Advertisement

Rheumatology International

, Volume 38, Issue 5, pp 715–724 | Cite as

Clinical connection between rheumatoid arthritis and liver damage

  • Biljana Radovanović-Dinić
  • Snežana Tešić-Rajković
  • Valentina Zivkovic
  • Saša Grgov
Review
  • 213 Downloads

Abstract

When liver damage is present in rheumatoid arthritis (RA) patients, it is sometimes difficult to determine whether it is a hepatic manifestation of RA, associated primary liver disease or hepatotoxic liver disease which developed during the treatment of RA. Liver damage during RA is most common in the form of asymptomatic abnormal liver tests. Occasionally, liver damage may progress to cirrhosis. Patients with RA are more susceptible to an associated autoimmune liver disease. Medications used in rheumatology are often hepatotoxic and it is difficult to differentiate between hepatic manifestations of the primary disease and potential hepatotoxicity of the administered medications. The significance of the paper is in the fact that it includes the most relevant and the latest information on this commonly present problem in clinical practice. The aim of the author is to provide comprehensive but at the same time concise data which will be useful to the doctors who come into contact with RA patients with symptomatic or asymptomatic liver disease. Timely diagnosis and treatment of liver disease in RA patients can significantly influence the course and outcome of rheumatoid arthritis.

Keywords

Rheumatoid Arthritis Liver Hepatitis Biological therapy 

Notes

Acknowledgements

The authors would like to thank dr Lara Zebic BDS from Birmingham in England, for her helpful advice.

Author contributions

BRD prepared the first draft of the manuscript and contributed to the final version of the paper. STR, VZ and SG read, corrected and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflict of interest.

