A Single Center Review of the Use of Mycophenolate Mofetil in the Treatment of Autoimmune Hepatitis
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1 CLINICAL GASTROENTEROLOGY AND HEPATOLOGY 2008;6: A Single Center Review of the Use of Mycophenolate Mofetil in the Treatment of Autoimmune Hepatitis JONATHAN T. HLIVKO, MITCHELL L. SHIFFMAN, R. TODD STRAVITZ, VELIMIR A. LUKETIC, ARUN J. SANYAL, MICHAEL FUCHS, and RICHARD K. STERLING Division of Gastroenterology, Hepatology, and Nutrition, Virginia Commonwealth University Health System, Richmond, Virginia Background & Aims: Standard treatment for autoimmune hepatitis (AIH) involves immune suppression by using prednisone alone or in combination with azathioprine (AZA). Although this regimen achieves remission in approximately 80%, some patients are intolerant or do not respond. Mycophenolate mofetil (MMF) is a potent immunosuppressant. However, its utility in AIH is not well-defined. Methods: We performed a retrospective longitudinal analysis of patients with AIH. Results: We identified 128 patients with AIH: mean age, 42.8 years; 83% female; 69% white. At presentation, median AST and ALT were 227 and 261 U/L, respectively, and bridging fibrosis and cirrhosis were present in 38% and 22%, respectively. Overall, 29 patients received MMF; 12 were switched to MMF after intolerance or nonresponse to prednisone AZA, whereas 17 received MMF prednisone as initial therapy. The main reasons for switching to MMF were nausea/vomiting (n 4) and failure to normalize liver enzymes (n 3). Ten of the 29 patients who received MMF therapy (34%) discontinued MMF as a result of side effects. Sixteen (84%) of the remaining 19 patients on MMF achieved remission, which closely matched the remission rate of those who remained on prednisone AZA (82%). The only independent clinical factor that predicted the eventual need for the use of MMF was absence of cirrhosis (P.0067). Conclusions: (1) MMF was associated with a high rate of intolerance (34%). (2) In those who could tolerate it, it was associated with a high rate of remission (84%). (3) Absence of cirrhosis on presentation was the only independent factor associated with eventual need for MMF. Autoimmune hepatitis (AIH) is a chronic disorder, occurring mainly in women, that is characterized by persistent hepatocellular necrosis and inflammation that if untreated can progress to cirrhosis and liver failure. 1 3 The etiology of AIH is related to dysfunction of the immune system directed against hepatocytes and is characterized by interface hepatitis and portal plasma cell infiltration found on liver biopsy, circulating autoantibodies and high serum globulin concentration, presence of other autoimmune disorders, and response to immunosuppressive therapy During the 1970s there were several controlled clinical studies performed that established the effectiveness of prednisone alone or in combination with azathioprine (AZA) for the treatment of AIH This therapeutic regimen has now become standard therapy, with remission rates of approximately 80% when it is used as first-line maintenance therapy. 13,14 Unfortunately, a minority of patients are either refractory or intolerant to standard therapy. Treatment of these complex patients has been attempted with various second-line therapeutic agents including cyclosporine, tacrolimus, mycophenolate mofetil (MMF), budesonide, and 6-mercaptopurine Each of these immunosuppressive agents has had varying degrees of success when used to treat a patient who failed standard therapy, but none has been formally recommended as the optimal secondline therapeutic agent to use when prednisone alone or in combination with AZA fails. MMF is an ester prodrug of mycophenolic acid that, on absorption, inhibits inosine monophosphate dehydrogenase, which prevents purine nucleotide synthesis and leads to inhibition of T- and B-cell lymphocyte proliferation. 