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Russian Journal of Gastroenterology, Hepatology, Coloproctology

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Diagnosis and Treatment of Patients with Autoimmune Hepatitis (Experts’ Agreement)

https://doi.org/10.22416/1382-4376-2024-34-6-100-119

Abstract

Background. In the last decade, the understanding of the pathogenesis of autoimmune hepatitis (AIH) has significantly deepened, based on the results of new clinical studies some diagnostic issues have been revised and immunosuppressive therapy regimens have been optimized.
Materials and methods. The latest Russian clinical guidelines for the diagnosis and treatment of AIH were presented in 2013; and in 2017, the first Russian agreement on the diagnosis and treatment of AIH was held. Updating approaches to the management of patients with AIH necessitated next systematization for use in clinical practice. In February 2024, the final session was held to discuss the provisions of the second agreement on the diagnosis and treatment of AIH.
Results. This publication presents the main discussion points of the agreement regarding methods and algorithms for detecting autoantibodies, the role of liver biopsy, revised morphological criteria for AIH, optimized immunosuppressive therapy regimens, updated criteria for assessing the response to therapy.
Conclusions. The agreement was the result of the work of a group of experts on the diagnosis and treatment of AIH and represents the basis for the creation of updated federal clinical guidelines.

About the Authors

Yu. G. Sandler
Loginov Moscow Clinical Scientific Center
Russian Federation

Yuliya G. Sandler — Cand. Sci. Med., Senior Researcher of the Department of Hepatology

111123, Moscow, Entuziastov highway, 86 


E. V. Vinnitskaya
Loginov Moscow Clinical Scientific Center
Russian Federation

Elena V. Vinnitskaya — Dr. Sci. (Med.), Head of the Department of Hepatology

111123, Moscow, Entuziastov highway, 86


K. L. Raikhelson
Saint Petersburg State University
Russian Federation

Karina L. Raikhelson — Dr. Sci. (Med.), Professor of the Scientific and Educational Center of Gastroenterology and Hepatology

199226, Saint Petersburg, Korablestroiteley str., 20–1


K. V. Ivashkin
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Konstantin V. Ivashkin — Dr. Sci. Med., Professor of the Department of Propaedeutics of Internal Medicine, Gastroenterology and Hepatology

119435, Moscow, Pogodinskaya str., 1, build. 1


S. N. Batskikh
Loginov Moscow Clinical Scientific Center
Russian Federation

Sergey N. Batskikh — Dr. Sci. (Med.), Leading Researcher of the Department of Hepatology

111123, Moscow, Entuziastov highway, 86


E. N. Aleksandrova
Loginov Moscow Clinical Scientific Center
Russian Federation

Elena N. Aleksandrova — Dr. Sci. (Med.), Head of the Laboratory of Clinical Immunology

111123, Moscow, Entuziastov highway, 86


D. T. Abdurakhmanov
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Dzhamal T. Abdurakhmanov — Dr. Sci. (Med.), Professor of the Department of Internal, Occupational Diseases and Pulmonology

119435, Moscow, Pogodinskaya str., 1, build. 1


D. I. Abdulganieva
Kazan State Medical University
Russian Federation

Diana I. Abdulganieva — Dr. Sci. Med., Professor, Head of the Department of Hospital Therapy

420012, Kazan, Butlerova str., 49


I. G. Bakulin
North-Western State Medical University named after I.I. Mechnikov
Russian Federation

Igor G. Bakulin — Dr. Sci. (Med.), Professor, Head of the Department of Propaedeutics of Internal Medicine, Gastroenterology and Dietetics named after S.M. Ryss

191015, Saint Petersburg, Kirochnaya str., 41


A. O. Bueverov
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Alexey O. Bueverov — Dr. Sci. (Med.), Professor at the Department of Medical and Social Expertise, Emergency and Pathogenetic Therapy

119435, Moscow, Pogodinskaya str., 1, build. 1


S. L. Vorobyev
OOO National Center for Clinical Morphological Diagnostics
Russian Federation

Sergey L. Vorobyev — Cand. Sci. (Med.), Director

192071, Saint Petersburg, Slavy Ave., 32, lit. A


O. A. Gerasimova
Saint Petersburg State University; Russian Scientific Center for Radiology and Surgical Technologies named after Academician A.M. Granov
Russian Federation

Olga A. Gerasimova — Dr. Sci. Med., Professor of the Scientific and Educational Center of Gastroenterology and Hepatology; Head of the Outpatient Center for Transplantology, Hepatology and Nephrology

199226, Saint Petersburg, Korablestroiteley str., 20–1


A. I. Dolgushina
South Ural State Medical University
Russian Federation

Anastasia I. Dolgushina — Dr. Sci. (Med.), Head of the Department of Hospital Therapy