References

  1. 1.
    Smolen JS, Aletaha D, McInnes IB (2016) Rheumatoid arthritis. Lancet 388(10055):2023–2038CrossRefPubMedGoogle Scholar
  2. 2.
    Shimoda S, Chong Y, Akahoshi M, Niiro H, Tsukamoto H (2016) Hepatic and gastrointestinal manifestations in rheumatic and connective tissue diseases. J Gen Fam Med 17(2):132–137CrossRefGoogle Scholar
  3. 3.
    Hocking WG, Lasser K, Ungerer R, Bersohn M, Palos M, Spiegel T (1981) Spontaneous hepatic rupture in rheumatoid arthritis. Arch Intern Med 141:792–794CrossRefPubMedGoogle Scholar
  4. 4.
    Chentoufi AA, Serov YA, Alazmi M, Baba K (2014) Immune components of liver damage associated with connective tissue diseases. J Clin Transl Hepatol 2(1):37–44PubMedPubMedCentralGoogle Scholar
  5. 5.
    Soultati A, Dourakis S (2005) Hepatic manifestations of autoimmune rheumatic diseases. Ann Gastroenterol 18(3):309–324Google Scholar
  6. 6.
    Selmi C, De Santis M, Gershwin ME (2011) Liver involvement in subjects with rheumatic disease. Arthritis Res Ther 13:226CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Kojima H, Uemura M, Sakurai S, Ann T, Ishii Y, Imazu H, Yoshikawa M, Ichijima K, Fukui H (2002) Clinical features of liver disturbance in rheumatoid diseases: clinicopathological study with special reference to the cause of liver disturbance. J Gastroenterol 37:617–625CrossRefPubMedGoogle Scholar
  8. 8.
    Gasparyan AY, Ayvazyan L, Blackmore H, Kitas GD (2011) Writing a narrative biomedical review: considerations for authors, peer reviewers, and editors. Rheumatol Int 31(11):1409–1417.  https://doi.org/10.1007/s00296-011-1999-3 CrossRefPubMedGoogle Scholar
  9. 9.
    Still GF (1897) On a form of chronic joint disease in children. Med Chir Trans 80:47–60CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Ebert EC, Hagspiel KD (2011) Gastrointestinal and hepatic manifestations of rheumatoid arthritis. Dig Dis Sci 56(2):295–302CrossRefPubMedGoogle Scholar
  11. 11.
    Lee JE, Kim IJ, Cho MS, Lee J (2017) A case of rheumatoid vasculitis involving hepatic artery in early rheumatoid arthritis. J Korean Med Sci 32(7):1207–1210CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Das S, Padhan P (2017) An overview of the extraarticular involvement in rheumatoid arthritis and its management. J Pharmacol Pharmacother 8(3):81–86PubMedPubMedCentralGoogle Scholar
  13. 13.
    Rigby WFC, Lampl K, Low JM, Furst DE (2017) Review of routine laboratory monitoring for patients with rheumatoid arthritis receiving biologic or nonbiologic DMARDs. Int J Rheumatol 2017:9614241CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Cojocaru M, Cojocaru IM, Silosi I, Vrabie CD (2013) Liver involvement in patients with systemic autoimmune diseases. Medica 8(4):394–397Google Scholar
  15. 15.
    Ruderiman EM, Crawford JM, Maier A, Liu JJ, Gravallese EM, Weinblatt ME (1997) Histologic liver abnormalities in an autopsy series of patients with rheumatoid arthritis. Br J Rheumatol 36(2):210–213CrossRefGoogle Scholar
  16. 16.
    Mills PR, MacSween RN, Dick WC, More IA, Watkinson G (1980) Liver disease in rheumatoid arthritis. Scott Med J 25(1):18–22CrossRefPubMedGoogle Scholar
  17. 17.
    Selmi C, Mackay IR, Gershwin ME (2007) The immunological milieu of the liver. Semin Liver Dis 27:129–139CrossRefPubMedGoogle Scholar
  18. 18.
    Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD (2009) Liver biopsy. Hepatology 49:1017–1044CrossRefPubMedGoogle Scholar
  19. 19.
    Mizuno K, Ikeda K, Saida Y, Takenaka R, Shibata M, Takeuchi T (1996) Hepatic hemorrhage in malignant rheumatoid arthritis. Am J Gastroenterol 91:2624–2625PubMedGoogle Scholar
  20. 20.