18 This inhibitory process makes MMF a potent immunosuppressant and has allowed it to be used in clinical practice for the successful treatment of autoimmune disorders. Transplant centers have begun to incorporate MMF into the management of heart, renal, and liver transplant patients In fact, MMF has replaced AZA in many transplant centers because of its success in preventing graft rejection in those who were intolerant of AZA. 23,24 Therefore, it seems logical that MMF therapy could be attempted in a patient with AIH who is intolerant or unresponsive to standard therapy. Although several small retrospective studies have demonstrated the effectiveness of using MMF to treat AIH patients who fail standard therapy, one study of 8 patients found that MMF was not an effective alternative for those who failed standard therapy, 29 and therefore its utility in AIH remains to be defined. We describe our single center experience of treating AIH with MMF as a second-line therapy in patients who are either unresponsive or intolerant of standard therapy. Patients and Methods We performed a retrospective longitudinal analysis of all AIH patients followed by the Hepatology Department at Virginia Commonwealth University Health System between 1988 and This study was approved by the Committee on Human Subject Protection at Virginia Commonwealth University Health System. Patients were diagnosed with AIH following Abbreviations used in this paper: AASLD, American Association for the Study of Liver Diseases; AIH, autoimmune hepatitis; ANA, antinuclear antibody; ASMA, anti smooth muscle antibody; AZA, azathioprine; MMF, mycophenolate mofetil by the AGA Institute /08/$34.00 doi: /j.cgh
2 September 2008 USE OF MMF IN THE TREATMENT OF AUTOIMMUNE HEPATITIS 1037 American Association for the Study of Liver Diseases (AASLD) guidelines, which include the combination of elevated serum aminotransferase levels, presence of antinuclear antibody (ANA) or anti smooth muscle antibodies (ASMAs), hypergammaglobulinemia, and histologic evidence of chronic hepatitis. 14 Patients were excluded from this study if they had any other cause of chronic liver disease including Wilson s disease, hemochromatosis, alpha 1 -antitrypsin deficiency, sclerosing cholangitis, primary biliary cirrhosis, drug-related liver disease, alcoholic liver disease, and chronic viral hepatitis B or C. The demographic and clinical data from the patient s initial presentation were analyzed. Drug regimens and subsequent corticosteroid withdrawal were decided by the treating hepatologist in accordance with the treatment response of each individual patient. There was not a defined protocol for the treatment of AIH or the use of MMF. Treatment guidelines for AIH established by AASLD were used to define remission as the resolution of symptoms, reduction in serum aminotransferase levels to less than twice the normal upper limit, normalization of serum bilirubin and gamma globulin levels, and improvement in liver histology to normal or only mild portal hepatitis. 14 Adjustments in medications were made at the discretion of the attending hepatologist and were not a defined protocol to minimize side effects. Relapse or treatment failure was defined as worsening of symptoms and/or an increase in serum aminotransferase levels to more than 3 times the normal upper limit, or increase in serum gamma globulin levels of more than 2 g/dl, which strongly correlates with the presence of further histologic damage. 14,30 Statistical Methods Demographic, clinical, laboratory, and histologic data are presented as mean and standard deviation for normally distributed data, median and interquartile range for non-normal distributed data, and proportions for categorical data as indicated. The primary outcomes were to assess the use of MMF in those with AIH, its tolerance, and rate of achieving remission. The data from initial presentation as well as the effectiveness of the therapeutic regimens at achieving and maintaining remission were compared between those who responded to standard therapy (prednisone AZA) and those who received MMF therapy. Differences in continuous variables were compared by two-tailed Student t test and analysis of variance, and categorical variables were assessed by 2 or Fisher exact test as appropriate. For the primary outcomes (use of MMF and response to therapy), factors found on univariate analysis with a P value.25 were entered into a stepwise multiple logistic regression model for each outcome. A P value.05 was considered significant. All analyses were performed with JMP IN 7.0 (SAS Institute, Cary, NC). Results A total of 128 patients with AIH who met inclusion and exclusion criteria were identified, and demographic as well as clinical characteristics at the time of diagnosis for this cohort were recorded (Table 1). The mean age at diagnosis was 42.8 years, 83% were female, and 69% were white. The median (interquartile range) was as follows: AST, 227 U/L (93 659); ALT, 261 U/L ( ); alkaline phosphatase, 161 U/L ( ); and total bilirubin, 1.3 mg/dl ( ). The mean