Pancreatic involvement in inflammatory bowel disease: a review
PDF (Русский)

Keywords

inflammatory bowel disease, acute pancreatitis, autoimmune pancreatitis, extraintestinal manifestations, pancreas

How to Cite

Fousekis, F. S., Theopistos, V. I., Katsanos, K. H., & Christodouloua, D. K. (2019). Pancreatic involvement in inflammatory bowel disease: a review. Herald of Pancreatic Club, 44(3), 23-32. https://doi.org/10.33149/vkp.2019.03.02

Abstract views: 7
PDF Downloads: 12

Abstract

Inflammatory bowel disease (IBD) is a multisystemic disease, and pancreatic manifestations of IBD are not uncommon. The incidence of several pancreatic diseases in Crohn’s disease and ulcerative colitis is more frequent compared to the general population. Pancreatic manifestations in IBD include a wide heterogenic group of disorders and abnormalities of the pancreas and range from mild self-limited diseases to severe disorders. Acute pancreatitis, chronic pancreatitis, autoimmune pancreatitis, pancreatic autoantibodies, exocrine pancreatic insufficiency and asymptomatic imaging and laboratory abnormalities are included in related-IBD pancreatic manifestations. Involvement of the pancreas in IBD may be the result of IBD itself or of medications used.

https://doi.org/10.33149/vkp.2019.03.02
PDF (Русский)

