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Volynets G.V.

Pirogov Russian National Research Medical University

Nikitin A.V.

Pirogov Russian National Research Medical University;
Morozov Children’s City Clinical Hospital

Skvortsova T.A.

Pirogov Russian National Research Medical University;
Morozov Children’s City Clinical Hospital

Kokiashvili V.S.

Pirogov Russian National Research Medical University

Drug-induced autoimmune-like hepatitis

Authors:

Volynets G.V., Nikitin A.V., Skvortsova T.A., Kokiashvili V.S.

More about the authors

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To cite this article:

Volynets GV, Nikitin AV, Skvortsova TA, Kokiashvili VS. Drug-induced autoimmune-like hepatitis. Russian Journal of Evidence-Based Gastroenterology. 2024;13(1):58‑65. (In Russ.)
https://doi.org/10.17116/dokgastro20241301158

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References:

  1. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Autoimmune hepatitis. Journal of Hepatology. 2015;63(4):971-1004. https://doi.org/10.1016/j.jhep.2015.06.030
  2. Lammert C, Chalasani SN, Atkinson EJ, McCauley BM, Lazaridis KN. Environmental risk factors are associated with autoimmune hepatitis. Liver International. 2021;41(10):2396-2403. https://doi.org/10.1111/liv.14944
  3. Mack CL, Adams D, Assis DN, Kerkar N, Manns MP, Mayo MJ, Vierling JM, Alsawas M, Murad MH, Czaja AJ. 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.  https://doi.org/10.1002/hep.31065
  4. Andrade RJ, Chalasani N, Björnsson ES, Suzuki A, Kullak-Ublick GA, Watkins PB, Devarbhavi H, Merz M, Lucena MI, Kaplowitz N, Aithal GP. Drug-induced liver injury. Nature Reviews. Disease Primers. 2019;5(1):58.  https://doi.org/10.1038/s41572-019-0105-0
  5. Pinazo-Bandera JM, García-Cortés M, Andrade RJ. AASLD practice guidance on drug, herbal, and dietary supplement-induced liver injury: also useful for hepatobiliary surgeons. Hepatobiliary Surgery and Nutrition. 2023;12(5):746-751.  https://doi.org/10.21037/hbsn-23-319
  6. Hoofnagle JH, Björnsson ES. Drug-induced liver injury — types and phenotypes. New England Journal of Medicine. 2019;381(3): 264-273.  https://doi.org/10.1056/NEJMra1816149
  7. European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Drug-induced liver injury. Journal of Hepatology. 2019;70(6):1222-1261. https://doi.org/10.1016/j.jhep.2019.02.014
  8. Stephens C, Robles-Diaz M, Medina-Caliz I, Garcia-Cortes M, Ortega-Alonso A, Sanabria-Cabrera J, Gonzalez-Jimenez A, Alvarez-Alvarez I, Slim M, Jimenez-Perez M, Gonzalez-Grande R, Fernández MC, Casado M, Soriano G, Román E, Hallal H, Romero-Gomez M, Castiella A, Conde I, Prieto M, Moreno-Planas JM, Giraldez A, Moreno-Sanfiel JM, Kaplowitz N, Lucena MI, Andrade RJ; Participating clinical centres. Participating clinical centres. Comprehensive analysis and insights gained from long-term experience of the Spanish DILI Registry. Journal of Hepatology. 2021;75(1):86-97.  https://doi.org/10.1016/j.jhep.2021.01.029
  9. Björnsson E, Talwalkar J, Treeprasertsuk S, Kamath PS, Takahashi N, Sanderson S, Neuhauser M, Lindor K. Drug-induced autoimmune hepatitis: clinical characteristics and prognosis. Hepatology. 2010;51(6):2040-2048. https://doi.org/10.1002/hep.23588
  10. Björnsson ES, Bergmann O, Jonasson JG, Grondal G, Gudbjornsson B, Olafsson S. Drug-induced autoimmune hepatitis: response to corticosteroids and lack of relapse after cessation of steroids. Clinical Gastroenterology and Hepatology. 2017;15(10):1635-1636. https://doi.org/10.1016/j.cgh.2017.05.027