454092, Chelyabinsk, Vorovskogo str., 64


M. S. Zhuravleva
North-Western State Medical University named after I.I. Mechnikov
Russian Federation

Mariia S. Zhuravleva — Cand. Sci. (Med.), Associate Professor of the Department of Propaedeutics of Internal Medicine, Gastroenterology and Dietetics named after S.M. Ryss

191015, Saint Petersburg, Kirochnaya str., 41


L. Yu. Ilchenko
N.I. Pirogov Russian National Research Medical University
Russian Federation

Liudmila Yu. Ilchenko — Dr. Sci. (Med.), Professor, Professor of the Department of Hospital Therapy named after Academician G.I. Storozhakov, N.I. Pirogov Russian National Research Medical University

117513, Moscow, Ostrovityanova str., 1


V. E. Karev
Pediatric Research and Clinical Center for Infectious Diseases under the Federal Medical Biological Agency
Russian Federation

Vadim E. Karev — Dr. Sci. (Med.), Head of the Department of Tissue and Pathomorphological Research Methods

197022, Saint Petersburg, Professora Popova str., 9


N. V. Korochanskaya
Kuban State Medical University
Russian Federation

 Natalia V. Korochanskaya — Dr. Sci. (Med.), Professor of the Department of Surgery No. 3 of the Faculty of Advanced Training and Professional Retraining of Specialists

350063, Krasnodar, Mitrofana Sedina str., 4 


I. L. Kliaritskaia
V.I. Vernadsky Crimean Federal University
Russian Federation

Irina L. Kliaritskaia — Dr. Sci. (Med.), Professor, Head of the Department of Therapy, Gastroenterology, Cardiology and General Medical Practice (Family Medicine) of the Fa-culty of Training of Highly Qualified Medical Personnel and Continuing Professional Education of the S.I. Georgievsky Medical Academy

295051, Simferopol, Lenina Blvd, 5/7


N. S. Karnaukhov
Loginov Moscow Clinical Scientific Center
Russian Federation

Nikolay S. Karnaukhov — Cand. Sci. (Med.), Head of the Department of Pathomorphology

111123, Moscow, Entuziastov highway, 86


S. V. Lapin
Academician I.P. Pavlov First St. Petersburg State Medical University
Russian Federation

Sergey V. Lapin — Cand. Sci. (Med.), Head of the Laboratory for Diagnostics of Autoimmune Diseases of the Scientific and Methodological Center for Molecular Medicine of the Ministry of Health of the Russian Federation

197101, Saint Petersburg, L’va Tolstovo str., 6-8


M. A. Livzan
Omsk State Medical University
Russian Federation

Maria A. Livzan — Dr. Sci. (Med.), Corresponding Member of the Russian Academy of Sciences, Professor, Head of the Department of Faculty Therapy and Gastroenterology, Rector

644099, Omsk, Lenina str., 12


M. V. Maevskaya
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Marina V. Maevskaya — Dr. Sci. (Med.), Professor, Consultant at the Diagnostic and Treatment Department of the University Clinical Hospital No. 2

119048, Moscow, Trubetskaya str., 8/2


N. V. Marchenko
Russian Scientific Center for Radiology and Surgical Technologies named after Academician A.M. Granov
Russian Federation

Natalia V. Marchenko — Cand. Sci. Med., Associate Professor of the Scientific and Educational Center of Gastroenterology and Hepatology, Saint Petersburg State University; Gastroenterologist

199226, Saint Petersburg, Korablestroiteley str., 20


T. P. Nekrasova
I.M. Sechenov First Moscow State Medical University (Sechenov University)
Russian Federation

Tatiyana P. Nekrasova — Cand. Sci. (Med.), Associate Professor at the Institute of Clinical Morphology and Digital Pathology

119435, Moscow, Pogodinskaya str., 1, build. 1


I. G. Nikitin
N.I. Pirogov Russian National Research Medical University
Russian Federation

Igor G. Nikitin — Dr. Sci. (Med.), Professor, Head of the Department of Hospital Therapy No. 2 of the Faculty of Therapy

117513, Moscow, Ostrovityanova str., 1


A. A. Novikov
Loginov Moscow Clinical Scientific Center
Russian Federation

Alexander A. Novikov — Dr. Sci. (Med.), Leading Researcher of the Laboratory of Clinical Immunology

111123, Moscow, Entuziastov highway, 86


R. G. Saifutdinov
Kazan State Medical Academy — Branch Campus of the Russian Medical Academy of Continuous Professional Education
Russian Federation

Rafik G. Saifutdinov — Dr. Sci. (Med.), Head of the Department of Therapy

420012, Kazan, Butlerova str., 36 


E. V. Skazyvaeva
North-Western State Medical University named after I.I. Mechnikov
Russian Federation

Ekaterina V. Skazyvaeva — Cand. Sci. (Med.), Associate Professor of the Department of Propaedeutics of Internal Medicine, Gastroenterology and Dietetics named after S.M. Ryss

