Extraintestinal manifestations of inflammatory bowel diseases: modern conception and contribution to the disease insight


DOI: https://dx.doi.org/10.18565/therapy.2022.1.71-93

Bakulin I.G., Skalinskaya M.I., Skazyvaeva E.V., Rasmagina I.A., Zhuravleva M.S., Usachev R.A.

I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia, Saint Petersburg
Abstract. Due to the significant influence of the extra-intestinal manifestations on the prognosis and management of patients with inflammatory bowel diseases (IBD), it is relevant to study their pathogenesis, as well as to improve diagnostic and therapeutic approaches. The review article highlights modern international views on the pathogenesis of extra-intestinal manifestations in Crohn’s disease and ulcerative colitis and clinical diversity of the affected organs and systems disorders, including the musculoskeletal system, skin, oral cavity, renal, hepatobiliary and ocular systems, lungs and peripheral vessels. Information about the prevalence of the extra-intestinal manifestations in IBD varies. In general, according to the authors from various countries, the highest prevalence of the extra-intestinal manifestations was noted in Crohn’s disease, in female patients, in smokers, and patients with a longer duration of the disease. According to the modern concepts, extra-intestinal manifestations are considered to be the result of an antigen-specific immune response of the intestine to cells outside of the intestine, or an independent inflammatory event that is initiated as a result of the presence of genetic risk factors and/or environmental risk factors. In the present article the own data of the North-Western IBD Registry from Saint-Petersburg (Russia) on the frequency and features of extra-intestinal manifestations of IBD are represented, analyzed and compared with the world data.
Keywords: episcleritis, scleritis, aphthous stomatitis, sacroiliitis, pyoderma gangrenosum, spondyloarthritis, Crohn’s disease, inflammatory bowel diseases, primary sclerosing cholangitis, erythema nodosum, portal vein thrombosis, ulcerative colitis, uveitis
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Literature


  1. Ивашкин В.Т., Шелыгин Ю.А., Абдулганиева Д.И. с соавт. Клинические рекомендации по диагностике и лечению болезни Крона у взрослых (проект). Колопроктология. 2020; 2: 8–38. [Ivashkin V.T., Shelygin Yu.A., Abdulganieva D.I. et al. Crohn’s disease. Clinical recommendations (preliminary version). Koloproctologiya = Coloproctology. 2020; 2: 8–38 (In Russ.)]. https://dx.doi.org/10.33878/2073-7556-2020-19-2-8-38.

  2. Бакулин И.Г., Жигалова Т.Н., Латария Э.Л. с соавт. Опыт внедрения Федерального регистра пациентов с воспалительными заболеваниями кишечника в Санкт-Петербурге. Фарматека. 2017; S5: 56–59. [Bakulin I.G., Zhigalova T.N., Latariya Eh.L. et al. Experience of introduction of the Federal Registry of patients with inflammatory bowel diseases in Saint Petersburg. Farmateka. 2017; S5: 56–59 (In Russ.)].

  3. Маев И.В., Шелыгин Ю.А., Скалинская М.И. с соавт. Патоморфоз воспалительных заболеваний кишечника. Вестник Российской академии медицинских наук. 2020; 1: 27–35. [Maev I.V., Shelygin Yu.A., Skalinskaya M.I. et al. The pathomorphosis of inflammatory bowel diseases. Vestnik Rossiyskoy akademii meditsinskikh nauk = Annals of the Russian Academy of Medical Sciences. 2020; 1: 27–35 (In Russ.)]. https://dx.doi.org/10.15690/vramn1219.

  4. Bernstein C.N., Blanchard J.F., Rawsthorne P., Yu N. The prevalence of extraintestinal diseases in inflammatory bowel disease: a population-based study. Am J Gastroenterol. 2001; 96(4): 1116–22. https://dx.doi.org/10.1111/j.1572-0241.2001.03756.x.

  5. Walldorf J., Twarz M., Schober C. et al. High frequency of secondary, but not primary ocular manifestations of inflammatory bowel disease in patients treated at a tertiary care center. Eur J Gastroenterol Hepatol. 2018; 30(12): 1502–6. https://dx.doi.org/10.1097/MEG.0000000000001248.

  6. Karmiris K., Avgerinos A., Tavernaraki A. et al. Prevalence and characteristics of extra-intestinal manifestations in a large cohort of Greek patients with inflammatory bowel disease. J Crohns Colitis. 2016; 10(4): 429–36. https://dx.doi.org/10.1093/ecco-jcc/jjv232.

  7. Vavricka S.R., Rogler G., Gantenbein C. et al. Chronological order of appearance of extraintestinal manifestations relative to the time of IBD diagnosis in the Swiss Inflammatory Bowel Disease Cohort. Inflamm Bowel Dis. 2015; 21(8): 1794–800. https://dx.doi.org/10.1097/MIB.0000000000000429.