References

1. Altman H. S., Phillips G., Bank S., Klotz H. Pancreatitis associated with duodenal Crohn’s disease. Am J Gastroenterol. 1983. Vol. 78, No 3. P. 174–177.
2. Angelini G., Cavallini G., Bovo P., Brocco G., Castagnini A., Lavarini E., Merigo F. Pancreatic function in chronic inflammatory bowel disease. Int J Pancreatol. 1988. Vol. 3, No 2–3. P. 185–193.
3. Barthet M., Hastier P., Bernard J. P., Bordes G., Frederick J., Allio S., Mambrini P. Chronic pancreatitis and inflammatory bowel disease: true or coincidental association? Am J Gastroenterol. 1999. Vol. 94, No 8. P. 2141–2148.
4. Barthet M., Lesavre N., Desplats S., Panuel M., Gasmi M., Bernard J. P., Dagorn J. C. Frequency and characteristics of pancreatitis in patients with inflammatory bowel disease. Pancreatology. 2006. Vol. 6, No 5. P. 464–471.
5. Bermejo F., Lopez-Sanroman A., Taxonera C., Gisbert J. P., Perez-Calle J. L., Vera I., Menchen L. Acute pancreatitis in inflammatory bowel disease, with special reference to azathioprine-induced pancreatitis. Aliment PharmacolTher. 2008. Vol. 28, No 5. P. 623–628.
6. Bogdanos D. P., Rigopoulou E. I., Smyk D. S., Roggenbuck D., Reinhold D., Forbes A., Laass M. W. Diagnostic value, clinical utility and pathogenic significance of reactivity to the molecular targets of Crohn's disease specific-pancreatic autoantibodies. Autoimmun Rev. 2011. Vol. 11, No 2. P. 143–148.
7. Bogdanos D. P., Roggenbuck D., Reinhold D., Wex T., Pavlidis P., von Arnim U., Malfertheiner P. Pancreatic-specific autoantibodies to glycoprotein 2 mirror disease location and behaviour in younger patients with Crohn’s disease. BMC Gastroenterol. 2012. Vol. 12. P. 102.
8. Bokemeyer B. Asymptomatic elevation of serum lipase and amylase in conjunction with Crohn’s disease and ulcerative colitis. Z Gastroenterol. 2002. Vol. 40, No 1. P. 5–10.
9. Broide E., Dotan I., Weiss B., Wilschanski M., Yerushalmi B., Klar A., Levine A. Idiopathic pancreatitis preceding the diagnosis of inflammatory bowel disease is more frequent in pediatric patients. J PediatrGastroenterolNutr. 2011. Vol. 52, No 6. P. 714–717.
10. Chen Y. L., Hsu C. W., Cheng C. C., Yiang G. T., Lin C. S., Lin C. L., Sung F. C. Increased subsequent risk of inflammatory bowel disease association in patients with chronic pancreatitis: a nationwide population-based cohort study. Curr Med Res Opin. 2017. Vol. 33, No 6. P. 1077–1082.
11. Chen Y. T., Su J. S., Tseng C. W., Chen C. C., Lin C. L., Kao C. H. Inflammatory bowel disease on the risk of acute pancreatitis: a population-based cohort study. J GastroenterolHepatol. 2016. Vol. 31, No 4. P. 782–787.
12. Conwell D. L., Lee L. S., Yadav D., Longnecker D. S., Miller F. H., Mortele K. J., Levy M. J. et al. American Pancreatic Association Practice Guidelines in Chronic Pancreatitis: evidence-based report on diagnostic guidelines. Pancreas. 2014. Vol. 43, No 8. P. 1143–1162.
13. Dong L. H., Liu Z. M., Wang S. J., Zhao S. J., Zhang D., Chen Y., Wang Y. S. Corticosteroid therapy for severe acute pancreatitis: a meta-analysis of randomized, controlled trials. Int J ClinExpPathol. 2015. Vol. 8, No 7. P. 7654–7660.
14. Faintuch J., Mott C. B., Machado M. C. Pancreatitis and pancreatic necrosis during sulfasalazine therapy. Int Surg. 1985. Vol. 70, No 3. P. 271–272.
15. Fernandez J., Sala M., Panes J., Feu F., Navarro S., Teres J. Acute pancreatitis after long-term 5-aminosalicylic acid therapy. Am J Gastroenterol. 1997. Vol. 92, No 12. P. 2302–2303.
16. Forsmark C. E., Baillie J., Practice AGAIC, Economics C, Board AGAIG. AGA Institute technical review on acute pancreatitis. Gastroenterology. 2007. Vol. 132, No 5. P. 2022–2044.
17. Garau P., Orenstein S. R., Neigut D. A., Kocoshis S. A. Pancreatitis associated with olsalazine and sulfasalazine in children with ulcerative colitis. J PediatrGastroenterolNutr. 1994. Vol. 18, No 4. P. 481–485.
18. Garrido Gomez E., Lopez San Roman A., Bermejo San Jose F. Idiopathic pancreatitis in inflammatory bowel disease. J Crohns Colitis. 2008. Vol. 2, No 3. P. 237–240.