191015, St. Petersburg, Kirochnaya str., 41


V. E. Syutkin
Medical and Biological University of Innovation and Continuous Education, State Research Center — Byrnasyan Federal Medical Biophysical Center of Federal Biological Agency; N.V. Sklifosovsky Research Institute for Emergency Care of the Moscow City Health Department
Russian Federation

Vladimir E. Syutkin — Dr. Sci. (Med.), Professor of the Department of Surgery with Courses in Oncosurgery, Endoscopy, Surgical Pathology, Clinical Transplantology and Organ Donation; Leading Researcher of the Liver Transplant Department

129010, Moscow, Bolshaya Sukharevskaya sq., 3


M. K. Prashnova
Russian Scientific Center for Radiology and Surgical Technologies named after Academician A.M. Granov
Russian Federation

Mariya K. Prashnova — Cand. Sci. (Med.), Teaching Assistant of the Scientific and Educational Center of Gastroenterology and Hepatology

199226, Saint Petersburg, Korablestroiteley str., 20


T. Yu. Khaymenova
Loginov Moscow Clinical Scientific Center
Russian Federation

Tatyana Yu. Khaymenova — Cand. Sci. (Med.), Head of the Department of Liver Diseases

111123, Moscow, Entuziastov highway, 86


S. G. Khomerik
Loginov Moscow Clinical Scientific Center
Russian Federation

Sergey G. Khomeriki — Dr. Sci. (Med.), Professor, Head of the Pathomorphology Laboratory

111123, Moscow, Entuziastov highway, 86


References

1. Ivashkin V.T., Bueverov A.O., Abdulganieva D.I. Clinical guidelines for the diagnosis and treatment of autoimmune hepatitis. Moscow, 2013. (In Russ.).

2. Lamba M., Ngu J.H., Stedman C.A.M. Trends in incidence of autoimmune liver diseases and increasing incidence of autoimmune hepatitis. Clin Gastroenterol Hepatol. 2021;19(3):573–9.e1. DOI: 10.1016/j.cgh.2020.05.061

3. Hahn J.W., Yang H.R., Moon J.S., Chang J.Y., Lee K., Kim G.A., et al. Global incidence and prevalence of autoimmune hepatitis, 1970-2022: A systematic review and meta-analysis. Eclinicalmedicine. 2023;65:102280. DOI: 10.1016/j.eclinm.2023.102280

4. van den Brand F.F., van der Veen K.S., de Boer Y.S., van Gerven N.M., Lissenberg-Witte B.I., Beuers U., et al.; Dutch Autoimmune Hepatitis Study Group. Increased mortality among patients with vs without cirrhosis and autoimmune hepatitis. Clin Gastroenterol Hepatol. 2019;17(5):940–7.e2. DOI: 10.1016/j.cgh.2018.09.046

5. Bittermann T., Lewis J.D., Levy C., Goldberg D.S. Sociodemographic and geographic differences in the US epidemiology of autoimmune hepatitis with and without cirrhosis. Hepatology. 2023;77(2):367–78. DOI: 10.1002/hep.32653

6. Guyatt G.H., Oxman A.D., Vist G.E., Kunz R., FalckYtter Y., Alonso-Coello P., et al.; GRADE Working Group. GRADE: An emerging consensus on rating quality 36 of evidence and strength of recommendations. BMJ. 2008;336(7650):924–6. DOI: 10.1136/bmj.39489.470347.AD

7. McGonagle D., McDermott M.F. A proposed classification of the immunological diseases. PLoS Med. 2006;3(8):e297. DOI: 10.1371/journal.pmed.0030297

8. Alvarez F., Berg P.A., Bianchi F.B., Bianchi L., Burroughs A.K., Cancado E.L., et al. International autoimmune hepatitis group report: Review of criteria for diagnosis of autoimmune hepatitis. J Hepatol. 1999;31(5):929–38. DOI: 10.1016/s0168-8278(99)80297-9

9. Hennes E.M., Zeniya M., Czaja A.J., Parés A., Dalekos G.N., Krawitt E.L., et al.; International Autoimmune Hepatitis Group. Simplified criteria for the diagnosis of autoimmune hepatitis. Hepatology. 2008;48(1):169–76. DOI: 10.1002/hep.22322

10. Wang Q., Yang F., Miao Q., Krawitt E.L., Gershwin M.E., Ma X. The clinical phenotypes of autoimmune hepatitis: A comprehensive review. J Autoimmun. 2016;66:98–107. DOI: 10.1016/j.jaut.2015.10.006

11. Czaja A.J., Bayraktar Y. Non-classical phenotypes of autoimmune hepatitis and advances in diagnosis and treatment. World J Gastroenterol. 2009;15(19):2314–28. DOI: 10.3748/wjg.15.2314