  11. Suzuki A, Brunt EM, Kleiner DE, Miquel R, Smyrk TC, Andrade RJ, Lucena MI, Castiella A, Lindor K, Björnsson E. The use of liver biopsy evaluation in discrimination of idiopathic autoimmune hepatitis versus drug-induced liver injury. Hepatology. 2011;54(3):931-939.  https://doi.org/10.1002/hep.24481
  12. Andrade RJ, Robles-Diaz M, Castiella A. Characterizing Drug-Induced Liver Injury With Autoimmune Features. Clinical Gastroenterology and Hepatology. 2016;14(12):1844-1845. https://doi.org/10.1016/j.cgh.2016.07.022
  13. Weiler-Normann C, Schramm C. Drug induced liver injury and its relationship to autoimmune hepatitis. Journal of Hepatology. 2011;55(4):747-749.  https://doi.org/10.1016/j.jhep.2011.02.024
  14. deLemos AS, Foureau DM, Jacobs C, Ahrens W, Russo MW, Bonkovsky HL. Drug-induced liver injury with autoimmune features. Seminars in Liver Disease. 2014;34(2):194-204.  https://doi.org/10.1055/s-0034-1375959
  15. Björnsson ES, Medina-Caliz I, Andrade RJ, Lucena MI. Setting up criteria for drug-induced autoimmune-like hepatitis through a systematic analysis of published report. Hepatology Communications. 2022;6(8):1895-1909. https://doi.org/10.1002/hep4.1959
  16. Czaja AJ. Drug-induced autoimmune-like hepatitis. Digestive Diseases and Sciences. 2011;56(4):958-976.  https://doi.org/10.1007/s10620-011-1611-4
  17. Andrade RJ, Aithal GP, de Boer YS, Liberal R, Gerbes A, Regev A, Terziroli Beretta-Piccoli B, Schramm C, Kleiner DE, De Martin E, Kullak-Ublick GA, Stirnimann G, Devarbhavi H, Vierling JM, Manns MP, Sebode M, Londoño MC, Avigan M, Robles-Diaz M, García-Cortes M, Atallah E, Heneghan M, Chalasani N, Trivedi PJ, Hayashi PH, Taubert R, Fontana RJ, Weber S, Oo YH, Zen Y, Licata A, Lucena MI, Mieli-Vergani G, Vergani D, Björnsson ES; IAIHG and EASL DHILI Consortium. Nomenclature, diagnosis and management of drug-induced autoimmune-like hepatitis (DI-ALH): An expert opinion meeting report. Journal of Hepatology. 2023;79(3):853-866.  https://doi.org/10.1016/j.jhep.2023.04.033
  18. Lohse AW, Sebode M, Bhathal PS, Clouston AD, Dienes HP, Jain D, Gouw ASH, Guindi M, Kakar S, Kleiner DE, Krech T, Lackner C, Longerich T, Saxena R, Terracciano L, Washington K, Weidemann S, Hübscher SG, Tiniakos D. 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 International. 2022;42(5):1058-1069. https://doi.org/10.1111/liv.15217
  19. de Boer YS, Kosinski AS, Urban TJ, Zhao Z, Long N, Chalasani N, Kleiner DE, Hoofnagle JH; Drug-Induced Liver Injury Network. Drug-Induced Liver Injury Network. Features of Autoimmune Hepatitis in Patients With Drug-induced Liver Injury. Clinical Gastroenterology and Hepatology. 2017;15(1):103-112.e2.  https://doi.org/10.1016/j.cgh.2016.05.043
  20. Licata A, Maida M, Cabibi D, Butera G, Macaluso FS, Alessi N, Caruso C, Craxì A, Almasio PL. Clinical features and outcomes of patients with drug-induced autoimmune hepatitis: a retrospective cohort study. Digestive and Liver Disease. 2014;46(12):1116-1120. https://doi.org/10.1016/j.dld.2014.08.040
  21. Codoni G, Kirchner T, Engel B, Villamil AM, Efe C, Stättermayer AF, Weltzsch JP, Sebode M, Bernsmeier C, Lleo A, Gevers TJ, Kupčinskas L, Castiella A, Pinazo J, De Martin E, Bobis I, Sandahl TD, Pedica F, Invernizzi F, Del Poggio P, Bruns T, Kolev M, Semmo N, Bessone F, Giguet B, Poggi G, Ueno M, Jang H, Elpek GÖ, Soylu NK, Cerny A, Wedemeyer H, Vergani D, Mieli-Vergani G, Lucena MI, Andrade RJ, Zen Y, Taubert R, Terziroli Beretta-Piccoli B. Histological and serological features of acute liver injury after SARS-CoV-2 vaccination. JHEP Reports. 2022;5(1):100605. https://doi.org/10.1016/j.jhepr.2022.100605