  8. Roth N., Biedermann L., Fournier N. et al. Occurrence of skin manifestations in patients of the Swiss Inflammatory Bowel Disease Cohort Study. PLoS One. 2019; 14(1): e0210436. https://dx.doi.org/10.1371/journal.pone.0210436.

  9. van Erp S.J., Brakenhoff L.K., van Gaalen F.A. et al. Classifying back pain and peripheral joint complaints in inflammatory bowel disease patients: A prospective longitudinal follow-up study. J Crohns Colitis. 2016; 10(2): 166–75. https://dx.doi.org/10.1093/ecco-jcc/jjv195.

  10. Severs M., Spekhorst L.M., Mangen M.J.J. et al. Sex-related differences in patients with inflammatory bowel disease: Results of 2 prospective cohort studies. Inflamm Bowel Dis. 2018; 24(6): 1298–306. https://dx.doi.org/10.1093/ibd/izy004.

  11. Roberts H., Rai S.N., Pan J. et al. Extraintestinal manifestations of inflammatory bowel disease and the influence of smoking. Digestion. 2014; 90(2): 122–29. https://dx.doi.org/10.1159/000363228.

  12. Severs M., van Erp S.J.H., van der Valk M.E. et al. Smoking is associated with extra-intestinal manifestations in inflammatory bowel disease. J Crohns Colitis. 2016; 10(4): 455–61. https://dx.doi.org/10.1093/ecco-jcc/jjv238.

  13. Jang H.J., Kang B., Choe B.H. The difference in extraintestinal manifestations of inflammatory bowel disease for children and adults. Transl Pediatr. 2019; 8(1): 4–15. https://dx.doi.org/10.21037/tp.2019.01.06.

  14. Grossman B.J., DeBenedetti C.D. Extraintestinal manifestations of chronic inflammatory bowel disease in children. Proc Inst Med Chic. 1970; 28(3): 119.

  15. Stawarski A., Iwanczak B., Krzesiek E., Iwanczak F. [Intestinal complications and extraintestinal manifestations in children with inflammatory bowel disease. Pol Merkur Lekarski. 2006; 20(115): 22–25 (in Polish)].

  16. Greuter T., Bertoldo F., Rechner R. et al. Extraintestinal manifestations of pediatric inflammatory bowel disease: Prevalence, presentation, and anti-TNF treatment. J Pediatr Gastroenterol Nutr. 2017; 65(2): 200–6. https://dx.doi.org/10.1097/MPG.0000000000001455.

  17. Breban M., Tap J., Leboime A. et al. Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann Rheum Dis. 2017; 76(9): 1614–22. https://dx.doi.org/10.1136/annrheumdis-2016-211064.

  18. Eppinga H., Thio H.B., Schreurs M.W.J. et al. Depletion of Saccharomyces cerevisiae in psoriasis patients, restored by Dimethylfumarate therapy (DMF). PloS One. 2017; 12(5): e0176955. https://dx.doi.org/10.1371/journal.pone.0176955.

  19. Kummen M., Holm K., Anmarkrud J.A. et al. The gut microbial profile in patients with primary sclerosing cholangitis is distinct from patients with ulcerative colitis without biliary disease and healthy controls. Gut. 2017; 66(4): 611–19. https://dx.doi.org/10.1136/gutjnl-2015-310500.

  20. Wen X., Hu X., Miao L. et al. Epigenetics, microbiota, and intraocular inflammation: New paradigms of immune regulation in the eye. Prog Retin Eye Res. 2018; 64: 84–95. https://dx.doi.org/10.1016/j.preteyeres.2018.01.001.

  21. Ciccia F., Guggino G., Rizzo A. et al. Type 3 innate lymphoid cells producing IL-17 and IL-22 are expanded in the gut, in the peripheral blood, synovial fluid and bone marrow of patients with ankylosing spondylitis. Ann Rheum Dis. 2015; 74(9): 1739–47. https://dx.doi.org/10.1136/annrheumdis-2014-206323.

  22. Cuthbert R.J., Fragkakis E.M., Dunsmuir R. et al. Brief report: Group 3 innate lymphoid cells in human enthesis. Arthritis Rheumatol. 2017; 69(9): 1816–22. https://dx.doi.org/10.1002/art.40150.

  23. Godefroy E., Alameddine J., Montassier E. et al. Expression of CCR6 and CXCR6 by gut-derived CD4+/CD8α+ T-regulatory cells, which are decreased in blood samples from patients with inflammatory bowel diseases. Gastroenterology. 2018; 155(4): 1205–17. https://dx.doi.org/10.1053/j.gastro.2018.06.078.