12. Terziroli Beretta-Piccoli B., Mieli-Vergani G., Vergani D. Autoimmune hepatitis: Serum autoantibodies in clinical practice. Clin Rev Allergy Immunol. 2022;63(2):124–37. DOI: 10.1007/s12016-021-08888-9

13. Czaja A.J. Autoantibodies as prognostic markers in autoimmune liver disease. Dig Dis Sci. 2010;55(8):2144–61. DOI: 10.1007/s10620-010-1268-4

14. Baeres M., Herkel J., Czaja A.J., Wies I., Kanzler S., Cancado E.L., et al. Establishment of standardised SLA/LP immunoassays: Specificity for autoimmune hepatitis, worldwide occurrence, and clinical characteristics. Gut. 2002;51(2):259–64. DOI: 10.1136/gut.51.2.259

15. Efe C., Ozaslan E., Wahlin S., Purnak T., Muratori L., Quarneti C., et al. Antibodies to soluble liver antigen in patients with various liver diseases: A multicentre study. Liver Int. 2013;33(2):190–6. DOI: 10.1111/liv.12022

16. Vergani D., Alvarez F., Bianchi F.B., Cançado E.L., Mackay I.R., Manns M.P., et al.; International Autoimmune Hepatitis Group. Liver autoimmune serology: A consensus statement from the committee for autoimmune serology of the International Autoimmune Hepatitis Group. J Hepatol. 2004;41(4):677–83. DOI: 10.1016/j.jhep.2004.08.002

17. Sebode M., Weiler-Normann C., Liwinski T., Schramm C. Autoantibodies in autoimmune liver disease-clinical and diagnostic relevance. Front Immunol. 2018;9:609. DOI: 10.3389/fimmu.2018.00609

18. Terjung B., Söhne J., Lechtenberg B., Gottwein J., Muennich M., Herzog V., et al. p-ANCAs in autoimmune liver disorders recognise human beta-tubulin isotype 5 and cross-react with microbial protein FtsZ. Gut. 2010;59(6):808–16. DOI: 10.1136/gut.2008.157818

19. Yimam K.K., Bowlus C.L. Diagnosis and classification of primary sclerosing cholangitis. Autoimmun Rev. 2014;13(4–5):445–50. DOI: 10.1016/j.autrev.2014.01.040

20. Terziroli Beretta-Piccoli B., Mieli-Vergani G., Vergani D. Serology in autoimmune hepatitis: A clinical-practice approach. Eur J Intern Med. 2018;48:35–43. DOI: 10.1016/j.ejim.2017.10.006

21. Mack C.L., Adams D., Assis D.N., Kerkar N., Manns M.P., Mayo M.J., et al. Diagnosis and management of autoimmune hepatitis in adults and children: 2019 practice guidance and guidelines from the American Association for the Study of Liver Diseases. Hepatology. 2020;72(2):671–722. DOI: 10.1002/hep.31065

22. Zachou K., Muratori P., Koukoulis G.K., Granito A., Gatselis N., Fabbri A., et al. Review article: Autoimmune hepatitis —current management and challenges. Aliment Pharmacol Ther. 2013;38:887–913.

23. European Association for the Study of the Liver. EASL clinical practice guidelines: Autoimmune hepatitis. J Hepatol. 2015;63(4):971–1004. DOI: 10.1016/j.jhep.2015.06.030

24. Czaja A.J. Autoantibody-negative autoimmune hepatitis. Dig Dis Sci. 2012;57(3):610–24. DOI: 10.1007/s10620-011-2017-z

25. Bueverov A.O. Seronegative autoimmune hepatitis. Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2017;27(2):27–33. (In Russ.).

26. Galaski J., Weiler-Normann C., Schakat M., Zachou K., Muratori P., Lampalzer S., et al. Update of the simplified criteria for autoimmune hepatitis: Evaluation of the methodology for immunoserological testing. J Hepatol. 2021;74(2):312–20. DOI: 10.1016/j.jhep.2020.07.032

27. Chan E.K.L., von Mühlen C.A., Fritzler M.J., Damoiseaux J., Infantino M., Klotz W., et al.; ICAP Committee. The International Consensus on ANA Patterns (ICAP) in 2021 — The 6th Workshop and current perspectives. J Appl Lab Med. 2022;7(1):322–30. DOI: 10.1093/jalm/jfab140

28. Muñoz-Sánchez G., Pérez-Isidro A., Ortiz de Landazuri I., López-Gómez A., Bravo-Gallego L.Y., Garcia-Ormaechea M., et al. on behalf of the Geai-Sei Workshop participants. Working algorithms and detection methods of autoantibodies in autoimmune liver disease: A nationwide study. Diagnostics (Basel). 2022;12(3):697. DOI: 10.3390/diagnostics12030697