  22. Björnsson ES, Stephens C, Atallah E, Robles-Diaz M, Alvarez-Alvarez I, Gerbes A, Weber S, Stirnimann G, Kullak-Ublick G, Cortez-Pinto H, Grove JI, Lucena MI, Andrade RJ, Aithal GP. A new framework for advancing in drug-induced liver injury research. The Prospective European DILI Registry. Liver International. 2023;43(1):115-126.  https://doi.org/10.1111/liv.15378
  23. Castiella A, Zapata E, Lucena MI, Andrade RJ. Drug-induced autoimmune liver disease: a diagnostic dilemma of an increasingly reported disease. World Journal of Hepatology. 2014;6(4):160-168.  https://doi.org/10.4254/wjh.v6.i4.160
  24. Febres-Aldana CA, Alghamdi S, Krishnamurthy K, Poppiti RJ. Liver fibrosis helps to distinguish autoimmune hepatitis from DILI with autoimmune features: a review of twenty cases. Journal of Clinical and Translational Hepatology. 2019;7(1):21-26.  https://doi.org/10.14218/JCTH.2018.00053
  25. Ghabril M, Bonkovsky HL, Kum C, Davern T, Hayashi PH, Kleiner DE, Serrano J, Rochon J, Fontana RJ, Bonacini M; US Drug-Induced Liver Injury Network. US Drug-Induced Liver Injury Network. Liver injury from tumor necrosis factor-alpha antagonists: analysis of thirty-four cases. Clinical Gastroenterology and Hepatology. 2013;11(5):558-564.e3.  https://doi.org/10.1016/j.cgh.2012.12.025
  26. Rodrigues S, Lopes S, Magro F, Cardoso H, Horta e Vale AM, Marques M, Mariz E, Bernardes M, Lopes J, Carneiro F, Macedo G. Autoimmune hepatitis and anti-tumor necrosis factor alpha therapy: a single center report of 8 cases. World Journal of Gastroenterology. 2015;21(24):7584-7588. https://doi.org/10.3748/wjg.v21.i24.7584
  27. Björnsson ES, Gunnarsson BI, Gröndal G, Jonasson JG, Einarsdottir R, Ludviksson BR, Gudbjörnsson B, Olafsson S. Risk of drug-induced liver injury from tumor necrosis factor antagonists. Clinical Gastroenterology and Hepatology. 2015;13(3):602-608.  https://doi.org/10.1016/j.cgh.2014.07.062
  28. Björnsson HK, Gudbjornsson B, Björnsson ES. Infliximab-induced liver injury: clinical phenotypes, autoimmunity and the role of corticosteroid treatment. Journal of Hepatology. 2022;76(1):86-92.  https://doi.org/10.1016/j.jhep.2021.08.024
  29. García-Cortés M, Ortega-Alonso A, Matilla-Cabello G, Medina-Cáliz I, Castiella A, Conde I, Bonilla-Toyos E, Pinazo-Bandera J, Hernández N, Tagle M, Nunes V, Parana R, Bessone F, Kaplowitz N, Lucena MI, Alvarez-Alvarez I, Robles-Díaz M, Andrade RJ. Clinical presentation, causative drugs, and outcome of patients with autoimmune features in the Spanish DILI Regsitry and the Latin American DILI Network. Liver International. 2023;43(8):1749-1760. https://doi.org/10.1111/liv.15623
  30. Björnsson E, Davidsdottir L. The long-term follow-up after idiosyncratic drug-induced liver injury with jaundice. Journal of Hepatology. 2009;50(3):511-517.  https://doi.org/10.1016/j.jhep.2008.10.021
  31. Terziroli Beretta-Piccoli B, Mieli-Vergani G, Vergani D. The clinical usage and definition of autoantibodies in immune-mediated liver disease: a comprehensive overview. Journal of Autoimmunity. 2018;95:144-158.  https://doi.org/10.1016/j.jaut.2018.10.004
  32. Zeman MV, Hirschfield GM. Autoantibodies and liver disease: uses and abuses. Canadian Journal of Gastroenterology. 2010;24(4): 225-231.  https://doi.org/10.1155/2010/431913