    Matsumoto T, Kobayashi S, Shimizu H, Nakajima M, Watanabe S, Kitami N, Sato N, Abe H, Aoki Y, Hoshi T, Hashimoto H (2000) The liver in collagen diseases: pathologic study of 160 cases with particular reference to hepatic arteritis, primary biliary cirrhosis, autoimmune hepatitis and nodular regenerative hyperplasia of the liver. Liver 20:366–373CrossRefPubMedGoogle Scholar
  21. 21.
    Blank M, Gershwin ME (2008) Autoimmunity: from the mosaic to the kaleidoscope. J Autoimmun 30:1–4CrossRefPubMedGoogle Scholar
  22. 22.
    Poupon R (2010) Primary biliary cirrhosis: a 2010 update. J Hepatol 52:745–758CrossRefPubMedGoogle Scholar
  23. 23.
    Lindor KD, Gershwin ME, Poupon R, Kaplan M, Bergasa NV, Heathcote EJ (2009) Primary biliary cirrhosis. Hepatology 50:291–308CrossRefPubMedGoogle Scholar
  24. 24.
    Karlsen TH, Vesterhus M, Boberg KM (2014) Controversies in the management of primary biliary cirrhosis and primary sclerosing cholangitis. Aliment Pharmacol Ther 39(3):282–230CrossRefPubMedGoogle Scholar
  25. 25.
    Reshetnyak (2014) Primary biliary cirrhosis: clinical and laboratory criteria for its diagnosis. World J Gastroenterol 21(25):7683–7708CrossRefGoogle Scholar
  26. 26.
    Liaskos C, Bogdanos DP, Rigopoulou EI, Dalekos GN (2007) Development of antimitochondrial antibodies in patients with autoimmune hepatitis: art of facts or an artifact? J Gastroenterol Hepatol 22(3):454–455CrossRefPubMedGoogle Scholar
  27. 27.
    Bogdanos DP, Komorowski L (2011) Disease-specific autoantibodies in primary biliary cirrhosis. Clin Chim Acta 412(7–8):502–512CrossRefPubMedGoogle Scholar
  28. 28.
    Siegel JL, Luthra H, Donlinger J, Angulo P, Lindor K (2003) Association of primary biliary cirrhosis and rheumatoid arthritis. J Clin Rheumatol 9(6):340–343CrossRefPubMedGoogle Scholar
  29. 29.
    Whaley K, Goudie RB, Williamson J, Nuki G, Dick WC, Buchanan WW (1970) Liver disease in Sjogren’s syndrome and rheumatoid arthritis. Lancet i:861–863CrossRefGoogle Scholar
  30. 30.
    Smyk DS, Bogdanos DP, Mytilinaiou MG, Burroughs AK, Rigopoulou EI (2012) Rheumatoid arthritis and primary biliary cirrhosis: cause, consequence, or coincidence? Hindawi Publ Corp Arthritis.  https://doi.org/10.1155/2012/391567 (article ID 391567, 7 pages) Google Scholar
  31. 31.
    Mitchell MM, Lleo A, Zammataro L et al (2011) Epigenetic investigation of variably X chromosome inactivated genes in monozygotic female twins discordant for primary biliary cirrhosis. Epigenetics 6(1):95–102.  https://doi.org/10.4161/epi.6.1.13405 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Ospelt C, Reedquist KA, Gay S, Tak PP (2011) Inflammatory memories: Is epigenetics the missing link to persistent stromal cell activation in rheumatoid arthritis? Autoimmun Rev 10(9):519–524CrossRefPubMedGoogle Scholar
  33. 33.
    Bogdanos DP, Baum H, Vergani D, Burroughs AK (2010) The role of E. coli infection in the pathogenesis of primary biliary cirrhosis. Dis Mark 29:301–311CrossRefGoogle Scholar
  34. 34.
    Varyani FK, West J, Card TR (2011) An increased risk of urinary tract infection precedes development of primary biliary cirrhosis. BMC Gastroenterol 11:95CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Wilson C, Thakore D, Isenberg D, Ebringer A (1997) Correlation between anti Proteus antibodies and isolation rates of P. mirabilis in rheumatoidarthritis. Rheumatol Int 16:187–189CrossRefPubMedGoogle Scholar
  36. 36.
    Tiwana H, Wilson C, Walmsley RS, Wakefield AJ, Smith MS, Cox NL, Hudson MJ, Ebringer A (1997) Antibody responses to gut bacteria in ankylosing spondylitis, rheumatoid arthritis, Crohn’s disease and ulcerative colitis. Rheumatol Int 17(1):11–16CrossRefPubMedGoogle Scholar
  37. 37.
    Marasini B, Gagetta M, Rossi V, Ferrari P (2001) Rheumatic disorders and primary biliary cirrhosis: an appraisal of 170 Italian patients. Ann Rheum Dis 60(11):1046–1049CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Wolf DC (2017) Autoimmune hepatitis clinical presentation. IOP Publishing PhysicsWeb. https://emedicine.medscape.com/article/172356-clinical#b3. Accessed 25 Sept 2017