  24. Condliffe A.M., Kitchen E., Chilvers E.R. Neutrophil priming: Pathophysiological consequences and underlying mechanisms. Clin Sci (Lond). 1998; 94(5): 461–71. https://dx.doi.org/10.1042/cs0940461.

  25. Reeves E., James E. The role of polymorphic ERAP1 in autoinflammatory disease. Biosci Rep. 2018; 38(4): BSR20171503. https://dx.doi.org/10.1042/BSR20171503.

  26. Rogler G., Singh A., Kavanaugh A., Rubin D.T. Extraintestinal manifestations of inflammatory bowel disease: Current concepts, treatment, and implications for disease management. Gastroenterology. 2021; 161(4): 1118–32. https://dx.doi.org/10.1053/j.gastro.2021.07.042.

  27. Martin T.M., Smith J.R., Rosenbaum J.T. Anterior uveitis: Current concepts of pathogenesis and interactions with the spondyloarthropathies. Curr Opin Rheumatol. 2002; 14(4): 337–41. https://dx.doi.org/10.1097/00002281-200207000-00001.

  28. Peeters H., Vander Cruyssen B., Laukens D. et al. Radiological sacroiliitis, a hallmark of spondylitis, is linked with CARD15 gene polymorphisms in patients with Crohn’s disease. Ann Rheum Dis. 2004; 63(9): 1131–34. https://dx.doi.org/10.1136/ard.2004.021774.

  29. Weizman A., Huang B., Berel D. et al. Clinical, serologic, and genetic factors associated with pyoderma gangrenosum and erythema nodosum in inflammatory bowel disease patients. Inflamm Bowel Dis. 2014; 20(3): 525–33. https://dx.doi.org/10.1097/01.MIB.0000442011.60285.68.

  30. Kim J.M., Cheon J.H. Pathogenesis and clinical perspectives of extraintestinal manifestations in inflammatory bowel diseases. Intest Res. 2020; 18(3): 249–64. https://dx.doi.org/10.5217/ir.2019.00128.

  31. Cosnes J., Carbonnel F., Carrat F. et al. Effects of current and former cigarette smoking on the clinical course of Crohn’s disease. Aliment Pharmacol Ther. 1999; 13(11): 1403–11. https://dx.doi.org/10.1046/j.1365-2036.1999.00630.x.

  32. Savin Z., Kivity S., Yonath H., Yehuda S. Smoking and the intestinal microbiome. Arch Microbiol. 2018; 200(5): 677–84. https://dx.doi.org/10.1007/s00203-018-1506-2.

  33. Karreman M.C., Luime J.J., Hazes J.M.W., Weel A.E.A.M. The prevalence and incidence of axial and peripheral spondyloarthritis in inflammatory bowel disease: A systematic review and meta-analysis. J Crohns Colitis. 2017; 11(5): 631–42. https://dx.doi.org/10.1093/ecco-jcc/jjw199.

  34. Palm O., Moum B., Ongre A., Gran J.T. Prevalence of ankylosing spondylitis and other spondyloarthropathies among patients with inflammatory bowel disease: a population study (the IBSEN study). J Rheumatol. 2002; 29(3): 511–15.

  35. Horton D.B., Sherry D.D., Baldassano R.N., Weiss P.F. Enthesitis is an extraintestinal manifestation of pediatric inflammatory bowel disease. Ann Paediatr Rheumatol. 2012; 1(4): 10.5455/apr.102920121510. https://dx.doi.org/10.5455/apr.102920121510.

  36. Rudwaleit M., van der Heijde D., Landewe R. et al. The development of Assessment of SpondyloArthritis international Society classification criteria for axial spondyloarthritis (part II): Validation and final selection. Ann Rheum Dis. 2009; 68(6): 777–83. https://dx.doi.org/10.1136/ard.2009.108233.

  37. Sepriano A., Rubio R., Ramiro S. et al. Performance of the ASAS classification criteria for axial and peripheral spondyloarthritis: A systematic literature review and meta-analysis. Ann Rheum Dis. 2017; 76(5): 886–90. https://dx.doi.org/10.1136/annrheumdis-2016-210747.

  38. MacKay K., Mack C., Brophy S., Calin A. The Bath Ankylosing Spondylitis Radiology Index (BASRI): A new, validated approach to disease assessment. Arthritis Rheum. 1998; 41(12): 2263–70. https://dx.doi.org/10.1002/1529-0131(199812)41:12<2263::AID-ART23>3.0.CO;2-I.

  39. Garrett S., Jenkinson T., Kennedy L.G. et al. A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol. 1994; 21(12): 2286–91.

  40. Lukas C., Landewe R., Sieper J. et al. Development of an ASAS-endorsed disease activity score (ASDAS) in patients with ankylosing spondylitis. Ann Rheum Dis. 2009; 68(1): 18–24. https://dx.doi.org/10.1136/ard.2008.094870.