albumin Table 1. Patient Characteristics Variable Value N 128 Age (y) a Gender (% female) 83 Race (% white) 69 AST (U/L) b 227 (93 659) ALT (U/L) b 261 ( ) Alkaline phosphatase (U/L) b 161 ( ) Total bilirubin (mg/dl) b 1.3 ( ) Albumin (g/dl) a Globulin (g/dl) a ANA positive (%) 61 ASMA positive (%) 47 Bridging fibrosis (%) 38 Cirrhosis (%) 22 a Mean standard deviation. b Median (interquartile range). level was 3.54 g/dl, and mean total globulin was 4.1 g/dl. Sixty-one percent of the patients were positive for ANA, and 47% were positive for ASMA. Bridging fibrosis and cirrhosis were present in liver biopsies of 38% and 22% of patients, respectively. The therapeutic regimens of the 128 AIH patients included in our retrospective study were recorded and indicated that initial induction therapy consisted of prednisone (n 117), AZA, MMF, and tacrolimus alone (n 1 each). Eight patients did not receive induction therapy because of mild disease on biopsy and mild elevations in transaminase levels. Three patients received an immunosuppressant other than prednisone for induction therapy as a result of comorbid conditions such as severe osteoporosis or diabetes in which the risk of using prednisone outweighed the benefits. After induction therapy (Figure 1), first-line maintenance therapy was established and included standard therapy with combination prednisone AZA (n 85) and monotherapy with prednisone (n 7) and AZA (n 7), MMF therapy with combination prednisone MMF (n 16) and monotherapy with MMF (n 1), and the remaining patients were on monotherapy with tacrolimus (n 1) or no immunosuppressant therapy (n 11). Sixteen of the 99 patients receiving standard therapy as their first-line maintenance therapy failed or could not tolerate the treatment. The mean duration of therapy in these patients before changing their regimen was 13 months (range, 3 39 months). Twelve of these patients were switched to a second-line maintenance regimen with MMF therapy, which included 10 prednisone MMF, 1 MMF alone, and 1 prednisone MMF tacrolimus. The reasons these patients discontinued standard therapy are summarized in Table 2 and include nausea/vomiting (n 4), failure to normalize liver enzymes (n 3), pancreatitis (n 1), deep venous thrombosis (n 1), rash (n 1), hair loss (n 1), and intolerance (n 1). A total of 29 patients were found to have been treated with a regimen that used MMF therapy at a dose of mg/day. Of these, 16 were on 500 mg twice a day, and 13 were on 1000 mg twice a day. The 3 patients who failed to achieve remission while on MMF therapy included 1 patient on 500 mg twice a day and 2 on 1000 mg twice a day. Of the 10 (34%) patients who failed or could not tolerate MMF therapy, 6 were
3 1038 HLIVKO ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No. 9 Figure 1. Therapeutic regimens for 128 patients with AIH. on 500 mg twice a day, and 4 were on 1000 mg twice a day. Reasons for discontinuing MMF included headache (n 3), failure to normalize liver enzymes (n 3), nausea/vomiting (n 3), and myalgias (n 1). No patient required discontinuing MMF as a result of diarrhea or leukopenia. The remaining 19 patients who continued second-line maintenance therapy with MMF involved regimens that included MMF alone (n 5), MMF and prednisone (n 12), MMF combined with prednisone and tacrolimus (n 1), and MMF and cyclosporine (n 1). Of these 19 patients, there were 16 (84%) who entered remission (11 were on prednisone MMF, 3 on MMF alone, 1 Table 2. Reasons Patients Discontinued Prednisone (P) AZA and the MMF Regimen Started Patient Initial treatment Reason for switch MMF therapy 1 P AZA Nausea/vomiting P MMF 2 P AZA Nausea/vomiting P MMF 3 P AZA Nausea/vomiting P MMF 4 P AZA Nausea/vomiting P MMF 5 P AZA Failure to normalize LFTs P MMF 6 P AZA Failure to normalize LFTs P MMF FK 7 P AZA Intolerance P MMF 8 P AZA Pancreatitis P MMF 9 P AZA Deep venous thrombosis P MMF 10 P AZA Hair loss P MMF 11 P AZA Rash P MMF 12 AZA Failure to normalize LFTs MMF FK, tacrolimus; LFT, liver function tests. on prednisone MMF tacrolimus, and 1 on MMF cyclosporine). The doses of MMF in these 16 who entered remission were 500 mg twice a day in 9 patients and 1000 mg twice a day in 7 patients. Therefore, the overall remission rate was 55% (16/29) in those receiving MMF therapy and 84% (16/19) in those who tolerated MMF therapy (Figure 1). Evaluation of the 12 patients who received standard therapy for first-line therapy and then were switched to MMF for second-line therapy