  39. 39.
    Toulemonde G, Scoazec JY, Miossec P (2012) Treatment with etanercept of autoimmune hepatitis associated with rheumatoid arthritis: an open label proof of concept study. Ann Rheum Dis 71:1423–1424CrossRefPubMedGoogle Scholar
  40. 40.
    Tischendorf JJ, Hecker H, Kruger M, Manns MP, Meier PN (2007) Characterization, outcome, and prognosis in 273 patients with primary sclerosing cholangitis: a single center study. Am J Gastroenterol 102:107–114CrossRefPubMedGoogle Scholar
  41. 41.
    Hov JR, Boberg KM, Karlsen TH (2008) Autoantibodies in primary sclerosing cholangitis. World J Gastroenterol WJG 14(24):3781–3791.  https://doi.org/10.3748/wjg.14.3781 CrossRefPubMedGoogle Scholar
  42. 42.
    Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ, American Association for the Study of Liver Diseases, American College of Gastroenterology, American Gastroenterological Association (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Am J Gastroenterol 107(6):811–826  https://doi.org/10.1038/ajg.2012.128 CrossRefPubMedGoogle Scholar
  43. 43.
    Lim JS, Mietus-Snyder M, Valente A, Schwarz JM, Lustig RH (2010) The role of fructose in the pathogenesis of NAFLD and the metabolic syndrome. Nat Rev Gastroenterol Hepatol 7(5):251–264CrossRefPubMedGoogle Scholar
  44. 44.
    Arena U, Stasi C, Mannoni A, Benucci M, Maddali-Bongi S, Cammelli D, Assarat A, Marra F, Pinzani M (2012) Liver stiffness correlates with methotrexate cumulative dose in patients with rheumatoid arthritis. Dig Liver Dis 44(2):149–153CrossRefPubMedGoogle Scholar
  45. 45.
    Ahmed MH, Byrne CD (2005) Non Alcoholic Steatohepatitis and Metabolic syndrome. In: Byrne C, Wild S (eds) Metabolic syndrome. Wiley, Chichester, pp 279–305Google Scholar
  46. 46.
    Crowson CS, Matteson EL, Davis JM 3rd, Gabriel SE (2013) Contribution of obesity to the rise in incidence of rheumatoid arthritis. Arthritis Care Res (Hoboken) 65(1):71–77CrossRefGoogle Scholar
  47. 47.
    Koivuniemi R, Paimela L, Suomalinen R, Tornroth T, Leirisalo-Repo M (2008) Amyloidosis is frequently undetected in patients with rheumatoid arthritis. Amyloid 15(4):262–268CrossRefPubMedGoogle Scholar
  48. 48.
    Shimizu Y (2008) Liver in systemic disease. World J Gastroenterol 14(26):4111–4119CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Kumar R, Anandh K, Goel S (2015) Wilson’s disease masquerading as rheumatoid arthritis. Indian J Med Spec 6(1):33–35CrossRefGoogle Scholar
  50. 50.
    Schilsky ML, Mistry P (2001) Metabolic liver disease. Curr Opin Gastroenterol 17(3):221–231CrossRefPubMedGoogle Scholar
  51. 51.
    Cacoub P, Renou C, Rosenthal E, Cohen P, Loury I, Loustaud-Ratti V (2000) Extrahepatic manifestations associated with hepatitis C virus infection. A prospective multicenter study of 321patients. Extrahepatic manifestations associated with hepatitis C virus infection. A prospective multicenter study of 321 patients. The GERMIVIC. Groupe d’Etude et de Recherche en Medecine Interne et Maladies Infectieuses sur le Virus de l’Hepatite C. Medicine (Baltimore) 79(1):47–56CrossRefGoogle Scholar
  52. 52.
    Cacoub P, Comarmond C (2017) New insights into HCV-related rheumatologic disorders: a review. J Adv Res 8(2):89–97CrossRefPubMedGoogle Scholar
  53. 53.
    Koga T, Migita K, Miyashita T, Maeda Y, Nakamura M, Abiru S, Myoji M, Komori A, Yano K, Yatsuhashi H, Eguchi K, Ishibashi H (2008) Determination of anti-cyclic citrullinated peptide antibodies in the sera of patients with liver diseases. Clin Exp Rheumatol 26(1):121–124PubMedGoogle Scholar
  54. 54.