  41. Varkas G., Ribbens C., Louis E. et al. Expert consensus: practical algorithms for management of inflammatory bowel disease patients presenting with back pain or peripheral arthropathies. Aliment Pharmacol Ther. 2019; 50(11–12): 1204–13. https://dx.doi.org/10.1111/apt.15519.

  42. Stolwijk C., Pierik M., Landewe R. et al. Prevalence of self-reported spondyloarthritis features in a cohort of patients with inflammatory bowel disease. Can J Gastroenterol. 2013; 27(4): 199–205. https://dx.doi.org/10.1155/2013/139702.

  43. Tadbiri S., Peyrin-Biroulet L., Serrero M. et al. Impact of vedolizumab therapy on extra-intestinal manifestations in patients with inflammatory bowel disease: a multicentre cohort study nested in the OBSERV-IBD cohort. Aliment Pharmacol Ther. 2018; 47(4): 485–93. https://dx.doi.org/10.1111/apt.14419.

  44. Harbord M., Annese V., Vavricka S.R. et al. The First European Evidence-based Consensus on extra-intestinal manifestations in inflammatory bowel disease. J Crohns Colitis. 2016; 10(3): 239–54. https://dx.doi.org/10.1093/ecco-jcc/jjv213.

  45. Vavricka S.R., Schoepfer A., Scharl M. et al. Extraintestinal manifestations of inflammatory bowel disease. Inflamm Bowel Dis. 2015; 21(8): 1982–92. https://dx.doi.org/10.1097/MIB.0000000000000392.

  46. Vavricka S.R., Brun L., Ballabeni P. et al. Frequency and risk factors for extraintestinal manifestations in the Swiss inflammatory bowel disease cohort. Am J Gastroenterol. 2011; 106(1): 110–19. https://dx.doi.org/10.1038/ajg.2010.343.

  47. Greuter T., Navarini A., Vavricka S.R. Skin manifestations of inflammatory bowel disease. Clin Rev Allergy Immunol. 2017; 53(3): 413–27. https://dx.doi.org/10.1007/s12016-017-8617-4.

  48. States V., O’Brien S., Rai J.P. et al. Pyoderma gangrenosum in inflammatory bowel disease: A systematic review and meta-analysis. Dig Dis Sci. 2020; 65(9): 2675–85. https://dx.doi.org/10.1007/s10620-019-05999-4.

  49. Ashchyan H.J., Butler D.C., Nelson C.A. et al. The association of age with clinical presentation and comorbidities of pyoderma gangrenosum. JAMA Dermatol. 2018; 154(4): 409–13. https://dx.doi.org/10.1001/jamadermatol.2017.5978.

  50. Weenig R.H., Davis M.D.P., Dahl P.R., Su W.P.D. Skin ulcers misdiagnosed as pyoderma gangrenosum. N Engl J Med. 2002; 347(18): 1412–18. https://dx.doi.org/10.1056/NEJMoa013383.

  51. Yadav S., Singh S., Edakkanambeth Varayil J. et al. Hidradenitis suppurativa in patients with inflammatory bowel disease: A population-based cohort study in Olmsted County, Minnesota. Clin Gastroenterol Hepatol. 2016; 14(1): 65–70. https://dx.doi.org/10.1016/j.cgh.2015.04.173.

  52. Janse I.C., Koldijk M.J., Spekhorst L.M. et al. Identification of clinical and genetic parameters associated with hidradenitis suppurativa in inflammatory bowel disease. Inflamm Bowel Dis. 2016; 22(1): 106–13. https://dx.doi.org/10.1097/MIB.0000000000000579.

  53. Lukach A.J., Saul M.I., Ferris L.K., Swoger J.M. Risk Factors for Hidradenitis Suppurativa in Patients with Inflammatory Bowel Disease. Dig Dis Sci. 2018; 63(3): 755–60. https://dx.doi.org/10.1007/s10620-018-4919-5.

  54. Mylonas A., Conrad C. Psoriasis: Classical vs. paradoxical. The Yin-Yang of TNF and type I interferon. Front Immunol. 2018; 9: 2746. https://dx.doi.org/10.3389/fimmu.2018.02746.

  55. Boehncke W.H., Schon M.P. Psoriasis. Lancet. 2015; 386(9997): 983–94. https://dx.doi.org/10.1016/S0140-6736(14)61909-7.

  56. Nast A., Gisondi P., Ormerod A.D. et al. European S3-Guidelines on the systemic treatment of psoriasis vulgaris – Update 2015 – Short version—EDF in cooperation with EADV and IPC. J Eur Acad Dermatol Venereol. 2015; 29(12): 2277–94. https://dx.doi.org/10.1111/jdv.13354.