  33. Stephens C, Castiella A, Gomez-Moreno EM, Otazua P, López-Nevot MÁ, Zapata E, Ortega-Alonso A, Ruiz-Cabello F, Medina-Cáliz I, Robles-Díaz M, Soriano G, Roman E, Hallal H, Moreno-Planas JM, Prieto M, Andrade RJ, Lucena MI. Autoantibody presentation in drug-induced liver injury and idiopathic autoimmune hepatitis: the influence of human leucocyte antigen alleles. Pharmacogenetics and Genomics. 2016;26(9):414-422.  https://doi.org/10.1097/FPC.0000000000000230
  34. Weber S, Benesic A, Buchholtz ML, Rotter I, Gerbes AL. Antimitochondrial rather than antinuclear antibodies correlate with severe drug-induced liver injury. Digestive Diseases. 2021;39(3):275-282.  https://doi.org/10.1159/000511635
  35. van Gerven NM, Verwer BJ, Witte BI, van Erpecum KJ, van Buuren HR, Maijers I, Visscher AP, Verschuren EC, van Hoek B, Coenraad MJ, Beuers UH, de Man RA, Drenth JP, den Ouden JW, Verdonk RC, Koek GH, Brouwer JT, Guichelaar MM, Vrolijk JM, Mulder CJ, van Nieuwkerk CM, Bouma G; Dutch Autoimmune hepatitis STUDY group. Dutch Autoimmune hepatitis STUDY group. Epidemiology and clinical characteristics of autoimmune hepatitis in The Netherlands. Scandinavian Journal of Gastroenterology. 2014;49(10):1245-1254. https://doi.org/10.3109/00365521.2014.946083
  36. Lucena MI, Kaplowitz N, Hallal H, Castiella A, García-Bengoechea M, Otazua P, Berenguer M, Fernandez MC, Planas R, Andrade RJ. Recurrent drug-induced liver injury (DILI) with different drugs in the Spanish Registry: the dilemma of the relationship to autoimmune hepatitis. Journal of Hepatology. 2011;55(4):820-827.  https://doi.org/10.1016/j.jhep.2010.12.041
  37. Sharma R, Verna EC, Simon TG, Söderling J, Hagström H, Green PHR, Ludvigsson JF. Cancer Risk in Patients With Autoimmune Hepatitis: A Nationwide Population-Based Cohort Study With Histopathology. American Journal of Epidemiology. 2022;191(2):298-319.  https://doi.org/10.1093/aje/kwab119
  38. Chalasani NP, Maddur H, Russo MW, Wong RJ, Reddy KR; Practice Parameters Committee of the American College of Gastroenterology. ACG Clinical Guideline: Diagnosis and Management of Idiosyncratic Drug-Induced Liver Injury. American Journal of Gastroenterology. 2021;116(5):878-898.  https://doi.org/10.14309/ajg.0000000000001259
  39. Devarbhavi H, Aithal G, Treeprasertsuk S, Takikawa H, Mao Y, Shasthry SM, Hamid S, Tan SS, Philips CA, George J, Jafri W, Sarin SK; Asia Pacific Association of Study of Liver. Drug-induced liver injury: Asia Pacific Association of Study of Liver consensus guidelines. Hepatology International. 2021;15(2):258-282.  https://doi.org/10.1007/s12072-021-10144-3
  40. Fontana RJ, Liou I, Reuben A, Suzuki A, Fiel MI, Lee W, Navarro V. AASLD practice guidance on drug, herbal, and dietary supplement-induced liver injury. Hepatology. 2023;77(3):1036-1065. https://doi.org/10.1002/hep.32689
  41. de Boer YS, van Nieuwkerk CM, Witte BI, Mulder CJ, Bouma G, Bloemena E. Assessment of the histopathological key features in autoimmune hepatitis. Histopathology. 2015;66(3):351-362.  https://doi.org/10.1111/his.12558
  42. Kleiner DE, Chalasani NP, Lee WM, Fontana RJ, Bonkovsky HL, Watkins PB, Hayashi PH, Davern TJ, Navarro V, Reddy R, Talwalkar JA, Stolz A, Gu J, Barnhart H, Hoofnagle JH; Drug-Induced Liver Injury Network (DILIN). Hepatic histological findings in suspected drug-induced liver injury: systematic evaluation and clinical associations. Hepatology. 2014;59(2):661-670.  https://doi.org/10.1002/hep.26709
