/articles/nm.4360
- Abstract Viewed: 310 times
- PDF Downloaded: 123 times
- XML Downloaded: 45 times
- XML Downloaded: 625 times
- XML Downloaded: 79 times