  57. 57. Elmets C.A., Leonardi C.L., Davis D.M.R. et al. Joint AAD-NPF guidelines of care for the management and treatment of psoriasis with awareness and attention to comorbidities. J Am Acad Dermatol. 2019; 80(4): 1073–113. https://dx.doi.org/10.1016/j.jaad.2018.11.058.

  58. Peyrin-Biroulet L., Van Assche G., Gomez-Ulloa D. et al. Systematic review of tumor necrosis factor antagonists in extraintestinal manifestations in inflammatory bowel disease. Clin Gastroenterol Hepatol. 2017; 15(1): 25–36.e27. https://dx.doi.org/10.1016/j.cgh.2016.06.025.

  59. Travis S., Innes N., Davies M.G. et al. Sweet’s syndrome: An unusual cutaneous feature of Crohn’s disease or ulcerative colitis. The South West Gastroenterology Group. Eur J Gastroenterol Hepatol. 1997; 9(7): 715–20. https://dx.doi.org/10.1097/00042737-199707000-00013.

  60. Imhof L., Meier B., Frei P. et al. Severe Sweet’s syndrome with elevated cutaneous interleukin-1β after azathioprine exposure: Case report and review of the literature. Dermatol Basel Switz. 2015; 230(4): 293–98. https://dx.doi.org/10.1159/000371879.

  61. Patel A.V., Jones D.M., Hill J.C., MacDermott R.P. Development of metastatic Crohn’s disease of the skin while on anti-TNF biologics. Inflamm Bowel Dis. 2012; 18(6): 1188–90. https://dx.doi.org/10.1002/ibd.22904.

  62. Cury D.B., Moss A.C., Elias G., Nakao A. Adalimumab for cutaneous metastatic Crohn’s disease. Inflamm Bowel Dis. 2010; 16(5): 723–24. https://dx.doi.org/10.1002/ibd.21082.

  63. Bogenrieder T., Rogler G., Vogt T. et al. Orofacial granulomatosis as the initial presentation of Crohn’s disease in an adolescent. Dermatol Basel Switz. 2003; 206(3): 273–78. https://dx.doi.org/10.1159/000068900.

  64. Girlich C., Bogenrieder T., Palitzsch K.D. et al. Orofacial granulomatosis as initial manifestation of Crohn’s disease: a report of two cases. Eur J Gastroenterol Hepatol. 2002; 14(8): 873–76. https://dx.doi.org/10.1097/00042737-200208000-00010.

  65. Ribaldone D.G., Brigo S., Mangia M. et al. Oral manifestations of inflammatory bowel disease and the role of non-invasive surrogate markers of disease activity. Med Basel Switz. 2020; 7(6): E33. https://dx.doi.org/10.3390/medicines7060033.

  66. Lauritano D., Boccalari E., Di Stasio D. et al. Prevalence of oral lesions and correlation with intestinal symptoms of inflammatory bowel disease: A systematic review. Diagn Basel Switz. 2019; 9(3): E77. https://dx.doi.org/10.3390/diagnostics9030077.

  67. Vavricka S.R., Manser C.N., Hediger S. et al. Periodontitis and gingivitis in inflammatory bowel disease: a case-control study. Inflamm Bowel Dis. 2013; 19(13): 2768–77. https://dx.doi.org/10.1097/01.MIB.0000438356.84263.3b.

  68. Brito F., Zaltman C., Carvalho A.T.P. et al. Subgingival microflora in inflammatory bowel disease patients with untreated periodontitis. Eur J Gastroenterol Hepatol. 2013; 25(2): 239–45. https://dx.doi.org/10.1097/MEG.0b013e32835a2b70.

  69. Taleban S., Li D., Targan S.R. et al. Ocular manifestations in inflammatory bowel disease are associated with other extra-intestinal manifestations, gender, and genes implicated in other immune-related traits. J Crohns Colitis. 2016; 10(1): 43–49. https://dx.doi.org/10.1093/ecco-jcc/jjv178.

  70. Troncoso L.L., Biancardi A.L., de Moraes H.V., Zaltman C. Ophthalmic manifestations in patients with inflammatory bowel disease: A review. World J Gastroenterol. 2017; 23(32): 5836–48. https://dx.doi.org/10.3748/wjg.v23.i32.5836.

  71. Zeitz J., Mullhaupt B., Fruehauf H. et al. Hepatic failure due to hepatitis B reactivation in a patient with ulcerative colitis treated with prednisone. Hepatol Baltim Md. 2009; 50(2): 653–54. https://dx.doi.org/10.1002/hep.23035.

  72. Palmela C., Peerani F., Castaneda D. et al. Inflammatory bowel disease and primary sclerosing cholangitis: A review of the phenotype and associated specific features. Gut Liver. 2018; 12(1): 17–29. https://dx.doi.org/10.5009/gnl16510.