19. Goldin E., Libson E., Wengrower D., Antal S., Kovacs Z., Rachmilewitz D. Severe acute pancreatitis as the presenting symptom of primary sclerosing cholangitis: treatment by endoscopic insertion of a biliary stent. Int Surg.1990. Vol. 75, No 1. P. 58–60.
20. Gross S., Bakker S. F., van Bodegraven A. A., van Hoogstraten I. M., Gelderman K. A., Bouma G., Mulder C. J. Increased IgA glycoprotein-2 specific antibody titres in refractory celiac disease. J Gastrointestin Liver Dis. 2014. Vol. 23, No 2. P. 127–133.
21. Heap G. A., Weedon M. N., Bewshea C. M., Singh A., Chen M., Satchwell J. B., Vivian J. P. et al. HLA-DQA1-HLA-DRB1 variants confer susceptibility to pancreatitis induced by thiopurineimmunosuppressants. Nat Genet. 2014. Vol. 46, No 10. P. 1131–1134.
22. Heikius B., Niemela S., Lehtola J., Karttunen T., Lahde S. Pancreatic duct abnormalities and pancreatic function in patients with chronic inflammatory bowel disease. Scand J Gastroenterol. 1996. Vol. 31, No 5. P. 517–523.
23. Isaacs K. L., Murphy D. Pancreatitis after rectal administration of 5-aminosalicylic acid. J ClinGastroenterol. 1990. Vol. 12, No 2. P. 198–199.
24. Joossens S., Vermeire S., Van Steen K., Godefridis G., Claessens G., Pierik M., Vlietinck R. et al. Pancreatic autoantibodies in inflammatory bowel disease. Inflamm Bowel Dis. 2004. Vol. 10, No 6. P. 771–777.
25. Kamisawa T., Chari S. T, Giday S. A., Kim M. H., Chung J. B., Lee K. T., Werner J. Clinical profile of autoimmune pancreatitis and its histological subtypes: an international multicenter survey. Pancreas. 2011. Vol. 40, No 6. P. 809–814.
26. Katz S., Bank S., Greenberg R. E., Lendvai S., Lesser M., Napolitano B. Hyperamylasemia in inflammatory bowel disease. J ClinGastroenterol. 1988. Vol. 10, No 6. P. 627–630.
27. Ledder O., Lemberg D. A., Day A. S. Thiopurine-induced pancreatitis in inflammatory bowel diseases. Expert Rev GastroenterolHepatol. 2015. Vol. 9, No 4. P. 399–403.
28. Lindkvist B. Diagnosis and treatment of pancreatic exocrine insufficiency. World J Gastroenterol. 2013. Vol. 19, No 42. P. 7258–7266.
29. Liu Y. P., Wu H. Y., Yang X., Xu H. Q., Li Y. C., Shi D. C., Huang J. F. Association between thiopurine S-methyltransferase polymorphisms and thiopurine-induced adverse drug reactions in patients with inflammatory bowel disease: a meta-analysis. PLoS One. 2015. Vol. 10, No 3. P. e0121745.
30. Lorenzo D., Maire F., Stefanescu C., Gornet J. M., Seksik P., Serrero M., Bournet B. Features of autoimmune pancreatitis associated with inflammatory bowel diseases. ClinGastroenterolHepatol. 2018. Vol. 16, No 1. P. 59–67.
31. Maconi G., Dominici R., Molteni M., Ardizzone S., Bosani M., Ferrara E., Gallus S. Prevalence of pancreatic insufficiency in inflammatory bowel diseases. Assessment by fecal elastase-1. Dig Dis Sci. 2008. Vol. 53, No 1. P. 262–270.
32. Majumder S., Chari S. T. Chronic pancreatitis. Lancet. 2016. Vol. 387, No 10031. P. 1957–1966.
33. Maurer P., Haag K., Roth M., Kuder C., Scholmerich J. No evidence for abnormal gallbladder emptying in Crohn’s disease. Hepatogastroenterology. 1996. Vol. 43, No 10. P. 807–812.
34. Michaels M. A., Jendrek S. T., Korf T., Nitzsche T., Teegen B., Komorowski L., Derer S. Pancreatic autoantibodies against CUZD1 and GP2 are associated with distinct clinical phenotypes of Crohn’s disease. Inflamm Bowel Dis. 2015. Vol. 21, No 12. P. 2864–2872.
35. Miehsler W., Reinisch W., Valic E., Osterode W., Tillinger W., Feichtenschlager T., Grisar J. Is inflammatory bowel disease an independent and disease specific risk factor for thromboembolism? Gut. 2004. Vol. 53, No 4. P. 542–548.
36. Moolsintong P., Loftus E. V. Jr, Chari S. T., Egan L. J., Tremaine W. J., Sandborn W. J. Acute pancreatitis in patients with Crohn’s disease: clinical features and outcomes. Inflamm Bowel Dis. 2005. Vol. 11, No 12. P. 1080–1084.
37. Nesvaderani M., Eslick G. D., Cox M. R. Acute pancreatitis: update on management. Med J Aust. 2015. Vol. 202, No 8. P. 420–423.
38. Nitsche C., Maertin S., Scheiber J., Ritter C. A., Lerch M. M., Mayerle J. Drug-induced pancreatitis. CurrGastroenterol Rep. 2012. Vol. 14, No 2. P. 131–138.
39. O’Halloran E., Hogan A., Mealy K. Metronidazole-induced pancreatitis. HPB Surg. 2010. Vol. 2010. P. 523468.