    Maya R, Gershwin ME, Shoenfeld Y (2008) Hepatitis B virus (HBV) and autoimmune disease. Clin Rev Allergy Immunol 34(1):85–102.  https://doi.org/10.1007/s12016-007-8013-6 CrossRefPubMedGoogle Scholar
  55. 55.
    Yılmaz N, Karadağ Ö, Kimyon G et al (2014) Prevalence of hepatitis B and C infections in rheumatoid arthritis and ankylosing spondylitis: a multicenter countrywide study. Eur J Rheumatol 1(2):51–54.  https://doi.org/10.5152/eurjrheumatol.2014.018 CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Guennoc X, Narbonne V, Jousse-Joulin S, Devauchelle-Pensec V, Dougados M, Daurres JP et al (2009) Is screening for hepatitis B and C useful in patients with recent-onset polyarthritis? Results of the ESPOIR cohort study. J Rheumatol 36(7):1407–1413CrossRefPubMedGoogle Scholar
  57. 57.
    Zheng B, Li T, Lin Q, Huang Z, Wang M, Deng W, Liao Z, Gu J (2012) Prevalence of hepatitis B surface antigen in patients with ankylosing spondylitis and its association with HLA-B27: a retrospective study from south China. Rheumatol Int 32(7):2011–2016CrossRefPubMedGoogle Scholar
  58. 58.
    Zerrak A, Bour JB, Tavernier C, Dougados M, Maillefert JF (2005) Usefulness of routine hepatitis C virus, hepatitis B virus, and parvovirus B19 serology in the diagnosis of recent-onset inflammatory arthritides. Arthritis Rheum 53(3):477–478CrossRefPubMedGoogle Scholar
  59. 59.
    Lok AS, McMahon BJ (2009) Chronic hepatitis B: update 2009. Hepatology 50(3):661–662CrossRefPubMedGoogle Scholar
  60. 60.
    Ghany MG, Strader DB, Thomas DL, Seeff LB, American Association for the Study of Liver Diseases (2009) Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 49(4):1335–1374CrossRefPubMedGoogle Scholar
  61. 61.
    Saag KG, Teng GG, Patkar NM et al (2008) American College of Rheumatology 2008 recommendations for the use of nonbiologic and biologic disease-modifying antirheumatic drugs in rheumatoid arthritis. Arthritis Rheum 59(6):762–784CrossRefPubMedGoogle Scholar
  62. 62.
    Palmore TN, Shah NL, Loomba R, Borg BB, Lopatin U, Feld JJ, Khokhar F, Lutchman G, Kleiner DE, Young NS, Childs R, Barrett AJ, Liang TJ, Hoofnagle JH, Heller T (2009) Reactivation of hepatitis B with reappearance of hepatitis B surface antigen after chemotherapy and immunosuppression. Clin Gastroenterol Hepatol 7(10):1130–1137CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Cacoub P, Gragnani L, Comarmonda C, Zignegoe AL (2014) Extrahepatic manifestations of chronic hepatitis C virus infection. Dig Liver Dis 46(5):S165–S173CrossRefPubMedGoogle Scholar
  64. 64.
    Mori S, Fujiyama S (2015) Hepatitis B virus reactivation associated with antirheumatic therapy: risk and prophylaxis recommendations. World J Gastroenterol 21(36):10274–10289.  https://doi.org/10.3748/wjg.v21.i36.10274 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Nakamura J, Nagashima T, Nagatani K, Yoshio T, Iwamoto M, Minota S (2016) Reactivation of hepatitis B virus in rheumatoid arthritis patients treated with biological disease-modifying antirheumatic drugs. Int J Rheum Dis 19:470–475CrossRefPubMedGoogle Scholar
  66. 66.
    Joseph AM (2012) Treatment of rheumatoid arthritis in patients with concomitant chronic hepatitis C infection. Ther Adv Musculoskelet Dis 4(1):35–40CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Mota LM, Cruz BA, Brenol CV et al (2013) Guidelines for the drug treatment of rheumatoid arthritis. Rev Bras Reumatol 53(2):158–183CrossRefPubMedGoogle Scholar
  68. 68.
    Jensen KO, Angst E, Hetzer FH, Gingert C (2016) Acute cytomegalovirus hepatitis in an immunocompetent host as a reason for upper right abdominal pain. Case Rep Gastroenterol 10(1):36–43CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Trier N, Izarzugaza J, Chailyan A, Marcatili P, Houen G (2018) Human MHC-II with shared epitope motifs are optimal Epstein–Barr virus glycoprotein 42 ligands—relation to rheumatoid arthritis. Int J Mol Sci 19(1):317.  https://doi.org/10.3390/ijms19010317 CrossRefPubMedCentralGoogle Scholar