  73. de Vries A.B., Janse M., Blokzijl H., Weersma R.K. Distinctive inflammatory bowel disease phenotype in primary sclerosing cholangitis. World J Gastroenterol. 2015; 21(6): 1956–71. https://dx.doi.org/10.3748/wjg.v21.i6.1956.

  74. Rossi R.E., Conte D., Massironi S. Primary sclerosing cholangitis associated with inflammatory bowel disease: An update. Eur J Gastroenterol Hepatol. 2016; 28(2): 123–31. https://dx.doi.org/10.1097/MEG.0000000000000532.

  75. Little R., Wine E., Kamath B.M. et al. Gut microbiome in primary sclerosing cholangitis: A review. World J Gastroenterol. 2020; 26(21): 2768–80. https://dx.doi.org/10.3748/wjg.v26.i21.2768.

  76. Jose F.A., Garnett E.A., Vittinghoff E. et al. Development of extraintestinal manifestations in pediatric patients with inflammatory bowel disease. Inflamm Bowel Dis. 2009; 15(1): 63–68. https://dx.doi.org/10.1002/ibd.20604.

  77. Rocha H.C., Vilela E.G. Clinical aspects and prognosis of patients with inflammatory bowel disease associated with autoimmune liver diseases. Gastroenterol Hepatol. 2021; S0210-5705(21)00153-9. https://dx.doi.org/10.1016/j.gastrohep.2021.03.011. Online ahead of print.

  78. Woodward J., Neuberger J. Autoimmune overlap syndromes. Hepatol Baltim Md. 2001; 33(4): 994–1002. https://dx.doi.org/10.1053/jhep.2001.23316.

  79. Gregorio G.V., Portmann B., Karani J. et al. Autoimmune hepatitis/sclerosing cholangitis overlap syndrome in childhood: A 16-year prospective study. Hepatol Baltim Md. 2001; 33(3): 544–53. https://dx.doi.org/10.1053/jhep.2001.22131.

  80. Venkatesh P.G., Navaneethan U., Shen B. Hepatobiliary disorders and complications of inflammatory bowel disease. J Dig Dis. 2011; 12(4): 245–56. https://dx.doi.org/10.1111/j.1751-2980.2011.00511.x.

  81. Braun M., Fraser G.M., Kunin M. et al. Mesalamine-induced granulomatous hepatitis. Am J Gastroenterol. 1999; 94(7): 1973–74. https://dx.doi.org/10.1111/j.1572-0241.1999.01245.x.

  82. Dastis S.N., Latinne D., Sempoux C., Geubel A.P. Ulcerative colitis associated with IgG4 cholangitis: similar features in two HLA identical siblings. J Hepatol. 2009; 51(3): 601–5. https://dx.doi.org/10.1016/j.jhep.2009.05.032.

  83. Okazaki K., Uchida K., Koyabu M. et al. Recent advances in the concept and diagnosis of autoimmune pancreatitis and IgG4-related disease. J Gastroenterol. 2011; 46(3): 277–88. https://dx.doi.org/10.1007/s00535-011-0386-x.

  84. Novotny I., Dite P., Trna J. et al. Immunoglobulin G4-related cholangitis: A variant of IgG4-related systemic disease. Dig Dis Basel Switz. 2012; 30(2): 216–19. https://dx.doi.org/10.1159/000336706.

  85. Saroli Palumbo C., Restellini S., Chao C.Y. et al. Screening for nonalcoholic fatty liver disease in inflammatory bowel diseases: A cohort study using transient elastography. Inflamm Bowel Dis. 2019; 25(1): 124–33. https://dx.doi.org/10.1093/ibd/izy200.

  86. Langholz E., Munkholm P., Nielsen O.H. et al. Incidence and prevalence of ulcerative colitis in Copenhagen county from 1962 to 1987. Scand J Gastroenterol. 1991; 26(12): 1247–56. https://dx.doi.org/10.3109/00365529108998621.

  87. Nagahori M., Hyun S.B., Totsuka T. et al. Prevalence of metabolic syndrome is comparable between inflammatory bowel disease patients and the general population. J Gastroenterol. 2010; 45(10): 1008–13. https://dx.doi.org/10.1007/s00535-010-0247-z.

  88. Lapumnuaypol K., Kanjanahattakij N., Pisarcik D. et al. Effects of inflammatory bowel disease treatment on the risk of nonalcoholic fatty liver disease: a meta-analysis. Eur J Gastroenterol Hepatol. 2018; 30(8): 854–60. https://dx.doi.org/10.1097/MEG.0000000000001144.

  89. Magrì S., Paduano D., Chicco F. et al. Nonalcoholic fatty liver disease in patients with inflammatory bowel disease: Beyond the natural history. World J Gastroenterol. 2019; 25(37): 5676–86. https://dx.doi.org/10.3748/wjg.v25.i37.5676.