40. Pajares J. A., Hernandez L., Menchen P., Menchen L. Duodenopancreatic fistula complicating upper gastrointestinal Crohn’s disease: successful treatment with infliximab. Am J Gastroenterol. 2009. Vol. 104, No 7. P. 1863–1864.
41. Parente F., Pastore L., Bargiggia S., Cucino .C, Greco S., Molteni M., Ardizzone S. Incidence and risk factors for gallstones in patients with inflammatory bowel disease: a large case-control study. Hepatology. 2007. Vol. 45, No 5. P. 1267–1274.
42. Pavlidis P., Romanidou O., Roggenbuck D., Mytilinaiou M. G., Al-Sulttan F., Liaskos C., Smyk D. S. Ileal inflammation may trigger the development of GP2-specific pancreatic autoantibodies in patients with Crohn’s disease. ClinDevImmunol. 2012. Vol. 2012. P. 640835.
43. Picardo S., So K., Venugopal K., Chin M. Vedolizumab-induced acute pancreatitis: the first reported clinical case. BMJ Case Rep. 2018. Vol. 2018.
44. Pitchumoni C. S., Rubin A., Das K. Pancreatitis in inflammatory bowel diseases. J ClinGastroenterol. 2010. Vol. 44, No 4. P. 246–253.
45. Pitt H. A., King W. 3rd, Mann L. L., Roslyn J. J., Berquist W. E., Ament M. E., DenBesten L. Increased risk of cholelithiasis with prolonged total parenteral nutrition. Am J Surg. 1983. Vol. 145, No 1. P. 106–112.
46. Ramos L. R., Sachar D. B., DiMaio C. J., Colombel J. F., Torres J. Inflammatory bowel disease and pancreatitis: a review. J Crohns Colitis. 2016. Vol. 10, No 1. P. 95–104.
47. Rana S. S., Vilmann P. Endoscopic ultrasound features of chronic pancreatitis: A pictorial review. Endosc Ultrasound. 2015. Vol. 4, No 1. P. 10–14.
48. Ransford R. A., Langman M. J. Sulphasalazine and mesalazine: serious adverse reactions re-evaluated on the basis of suspected adverse reaction reports to the Committee on Safety of Medicines. Gut. 2002. Vol. 51, No 4. P. 536–539.
49. Rasmussen H. H., Fonager K., Sorensen H. T., Pedersen L., Dahlerup J. F., Steffensen F. H. Risk of acute pancreatitis in patients with chronic inflammatory bowel disease. A Danish 16-year nationwide follow-up study. Scand J Gastroenterol. 1999. Vol. 34, No 2. P. 199–201.
50. Ravi K., Chari S. T., Vege S. S., Sandborn W. J., Smyrk T. C., Loftus E. V. Jr. Inflammatory bowel disease in the setting of autoimmune pancreatitis. Inflamm Bowel Dis. 2009. Vol. 15, No 9. P. 1326–1330.
51. Russo L., Schneider G., Gardiner M. H., Lanes S., Streck P., Rosen S. Role of pharmacoepidemiology studies in addressing pharmacovigilance questions: a case example of pancreatitis risk among ulcerative colitis patients using mesalazine. Eur J ClinPharmacol. 2014. Vol. 70, No 6. P. 709–717.
52. Sadr-Azodi O., Mattsson F., Bexlius T. S., Lindblad M., Lagergren J., Ljung R. Association of oral glucocorticoid use with an increased risk of acute pancreatitis: a population-based nested case-control study. JAMA Intern Med. 2013. Vol. 173, No 6. P. 444–449.
53. Said K., Glaumann H., Bergquist A. Gallbladder disease in patients with primary sclerosing cholangitis. J Hepatol. 2008. Vol. 48, No 4. P. 598–605.
54. Sakorafas G. H., Milingos D., Peros G. Asymptomatic cholelithiasis: is cholecystectomy really needed? A critical reappraisal 15 years after the introduction of laparoscopic cholecystectomy. Dig Dis Sci. 2007. Vol. 52, No 5. P. 1313–1325.
55. Schreyer A. G., Jung M., Riemann J. F., Niessen C., Pregler B., Grenacher L., Hoffmeister A. S3 guideline for chronic pancreatitis — diagnosis, classification and therapy for the radiologist. Rofo. 2014. Vol. 186, No 11. P. 1002–1008.
56. Shimosegawa T., Chari S. T, Frulloni L., Kamisawa T., Kawa S., Mino-Kenudson M., Kim M. H. International consensus diagnostic criteria for autoimmune pancreatitis: guidelines of the International Association of Pancreatology. Pancreas. 2011. Vol. 40, No 3. P. 352–358.
57. Smyk D. S., Rigopoulou E. I., Koutsoumpas A. L., Kriese S., Burroughs A. K., Bogdanos D. P. Autoantibodies in autoimmune pancreatitis. Int J Rheumatol. 2012. Vol. 2012. P. 940831.
58. Soubieres A. A., Poullis A. Emerging role of novel biomarkers in the diagnosis of inflammatory bowel disease. World J GastrointestPharmacolTher. 2016. Vol. 7, No 1. P. 41–50.