  70. 70.
    Schiemann U, Kellner H (2002) Gastrointestinal side effects in the therapy of rheumatologic diseases. Z Gastroenetrol 40:937–943CrossRefGoogle Scholar
  71. 71.
    Lacroix I, Lapeyre-Mestre M, Bagheri H, Pathak A, Montastruc JL (2004) Club de Reflexion des cabinets de Groupe de Gastro-Enterologie (CREGG); General practitioner networks nonsteroidal anti-inflamatory drug-induced liver injury; a case–control study in primary care. Fundam Clin Pharmacol 18(2):201–206CrossRefPubMedGoogle Scholar
  72. 72.
    García Rodríguez LA, Williams R, Derby LE, Dean AD, Jick H (1994) Acute liver injury associated with nonsteroidal anti-inflammatory drugs and the role of risk factors. Arch Intern Med 154(3):311–316CrossRefPubMedGoogle Scholar
  73. 73.
    Tyagi P, Sharma BC, Sarin SK (2005) Cholestatic liver injury due to ibuprofen. Indian J Gastroenterol 24(2):77–78PubMedGoogle Scholar
  74. 74.
    Merlani G, Fox M, Oehen HP, Cathomas G, Renner EL, Fattinger K, Schneemann M, Kullak-Ublick GA (2001) Fatal hepatotoxicity secondary to nimesulide. Eur J Clin Pharmacol 57(4):321–326CrossRefPubMedGoogle Scholar
  75. 75.
    Mills PR, Sturrock RD (1982) Clinical associations between arthritis and liver disease. Ann Rheum Dis 41:295–307CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Goto E, Tomojiri S, Okamoto I, Tanaka K (2001) Methotrexate poisoning with acute hepatorenal dysfunction. J Toxicol Clin Toxicol 39:101–104CrossRefPubMedGoogle Scholar
  77. 77.
    Conway R, Carey JJ (2017) Risk of liver disease in methotrexate treated patients. World J Hepatol 9(26):1092–1100CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Curtis JR, Beukelman T, Onofrei A, Cassell S, Greenberg JD, Kavanaugh A, Reed G, Strand V, Kremer JM (2010) Elevated liver enzyme tests among patients with rheumatoid arthritis or psoriatic arthritis treated with methotrexate and/or leflunomide. Ann Rheum Dis 69(1):43–47CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Dirven L, Klarenbeek NB, van den Broek M, van Groenendael JH, de Sonnaville PB, Kerstens PJ, Huizinga TW, Dijkmans BA, Lems WF, Allaart CF (2013) Risk of alanine transferase (ALT) elevation in patients with rheumatoid arthritis treated with methotrexate in a DAS-steered strategy. Clin Rheumatol 32:585–590CrossRefPubMedGoogle Scholar
  80. 80.
    Conway R, Low C, Coughlan RJ, O’Donnell MJ, Carey JJ (2015) Risk of liver injury among methotrexate users: a meta-analysis of randomised controlled trials. Semin Arthritis Rheum 45(2):156–162CrossRefPubMedGoogle Scholar
  81. 81.
    Quintin E, Scoazec J-Y, Marotte H, Miossec P (2010) Rare incidence of methotrexate-specific lesions in liver biopsy of patients with arthritis and elevated liver enzymes. Arthritis Res Ther 12(4):R143.  https://doi.org/10.1186/ar3085 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Dehestani V, Shariati-Sarabi Z, Mohiti S, Akhlaghi S (2015) Liver toxicity in rheumatoid arthritis patients treated with methotrexate. Asia Pac J Med Toxicol 4:102–105Google Scholar
  83. 83.
    Schmajuk G, Miao Y, Yazdany J, Boscardin WJ, Daikh DI, Steinman MA (2014) Identification of risk factors for elevated transaminases in methotrexate users through an electronic health record. Arthritis Care Res (Hoboken) 66(8):1159–1166.  https://doi.org/10.1002/acr.22294 CrossRefGoogle Scholar
  84. 84.
    Whittle SL, Hughes RA (2004) Folate supplementation and methotrexate treatment in rheumatoid arthritis: a review. Rheumatology 43(3):267–271CrossRefPubMedGoogle Scholar
  85. 85.
    Prey S, Paul C (2009) Effect of folic or folinic acid supplementation on methotrexate-associated safety and efficacy in inflammatory disease: a systematic review. Br J Dermatol 160(3):622–628CrossRefPubMedGoogle Scholar