  90. Nakayama M., Tsuji H., Shimono J. et al. Primary biliary cirrhosis associated with ulcerative colitis. Fukuoka Igaku Zasshi. 2001; 92(10): 354–59.

  91. Xiao W.B., Liu Y.L. Primary biliary cirrhosis and ulcerative colitis: A case report and review of literature. World J Gastroenterol. 2003; 9(4): 878–80. https://dx.doi.org/10.3748/wjg.v9.i4.878.

  92. Ohge H., Takesue Y., Yokoyama T. et al. Progression of primary biliary cirrhosis after proctocolectomy for ulcerative colitis. J Gastroenterol. 2000; 35(11): 870–72. https://dx.doi.org/10.1007/s005350070026.

  93. Greenstein A.J., Sachar D.B., Panday A.K. et al. Amyloidosis and inflammatory bowel disease. A 50-year experience with 25 patients. Medicine (Baltimore). 1992; 71(5): 261–70. https://dx.doi.org/10.1097/00005792-199209000-00001.

  94. Wester A.L., Vatn M.H., Fausa O. Secondary amyloidosis in inflammatory bowel disease: a study of 18 patients admitted to Rikshospitalet University Hospital, Oslo, from 1962 to 1998. Inflamm Bowel Dis. 2001; 7(4): 295–300. https://dx.doi.org/10.1097/00054725-200111000-00003.

  95. Molina Infante J., Banares Canizares R., Gomez Camarero J., Perez Calle J.L. [Liver abscess and Crohn’ disease. Report of 3 cases]. Gastroenterol Hepatol. 2004; 27(5): 317–19 (In Spanish)]. https://dx.doi.org/10.1016/s0210-5705(03)70468-3.

  96. Bernabeu J.L., Leo E., Trigo C. et al. Crohn’s disease and liver abscess due to Pediococcus sp. Inflamm Bowel Dis. 2011; 17(10): 2207–8. https://dx.doi.org/10.1002/ibd.21622.

  97. Aguas M., Bastida G., Nos P. et al. Septic thrombophlebitis of the superior mesenteric vein and multiple liver abscesses in a patient with Crohn’s disease at onset. BMC Gastroenterol. 2007; 7: 22. https://dx.doi.org/10.1186/1471-230X-7-22.

  98. Parente F., Pastore L., Bargiggia S. et al. Incidence and risk factors for gallstones in patients with inflammatory bowel disease: A large case-control study. Hepatol Baltim Md. 2007; 45(5): 1267–74. https://dx.doi.org/10.1002/hep.21537.

  99. Navaneethan U., Shen B. Hepatopancreatobiliary manifestations and complications associated with inflammatory bowel disease. Inflamm Bowel Dis. 2010; 16(9): 1598–619. https://dx.doi.org/10.1002/ibd.21219.

  100. Mibu R., Makino I., Chijiiwa K. Gallstones and their composition in patients with ileoanal anastomosis. J Gastroenterol. 1995; 30(3): 413–15. https://dx.doi.org/10.1007/BF02347521.

  101. Broide E., Dotan I., Weiss B. et al. Idiopathic pancreatitis preceding the diagnosis of inflammatory bowel disease is more frequent in pediatric patients. J Pediatr Gastroenterol Nutr. 2011; 52(6): 714–17. https://dx.doi.org/10.1097/MPG.0b013e3182065cad.

  102. Pimentel A.M., Rocha R., Santana G.O. Crohn’s disease of esophagus, stomach and duodenum. World J Gastrointest Pharmacol Ther. 2019; 10(2): 35–49. https://dx.doi.org/10.4292/wjgpt.v10.i2.35.

  103. Suk Lee Y., Kim N.H., Hyuk Son J. et al. Type 2 autoimmune pancreatitis with Crohn’s disease. Intern Med Tokyo Jpn. 2018; 57(20): 2957–62. https://dx.doi.org/10.2169/internalmedicine.0213-17.

  104. Klebl F.H., Bataille F., Huy C. et al. Association of antibodies to exocrine pancreas with subtypes of Crohn’s disease. Eur J Gastroenterol Hepatol. 2005; 17(1): 73–77. https://dx.doi.org/10.1097/00042737-200501000-00015.

  105. Heikius B., Niemela S., Lehtola J., Karttunen T.J. Elevated pancreatic enzymes in inflammatory bowel disease are associated with extensive disease. Am J Gastroenterol. 1999; 94(4): 1062–69. https://dx.doi.org/10.1111/j.1572-0241.1999.01015.x.

  106. Eliadou E., Moleiro J., Ribaldone D.G. et al. Interstitial and granulomatous lung disease in inflammatory bowel disease patients. J Crohns Colitis. 2020; 14(4): 480–89. https://dx.doi.org/10.1093/ecco-jcc/jjz165.