  43. Danan G, Benichou C. Causality assessment of adverse reactions to drugs — I. A novel method based on the conclusions of international consensus meetings: application to drug-induced liver injuries. Journal of Clinical Epidemiology. 1993;46(11):1323-1330. https://doi.org/10.1016/0895-4356(93)90101-6
  44. García-Cortés M, Stephens C, Lucena MI, Fernández-Castañer A, Andrade RJ. Causality assessment methods in drug induced liver injury: strengths and weaknesses. Journal of Hepatology. 2011; 55(3):683-691.  https://doi.org/10.1016/j.jhep.2011.02.007
  45. Hayashi PH, Lucena MI, Fontana RJ, Bjornsson ES, Aithal GP, Barnhart H, Gonzalez-Jimenez A, Yang Q, Gu J, Andrade RJ, Hoofnagle JH. A revised electronic version of RUCAM for the diagnosis of DILI. Hepatology. 2022;76(1):18-31.  https://doi.org/10.1002/hep.32327
  46. Alvarez F, Berg PA, Bianchi FB, Bianchi L, Burroughs AK, Cancado EL, Chapman RW, Cooksley WG, Czaja AJ, Desmet VJ, Donaldson PT, Eddleston AL, Fainboim L, Heathcote J, Homberg JC, Hoofnagle JH, Kakumu S, Krawitt EL, Mackay IR, MacSween RN, Maddrey WC, Manns MP, McFarlane IG, Meyer zum Büschenfelde KH, Zeniya M. International Autoimmune Hepatitis Group Report: review of criteria for diagnosis of autoimmune hepatitis. Journal of Hepatology. 1999;31(5):929-938.  https://doi.org/10.1016/s0168-8278(99)80297-9
  47. Lammert C, Zhu C, Lian Y, Raman I, Eckert G, Li QZ, Chalasani N. Exploratory study of autoantibody profiling in drug-induced liver injury with an autoimmune phenotype. Hepatology Communications. 2020;4(11):1651-1663. https://doi.org/10.1002/hep4.1582
  48. Taubert R, Engel B, Diestelhorst J, Hupa-Breier KL, Behrendt P, Baerlecken NT, Sühs KW, Janik MK, Zachou K, Sebode M, Schramm C, Londoño MC, Habes S; UK-AIH Consortium; Oo YH, Lalanne C, Pape S, Schubert M, Hust M, Dübel S, Thevis M, Jonigk D, Beimdiek J, Buettner FFR, Drenth JPH, Muratori L, Adams DH, Dyson JK, Renand A, Graupera I, Lohse AW, Dalekos GN, Milkiewicz P, Stangel M, Maasoumy B, Witte T, Wedemeyer H, Manns MP, Jaeckel E. Quantification of polyreactive immunoglobulin G facilitates the diagnosis of autoimmune hepatitis. Hepatology. 2022;75(1):13-27.  https://doi.org/10.1002/hep.32134
  49. Sugimoto K, Ito T, Yamamoto N, Shiraki K. Seven cases of autoimmune hepatitis that developed after drug-induced liver injury. Hepatology. 2011;54(5):1892-1893. https://doi.org/10.1002/hep.24513
  50. Robles-Diaz M, Lucena MI, Kaplowitz N, Stephens C, Medina-Cáliz I, González-Jimenez A, Ulzurrun E, Gonzalez AF, Fernandez MC, Romero-Gómez M, Jimenez-Perez M, Bruguera M, Prieto M, Bessone F, Hernandez N, Arrese M, Andrade RJ; Spanish DILI Registry; SLatinDILI Network; Safer and Faster Evidence-based Translation Consortium. Use of Hy’s law and a new composite algorithm to predict acute liver failure in patients with drug-induced liver injury. Gastroenterology. 2014;147(1):109-118.e5.  https://doi.org/10.1053/j.gastro.2014.03.050
  51. Niu H, Ma J, Medina-Caliz I, Robles-Diaz M, Bonilla-Toyos E, Ghabril M, Lucena MI, Alvarez-Alvarez I, Andrade RJ. Potential benefit and lack of serious risk from corticosteroids in drug-induced liver injury: an international, multicentre, propensity score-matched analysis. Alimentary Pharmacology and Therapeutics. 2023; 57(8):886-896.  https://doi.org/10.1111/apt.17373

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