29. Bogdanos D.P., Invernizzi P., Mackay I.R., Vergani D. Autoimmune liver serology: Current diagnostic and clinical challenges. World J. Gastroenterol. 2008;14(21):3374–87. DOI: 10.3748/wjg.14.3374

30. Aleksandrova E.N., Dorofeev A.S., Novikov A.A., Sandler Yu.G. Autoantibodies in autoimmune liver diseases (literature review). Russian Clinical Laboratory Diagnostics. 2023;68(8):464–74. (In Russ.). DOI: 10.51620/0869-2084-2023-68-8-464-474

31. Laschtowitz A., Zachou K., Lygoura V., Pape S., Derben F., Jaeckel E., et al. Histological activity despite normal ALT and IgG serum levels in patients with autoimmune hepatitis and cirrhosis. JHEP Rep. 2021;3(4):100321. DOI: 10.1016/j.jhepr.2021.100321

32. van Gerven N.M., Verwer B.J., Witte B.I., van Hoek B., Coenraad M.J., van Erpecum K.J., et al.; Dutch Autoimmune Hepatitis Working Group. Relapse is almost universal after withdrawal of immunosuppressive medication in patients with autoimmune hepatitis in remission. J Hepatol. 2013;58(1):141–7. DOI: 10.1016/j.jhep.2012.09.009

33. Lohse A.W., Sebode M., Bhathal P.S., Clouston A.D., Dienes H.P., Jain D., et al. Consensus recommendations for histological criteria of autoimmune hepatitis from the International AIH Pathology Group: Results of a workshop on AIH histology hosted by the European Reference Network on Hepatological Diseases and the European Society of Pathology: Results of a workshop on AIH histology hosted by the European Reference Network on Hepatological Diseases and the European Society of Pathology. Liver Int. 2022;42(5):1058–69. DOI: 10.1111/liv.15217

34. Dhaliwal H.K., Hoeroldt B.S., Dube A.K., McFarlane E., Underwood J.C., Karajeh M.A., et al. Longterm prognostic significance of persisting histological activity despite biochemical remission in autoimmune hepatitis. Am J Gastroenterol. 2015;110(7):993–9. DOI: 10.1038/ajg.2015.139

35. Knodell R.G., Ishak K.G., Black W.C., Chen T.S., Craig R., Kaplowitz N., et al. Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology. 1981;1(5):431–5. DOI: 10.1002/hep.1840010511

36. Hartl J., Denzer U., Ehlken H., Zenouzi R., Peiseler M., Sebode M., et al. Transient elastography in autoimmune hepatitis: Timing determines the impact of inflammation and fibrosis. J Hepatol. 2016;65(4):769–75. DOI: 10.1016/j.jhep.2016.05.023

37. Lai J.C., Liang L.Y., Wong G.L. Noninvasive tests for liver fibrosis in 2024: Are there different scales for different diseases? Gastroenterol Rep (Oxf). 2024;12:goae096. DOI: 10.1093/gastro/goae096

38. Ishak K., Baptista A., Bianchi L., Callea F., De Groote J., Gudat F., et al. Histological grading and staging of chronic hepatitis. J Hepatol. 1995;22(6):696–9. DOI: 10.1016/0168-8278(95)80226-6

39. Ahn S., Jeong S.H., Cho E.J., Lee K., Kim G., Kim H. Comparison of four histological scoring systems for autoimmune hepatitis to improve diagnostic sensitivity. Clin Mol Hepatol. 2024;30(1):37–48. DOI: 10.3350/cmh.2023.0325

40. van Buuren H.R., Lammers W.J., Harms M.H., Hansen B.E. Surrogate endpoints for optimal therapeutic response to UDCA in primary biliary cholangitis. Dig Dis. 2015;33 Suppl 2:118–24. DOI: 10.1159/000440759

41. Ponsioen C.Y., Lindor K.D., Mehta R., Dimick-Santos L. Design and endpoints for clinical trials in primary sclerosing cholangitis. Hepatology. 2018;68(3):1174–88. DOI: 10.1002/hep.29882

42. Cook G.C., Mulligan R., Sherlock S. Controlled prospective trial of corticosteroid therapy in active chronic hepatitis. Q J Med. 1971;40(158):159–85. DOI: 10.1093/oxfordjournals.qjmed.a067264

43. Manns M.P., Woynarowski M., Kreisel W., Lurie Y., Rust C., Zuckerman E., et al. Budesonide induces remission more effectively than prednisone in a controlled trial of patients with autoimmune hepatitis. Gastroenterology. 2010;139(4):1198–206. DOI: 10.1053/j.gastro.2010.06.046