59. Spanier B. W., Dijkgraaf M. G., Bruno M. J. Epidemiology, aetiology and outcome of acute and chronic pancreatitis: an update. Best Pract Res ClinGastroenterol. 2008. Vol. 22, No 1. P. 45–63.
60. Srinath A. I., Gupta N., Husain S. Z. Probing the association of pancreatitis in inflammatory bowel disease. Inflamm Bowel Dis. 2016. Vol. 22, No 2. P. 465–475.
61. Steer M. L., Waxman I., Freedman S. Chronic pancreatitis. N Engl J Med. 1995. Vol. 332, No 22. P. 1482–1490.
62. Stobaugh D. J., Deepak P. Effect of tumor necrosis factor-alpha inhibitors on drug-induced pancreatitis in inflammatory bowel disease. Ann Pharmacother. 2014. Vol. 48, No 10. P. 1282–1287.
63. Sura M. E., Heinrich K. A., Suseno M. Metronidazole-associated pancreatitis. Ann Pharmacother. 2000. Vol. 34, No 10. P. 1152–1155.
64. Teich N., Mohl W., Bokemeyer B., Bundgens B., Buning J., Miehlke S., Huppe D. Azathioprine-induced acute pancreatitis in patients with inflammatory bowel diseases — a prospective study on incidence and severity. J Crohns Colitis. 2016. Vol. 10, No 1. P. 61–68.
65. Tenner S., Baillie J., DeWitt J., Vege S. S., American College of G. American College of Gastroenterology guideline: management of acute pancreatitis. Am J Gastroenterol. 2013. Vol. 108, No 9. P. 1400–1416.
66. Toda N., Akahane M., Kiryu S., Matsubara Y., Yamaji Y., Okamoto M., Minagawa N. Pancreas duct abnormalities in patients with ulcerative colitis: a magnetic resonance pancreatography study. Inflamm Bowel Dis. 2005. Vol. 11, No 10. P. 903–908.
67. Tornai T., Tornai D., Sipeki N., Tornai I., Alsulaimani R., Fechner K., Roggenbuck D. Loss of tolerance to gut immunity protein, glycoprotein 2 (GP2) is associated with progressive disease course in primary sclerosing cholangitis. Sci Rep. 2018. Vol. 8, No 1. P. 399.
68. Triantafillidis J. K., Cheracakis P., Hereti I. A., Argyros N., Karra E. Acute idiopathic pancreatitis complicating active Crohn’s disease: favorable response to infliximab treatment. Am J Gastroenterol. 2000. Vol. 95, No 11. P. 3334–3336.
69. Tromm A., Holtmann B., Huppe D., Kuntz H. D., Schwegler U., May B. Hyperamylasemia, hyperlipasemia and acute pancreatitis in chronic inflammatory bowel diseases. LeberMagenDarm. 1991. Vol. 21, No 1. P. 15–16. 19-22.
70. Tsen A., Alishahi Y., Rosenkranz L. Autoimmune pancreatitis and inflammatory bowel disease: an updated review. J ClinGastroenterol. 2017. Vol. 51, No 3. P. 208–214.
71. Tsesmeli N. E., Giannoulis K. E., Savopoulos C. G., Vretou E. E., Ekonomou I. A., Giannoulis E. K. Acute pancreatitis as a possible consequence of metronidazole during a relapse of ulcerative colitis. Eur J GastroenterolHepatol. 2007. Vol. 19, No 9. P. 805–806.
72. Uchida K., Okazaki K. Clinical and pathophysiological aspects of type 1 autoimmune pancreatitis. J Gastroenterol. 2018. Vol. 53, No 4. P. 475–483.
73. Ueki T., Kawamoto K., Otsuka Y., Minoda R., Maruo T., Matsumura K., Noma E. Prevalence and clinicopathological features of autoimmune pancreatitis in Japanese patients with inflammatory bowel disease. Pancreas. 2015. Vol. 44, No 3. P. 434–440.
74. Vavricka S. R., Schoepfer A., Scharl M., Lakatos P. L., Navarini A., Rogler G. Extraintestinal manifestations of inflammatory bowel disease. Inflamm Bowel Dis. 2015. Vol. 21, No 8. P. 1982–1992.
75. Weber P., Seibold F., Jenss H. Acute pancreatitis in Crohn's disease. J ClinGastroenterol. 1993. Vol. 17, No 4. P. 286–291.
76. Werlang M. E., Lewis M. D., Bartel M. J. Tumor Necrosis Factor Alpha Inhibitor-Induced Acute Pancreatitis. ACG Case Rep J. 2017. Vol. 4:e103.
77. Yadav D., Lowenfels A. B. The epidemiology of pancreatitis and pancreatic cancer. Gastroenterology. 2013. Vol. 144, No 6. P. 1252–1261.
78. Yung K., Oviedo J., Farraye F. A., Becker J. M., Andrews C. W. Jr, Lichtenstein D. Ampullary stenosis with biliary obstruction in duodenal Crohn's disease: a case report and review of the literature. Dig Dis Sci. 2005. Vol. 50, No 6. P. 1118–1121.
79. Zhang F. M., Xu C. F., Shan G. D., Chen H. T., Xu G. Q. Is gallstone disease associated with inflammatory bowel diseases? A meta-analysis. J Dig Dis. 2015. Vol. 16, No 11. P. 634–641.