  107. Bradley B., Branley H.M., Egan J.J. et al. Interstitial lung disease guideline: the British Thoracic Society in collaboration with the Thoracic Society of Australia and New Zealand and the Irish Thoracic Society. Thorax. 2008; 63 Suppl 5: v1–58. https://dx.doi.org/10.1136/thx.2008.101691.

  108. Murthy S.K., Robertson McCurdy A.B., Carrier M., McCurdy J.D. Venous thromboembolic events in inflammatory bowel diseases: A review of current evidence and guidance on risk in the post-hospitalization setting. Thromb Res. 2020; 194: 26–32. https://dx.doi.org/10.1016/j.thromres.2020.06.005.

  109. Talbot R.W., Heppell J., Dozois R.R., Beart R.W. Vascular complications of inflammatory bowel disease. Mayo Clin Proc. 1986; 61(2): 140–45. https://dx.doi.org/10.1016/s0025-6196(12)65200-8.

  110. Sridhar A.R.M., Parasa S., Navaneethan U. et al. Comprehensive study of cardiovascular morbidity in hospitalized inflammatory bowel disease patients. J Crohns Colitis. 2011; 5(4): 287–94. https://dx.doi.org/10.1016/j.crohns.2011.01.011.

  111. Danese S., Papa A., Saibeni S. et al. Inflammation and coagulation in inflammatory bowel disease: The clot thickens. Am J Gastroenterol. 2007; 102(1): 174–86. https://dx.doi.org/10.1111/j.1572-0241.2006.00943.x.

  112. Sinagra E., Aragona E., Romano C. et al. The role of portal vein thrombosis in the clinical course of inflammatory bowel diseases: Report on three cases and review of the literature. Gastroenterol Res Pract. 2012; 2012: 916428. https://dx.doi.org/10.1155/2012/916428.

  113. Zanoli L., Mikhailidis D.P., Bruno R.M. et al. Aortic stiffening is an extraintestinal manifestation of inflammatory bowel disease: Review of the literature and expert panel statement. Angiology. 2020; 71(8): 689–97. https://dx.doi.org/10.1177/0003319720918509.

  114. Panhwar M.S., Mansoor E., Al-Kindi S.G. et al. Risk of myocardial infarction in inflammatory bowel disease: A population-based national study. Inflamm Bowel Dis. 2019; 25(6): 1080–87. https://dx.doi.org/10.1093/ibd/izy354.

  115. Singh A.G., Crowson C.S., Singh S. et al. Risk of cerebrovascular accidents and ischemic heart disease in cutaneous lupus erythematosus: A population-based cohort study. Arthritis Care Res. 2016; 68(11): 1664–70. https://dx.doi.org/10.1002/acr.22892.


About the Autors

Igor G. Bakulin, MD, professor, head of the Department of propaedeutics of internal diseases, gastroenterology and dietology named after S.M. Ryss, I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 195027, Saint Petersburg, 47/24 Piskarevsky Drive. E-mail: igbakulin@yandex.ru.
ORCID: https://orcid.org/0000-0002-6151-2021
Maria I. Skalinskaya, PhD, associate professor, associate professor of the Department of propaedeutics of internal diseases, gastroenterology and dietology named after S.M. Ryss, I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 195027, Saint Petersburg, 47/24 Piskarevsky Drive.
E-mail: mskalinskaya@yahoo.com. ORCID: https://orcid.org/0000-0003-0769-8176
Ekaterina V. Skazyvaeva, PhD, associate professor, associate professor of the Department of propaedeutics of internal diseases, gastroenterology and dietology named after S.M. Ryss, I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 195027, Saint Petersburg, 47/24 Piskarevsky Drive.
E-mail: skazyvaeva@yandex.ru. ORCID: https://orcid.org/0000-0002-8563-6870
Irina A. Rasmagina, postgraduate student at the Department of propaedeutics of internal diseases, gastroenterology and dietology named after S.M. Ryss, I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 195027, Saint Petersburg, 47/24 Piskarevsky Drive. E-mail: irenerasmagina@gmail.com.
ORCID: https://orcid.org/0000-0003-3525-3289
Maria S. Zhuravleva, PhD, associate professor of the Department of propaedeutics of internal diseases, gastroenterology and dietology named after S.M. Ryss, I.I. Mechnikov North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 195027, Saint Petersburg, 47/24 Piskarevsky Drive. E-mail: ms_zhuravleva@mail.ru.
ORCID: https://orcid.org/0000-0003-4838-5707
Roman A. Usachev, student of the Faculty of general medicine, North-Western State Medical University of the Ministry of Healthcare of Russia. Address: 191015, Saint Petersburg, 41 Kirochnaya Str. E-mail: roman.usachev4@gmail.com. ORCID: https://orcid.org/0000-0002-4796-0063


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