44. Pape S., Snijders R.J.A.L.M., Gevers T.J.G., Chazouilleres O., Dalekos G.N., Hirschfield G.M., et al.; International Autoimmune Hepatitis Group (IAIHG) collaborators. Systematic review of response criteria and endpoints in autoimmune hepatitis by the International Autoimmune Hepatitis Group. J Hepatol. 2022;76(4):841–9. DOI: 10.1016/j.jhep.2021.12.041

45. Czaja A.J. Diagnosis and management of autoimmune hepatitis: Current status and future directions. Gut Liver. 2016;10(2):177–203. DOI: 10.5009/gnl15352

46. Urzúa Á., Pizarro C., Gajardo A., Poniachik R., Pavez C., Cattaneo M., et al. Autoimmune hepatitis with acute presentation: Clinical, biochemical, and histological features of 126 patients. Can J Gastroenterol Hepatol. 2022;2022:6470847. DOI: 10.1155/2022/6470847

47. Yasui S., Fujiwara K., Yonemitsu Y., Oda S., Nakano M., Yokosuka O. Clinicopathological features of severe and fulminant forms of autoimmune hepatitis. J Gastroenterol. 2011;46(3):378–90. DOI: 10.1007/s00535-010-0316-3

48. Biewenga M., Verhelst X., Baven-Pronk M., Putter H., van den Berg A., Colle I., et al.; Dutch Autoimmune Hepatitis Study Group. Aminotransferases during treatment predict long-term survival in patients with autoimmune hepatitis type 1: A landmark analysis. Clin Gastroenterol Hepatol. 2022;20(8):1776–83.e4. DOI: 10.1016/j.cgh.2021.05.024

49. Plagiannakos C.G., Hirschfield G.M., Lytvyak E., Roberts S.B., Ismail M., Gulamhusein A.F., et al.; Canadian Network for Autoimmune Liver Disease (CaNAL). Treatment response and clinical event-free survival in autoimmune hepatitis: A Canadian multicentre cohort study. J Hepatol. 2024;81(2):227–37. DOI: 10.1016/j.jhep.2024.03.021

50. Grossar L., Raevens S., Van Steenkiste C., Colle I., De Vloo C., Orlent H., et al. External validation of the IAIHG autoimmune hepatitis response criteria in a multicentric real-world cohort. JHEP Reports. 2024;6(9):101149. DOI: 10.1016/j.jhepr.2024.101149

51. Czaja A.J. Features and consequences of untreated type 1 autoimmune hepatitis. Liver Int. 2009;29(6):816–23. DOI: 10.1111/j.1478-3231.2008.01904.x

52. Wang G., Tanaka A., Zhao H., Jia J., Ma X., Harada K., et al. The Asian Pacific Association for the Study of the Liver clinical practice guidance: The diagnosis and management of patients with autoimmune hepatitis. Hepatol Int. 2021;15(2):223–57. DOI: 10.1007/s12072-021-10170-1

53. Czaja A.J. Treatment of autoimmune hepatitis. Semin Liver Dis. 2002;22(4):365–78. DOI: 10.1055/s-2002-35706

54. Lamers M.M., van Oijen M.G., Pronk M., Drenth J.P. Treatment options for autoimmune hepatitis: A systematic review of randomized controlled trials. J Hepatol. 2010;53(1):191–8. DOI: 10.1016/j.jhep.2010.01.037

55. Pape S., Gevers T.J.G., Vrolijk J.M., van Hoek B., Bouma G., van Nieuwkerk C.M.J., et al. High discontinuation rate of azathioprine in autoimmune hepatitis, independent of time of treatment initiation. Liver Int. 2020;40(9):2164–71. DOI: 10.1111/liv.14513

56. Zhang C., Wu S.S., Dong X.Q., Wu Z., Zhao H., Wang G.Q. The efficacy and safety of different doses of glucocorticoid for autoimmune hepatitis: A systematic review and meta-analysis. Medicine (Baltimore). 2019;98(52):e18313. DOI: 10.1097/MD.0000000000018313

57. Stellon A.J., Hegarty J.E., Portmann B., Williams R. Randomised controlled trial of azathioprine withdrawal in autoimmune chronic active hepatitis. Lancet. 1985;1(8430):668–70. DOI: 10.1016/s0140-6736(85)91329-7

58. Czaja A.J. Rapidity of treatment response and outcome in type 1 autoimmune hepatitis. J Hepatol. 2009;51(1):161–7. DOI: 10.1016/j.jhep.2009.02.026

59. Santiago P., Schwartz I., Tamariz L., Levy C. Systematic review with meta-analysis: Mycophenolate mofetil as a second-line therapy for autoimmune hepatitis. Aliment Pharmacol Ther. 2019;49(7):830–9. DOI: 10.1111/apt.15157

60. Dalekos G.N., Arvaniti P., Gatselis N.K., Gabeta S., Samakidou A., Giannoulis G., et al. Long-term results of mycophenolate mofetil vs. azathioprine use in individuals with autoimmune hepatitis. JHEP Rep. 2022;4(12):100601. DOI: 10.1016/j.jhepr.2022.100601