  86. 86.
    Sakthiswary R, Chan GY, Koh ET, Leong KP, Thong BY (2014) Methotrexate-associated nonalcoholic fatty liver disease with transaminitis in rheumatoid arthritis. Sci World J 2014:823763CrossRefGoogle Scholar
  87. 87.
    Malik F, Ranganathan P (2013) Methotrexate pharmacogenetics in rheumatoid arthritis: a status report. Pharmacogenomics 14(3):305–314.  https://doi.org/10.2217/pgs.12.214 CrossRefPubMedGoogle Scholar
  88. 88.
    Owen SA, Lunt M, Bowes J, Hider SL, Bruce IN, Thomson W, Barton A (2013) MTHFR gene polymorphisms and outcome of methotrexate treatment in patients with rheumatoid arthritis: analysis of key polymorphisms and meta-analysis of C677T and A1298C polymorphisms. Pharmacogenom J 13(2):137–147CrossRefGoogle Scholar
  89. 89.
    Aithal GP, Haugk B, Das S, Card T, Burt AD, Record CO (2004) Monitoring methotrexate-induced hepatic fibrosis in patients with psoriasis: are serial liver biopsies justified? Aliment Pharmacol Ther 19(4):391–399CrossRefPubMedGoogle Scholar
  90. 90.
    Ros S, Juanola X, Condom E, Canas C, Riera J, Guardiola J et al (2002) Light and electron microscopic analysis of liver biopsy samples from rheumatoid arthritis patients receiving long-term methotrexate therapy. Scand J Rheumatol 31:330–336CrossRefPubMedGoogle Scholar
  91. 91.
    Ledingham J, Gullick N, Irving K et al (2017) BSR and BHPR guideline for the prescription and monitoring of non-biologic disease-modifying anti-rheumatic drugs. Rheumatology 56(6):865–868.  https://doi.org/10.1093/rheumatology/kew479 CrossRefPubMedGoogle Scholar
  92. 92.
    Bird P, Griffiths H, Tymms K, Nicholls D, Roberts L, Arnold M, Burnet S, de Jager J, Scott J, Zochling J, Littlejohn G (2013) The SMILE study—safety of methotrexate in combination with leflunomide in rheumatoid arthritis. J Rheumatol 40(3):228–235CrossRefPubMedGoogle Scholar
  93. 93.
    Smolen JS, Landewé R, Bijlsma J et al (2017) EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2016 update. Ann Rheum Dis 76(6):960–977CrossRefPubMedGoogle Scholar
  94. 94.
    Visser K, Katchamart W, Loza E, Martinez-Lopez JA, Salliot C, Trudeau J et al (2009) Multinational evidence-based recommendations for the use of methotrexate in rheumatic disorders with a focus on rheumatoid arthritis: integrating systematic literature research and expert opinion of a broad international panel of rheumatologists in the 3E Initiative. Ann Rheum Dis 68(7):1086–1093CrossRefPubMedGoogle Scholar
  95. 95.
    Yeo W, Chan HL (2013) Hepatitis B virus reactivation associated with anti-neoplastic therapy. J Gastroenterol Hepatol 28(1):31–37CrossRefPubMedGoogle Scholar
  96. 96.
    Droz N, Gilardin L, Cacoub P et al (2013) Kinetic profiles and management of hepatitis B virus reactivation in patients with immune-mediated inflammatory diseases. Arthritis Care Res (Hoboken) 65(9):1504–1514CrossRefGoogle Scholar
  97. 97.
    Bersoff-Matcha SJ, Cao K, Jason M, Ajao A, Jones SC, Meyer T, Brinker A (2017) Hepatitis B virus reactivation associated with direct-acting antiviral therapy for chronic hepatitis c virus: a review of cases reported to the US Food and Drug Administration adverse event reporting system. Ann Intern Med 166(11):792–798CrossRefPubMedGoogle Scholar
  98. 98.
    Brunasso AM, Puntoni M, Gulia A, Massone C (2011) Safety of anti-tumour necrosis factor agents in patients with chronic hepatitis C infection: a systematic review. Rheumatology 50(9):1700–1711CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Clinic of Gastroenterology and HepatologyClinical Centre NisNišSerbia
  2. 2.Faculty of MedicineUniversity of NišNišSerbia
  3. 3.Institute for Treatment and RehabilitationNišSerbia
  4. 4.General HospitalLeskovacSerbia

Personalised recommendations