61. Dalekos G.N., Arvaniti P., Gatselis N.K., Samakidou A., Gabeta S., Rigopoulou E., et al. First results from a propensity matching trial of mycophenolate mofetil vs. azathioprine in treatment-naive AIH patients. Front Immunol. 2022;12:798602. DOI: 10.3389/fimmu.2021.798602

62. Snijders R.J.A.L.M., Stoelinga A.E.C., Gevers T.J.G., Pape S., Biewenga M., Tushuizen M.E., et al.; Dutch Autoimmune Hepatitis Working Group. An open-label randomised-controlled trial of azathioprine vs. mycophenolate mofetil for the induction of remission in treatment-naive autoimmune hepatitis. J Hepatol. 2024;80(4):576–85. DOI: 10.1016/j.jhep.2023.11.032

63. Terziroli Beretta-Piccoli B., Mieli-Vergani G., Vergani D. Autoimmune hepatitis: Standard treatment and systematic review of alternative treatments. World J Gastroenterol. 2017;23(33):6030–48. DOI: 10.3748/wjg.v23.i33.6030

64. Czaja A.J., Lindor K.D. Failure of budesonide in a pilot study of treatment-dependent autoimmune hepatitis. Gastroenterology. 2000;119(5):1312–6. DOI: 10.1053/gast.2000.0010000001

65. Woynarowski M., Nemeth A., Baruch Y., Koletzko S., Melter M., Rodeck B., et al.; European Autoimmune Hepatitis-Budesonide Study Group. Budesonide versus prednisone with azathioprine for the treatment of autoimmune hepatitis in children and adolescents. J Pediatr. 2013;163(5):1347–53.e1. DOI: 10.1016/j.jpeds.2013.05.042

66. Peiseler M., Liebscher T., Sebode M., Zenouzi R., Hartl J., Ehlken H., et al. Efficacy and limitations of budesonide as a second-line treatment for patients with autoimmune hepatitis. Clin Gastroenterol Hepatol. 2018;16(2):260–7.e1. DOI: 10.1016/j.cgh.2016.12.040

67. Wiegand J., Schüler A., Kanzler S., Lohse A., Beuers U., Kreisel W., et al. Budesonide in previously untreated autoimmune hepatitis. Liver Int. 2005;25(5):927–34. DOI: 10.1111/j.1478-3231.2005.01122.x

68. Lu F.B., Hu E.D., Xu L.M., Hu Y.B., Chen L., Wu J.L., et al. Comparative efficacy and tolerability of treatments for adult autoimmune hepatitis: A systematic review and network meta-analysis. Exp Ther Med. 2018;15(6):4838–50. DOI: 10.3892/etm.2018.6063

69. Hanouneh M., Ritchie M.M., Ascha M., Ascha M.S., Chedid A., Sanguankeo A., et al. A review of the utility of tacrolimus in the management of adults with autoimmune hepatitis. Scand J Gastroenterol. 2019;54(1):76–80. DOI: 10.1080/00365521.2018.1551498

70. Stoelinga A.E.C., Tushuizen M.E., van den Hout W.B., Girondo M.D.M.R., de Vries E.S., Levens A.D., et al.; Dutch Autoimmune Hepatitis Group. Tacrolimus versus mycophenolate for autoimmune hepatitis patients with incomplete response on first-line therapy (TAILOR study): A study protocol for a phase III, open-label, multicentre, randomised controlled trial. Trials. 2024;25(1):61. DOI: 10.1186/s13063-023-07832-w

71. De Lemos-Bonotto M., Valle-Tovo C., Costabeber A.M., Mattos A.A., Azeredo-da-Silva A.L.F. A systematic review and meta-analysis of second-line immunosuppressants for autoimmune hepatitis treatment. Eur J Gastroenterol Hepatol. 2018;30(2):212–6. DOI: 10.1097/MEG.0000000000001019

72. Tannous M.M., Cheng J., Muniyappa K., Farooq I., Bharara A., Kappus M., et al. Use of tacrolimus in the treatment of autoimmune hepatitis: A single centre experience. Aliment Pharmacol Ther. 2011;34(3):405–7. DOI: 10.1111/j.1365-2036.2011.04749.x

73. Baven-Pronk M.A., Hew J.M. Jr., Biewenga M., Tushuizen M.E., van den Berg A.P., Bouma G., et al.; Dutch Autoimmune Hepatitis Study Group. Calcineurin inhibitors in the treatment of adult autoimmune hepatitis: A systematic review. J Clin Transl Hepatol. 2022;10(6):1155–66. DOI: 10.14218/JCTH.2021.00535

74. Еfe C., Taii H.A., Ytting H., Aehling N., Bhanji R.A., Hagstrom H., et al. Tacrolimus and mycophenolate mofetil as second-line therapies for pediatric patients with autoimmune hepatitis. Dig Dis Sci. 2018;63(5):1348–54. DOI: 10.1007/s10620-018-5011-x

75. Ytting H., Larsen F.S. Everolimus treatment for patients with autoimmune hepatitis and poor response to standard therapy and drug alternatives in use. Scand J Gastroenterol. 2015;50(8):1025–31. DOI: 10.3109/00365521.2014.998271

76. Porcelli L., Quatrale A.E., Mantuano P., Silvestris N., Rolland J.F., Biancolillo L., et al. Synergistic antiproliferative and antiangiogenic effects of EGFR and mTOR inhibitors. Curr Pharm Des. 2013;19(5):918–26.

77. Weinberg E.M. Current and emerging treatments for autoimmune hepatitis. Gastroenterol Hepatol (N Y). 2024;20(3):176–8.

78. Adao I., Klepper A., Tana M. AIH therapy: Beyond first-line. Curr Hepatology Rep. 2024;23:341–8. DOI: 10.1007/s11901-024-00657-4

79. Weiler-Normann C., Schramm C., Quaas A., Wiegard C., Glaubke C., Pannicke N., et al. Infliximab as a rescue treatment in difficult-to-treat autoimmune hepatitis. J Hepatol. 2013;58(3):529–34. DOI: 10.1016/j.jhep.2012.11.010

80. Than N.N., Hodson J., Schmidt-Martin D., Taubert R., Wawman R.E., Botter M., et al. Efficacy of rituximab in difficult-to-manage autoimmune hepatitis: Results from the International Autoimmune Hepatitis Group. JHEP Rep. 2019;1(6):437–45. DOI: 10.1016/j.jhepr.2019.10.005

81. Riveiro-Barciela M., Barreira-Díaz A., Esteban P., Rota R., Álvarez-Navascúes C., Pérez-Medrano I., et al. Rituximab is a safe and effective alternative treatment for patients with autoimmune hepatitis: Results from the ColHai registry. Liver Int. 2024;44(9):2303–14. DOI: 10.1111/liv.15970

82. Kolev M., Sarbu A.C., Möller B., Maurer B., Kollert F., Semmo N. Belimumab treatment in autoimmune hepatitis and primary biliary cholangitis — a case series. J Transl Autoimmun. 2023;6:100189. DOI: 10.1016/j.jtauto.2023.100189

83. Arvaniti P., Giannoulis G., Gabeta S., Zachou K., Koukoulis G.K., Dalekos G.N. Belimumab is a promising third-line treatment option for refractory autoimmune hepatitis. JHEP Rep. 2020;2(4):100123. DOI: 10.1016/j.jhepr.2020.100123

84. Czaja A.J., Carpenter H.A. Histological features associated with relapse after corticosteroid withdrawal in type 1 autoimmune hepatitis. Liver Int. 2003;23(2):116–23. DOI: 10.1034/j.1600-0676.2003.00810.x

85. ÇavuşB., Akyuz F.,İliaz R., Atasoy A., Akyuz U., Demir K., et al. Is there any predictor for relapse after treatment withdrawal in autoimmune hepatitis patients in the real life? Int J Immunopathol Pharmacol. 2022;36:3946320221077860. DOI: 10.1177/03946320221077860

86. Hatoum S., Rockey D.C. Long-term outcomes of patients with autoimmune hepatitis induced cirrhosis after immunosuppressive treatment. Eur J Gastroenterol Hepatol. 2024;36(6):742–9. DOI: 10.1097/MEG.0000000000002714.


Review

For citations:

Sandler Yu.G., Vinnitskaya E.V., Raikhelson K.L., Ivashkin K.V., Batskikh S.N., Aleksandrova E.N., Abdurakhmanov D.T., Abdulganieva D.I., Bakulin I.G., Bueverov A.O., Vorobyev S.L., Gerasimova O.A., Dolgushina A.I., Zhuravleva M.S., Ilchenko L.Yu., Karev V.E., Korochanskaya N.V., Kliaritskaia I.L., Karnaukhov N.S., Lapin S.V., Livzan M.A., Maevskaya M.V., Marchenko N.V., Nekrasova T.P., Nikitin I.G., Novikov A.A., Saifutdinov R.G., Skazyvaeva E.V., Syutkin V.E., Prashnova M.K., Khaymenova T.Yu., Khomerik S.G. Diagnosis and Treatment of Patients with Autoimmune Hepatitis (Experts’ Agreement). Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2024;34(6):100-119. https://doi.org/10.22416/1382-4376-2024-34-6-100-119

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Tatiana L. Lapina - MD, PhD, associate professor, Department of Internal Diseases Propedeutics,
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