found that 8 (67%) were able to achieve remission. For comparison, examination of those patients receiving standard therapy found an overall remission rate of 69% (68/99), and for those patients who tolerated standard therapy, their remission rate was 82% (68/83). Evaluation of tolerance found that 84% (83/99) of patients tolerated standard therapy, and 66% (19/29) tolerated MMF therapy. The laboratory data from the initial presentation of the 99 patients who underwent standard therapy were compared with those of the 29 patients who were treated with MMF, and no significant differences were revealed (Table 3). When controlling for all initial clinical variables, the absence of cirrhosis on initial liver biopsy was the only significant independent variable (P.0067) that predicted the eventual need for MMF therapy. Discussion AIH, a disease most commonly seen in women, is caused by an immune system malfunction directed against hepatocytes. 1 3 The treatment of AIH involves immune suppression with corticosteroids alone or in combination with AZA. This treatment, which is considered standard therapy, is highly effective, achieving remission in approximately 80% of the
4 September 2008 USE OF MMF IN THE TREATMENT OF AUTOIMMUNE HEPATITIS 1039 Table 3. Comparison of the Initial Laboratory Values of the Standard Therapy Group With Those of Patients Treated With MMF Laboratory data Standard therapy MMF therapy P value N AST (U/L) ALT (U/L) Alkaline phosphatase (U/L) Total bilirubin (mg/dl) Albumin (g/dl) Total protein (g/dl) Total globulin (g/dl) Data presented as mean standard deviation. cases. 13,14 The subset of patients who do not respond to standard therapy or who cannot tolerate the side effects of corticosteroids or AZA have become the focus for the use of various immunosuppression agents including calcineurin inhibitors (cyclosporine and tacrolimus), purine inhibitor (MMF), and those with corticosteroid action (budesonide) All of the second-line immunosuppressive agents have had varying degrees of success in treating patients with AIH who failed or could not tolerate standard therapy. 17,28,31 Recently, much focus has been placed on MMF as a second-line therapy because it is being used more frequently in place of AZA in organ transplantation regimens. 23,24 Like AZA, MMF is a purine inhibitor. However, it is more lymphocyte-specific and is associated with somewhat less toxic side effects including less bone marrow suppression, fewer opportunistic infections, and lower incidence of acute rejection. 18,24 Furthermore, MMF has been used effectively to treat other autoimmune diseases such as systemic lupus erythematosus in which patients were intolerant of or resistant to the conventional immunosuppressive regimen, 32,33 rheumatoid arthritis, systemic vasculitis, and autoimmune hemolytic anemia MMF has been well-established through the use of prospective trials in transplant patients and has shown excellent efficacy, allowing it to replace AZA in many transplant center protocols. MMF has a decreased side effect profile as compared with the nephrotoxicity and neurotoxicity seen with long-term use of calcineurin inhibitors or the impaired glucose tolerance, obesity, and osteoporosis seen with steroids. 23,24 Therefore, it had a rational use in the treatment of AIH. To date, 4 studies with a total of 43 patients demonstrate that MMF can be used successfully to induce remission in patients with AIH who did not respond to or could not tolerate standard therapy Conversely, one study that examined 8 patients with AIH indicated that the use of MMF did not result in resolution of abnormal biochemical data, and it did not prevent further fibrosis. 29 In this report, we describe our experience with MMF therapy to treat 29 patients with AIH. We found that although 10 of the 29 patients (34%) were switched from MMF to another medical regimen, in those who could tolerate it, MMF was able to achieve a high rate of remission (84%) comparable to standard therapy. However, because initial use of standard therapy was tolerated by 83 of 99 patients (84%), prednisone AZA should still be used as first-line therapy. We compared the histologic and clinical data from the 29 patients who required MMF therapy with those of the patients who were on standard therapy and identified absence of cirrhosis on initial liver biopsy as the only independent variable significantly associated with eventual need for MMF. Therefore, we provide data that demonstrate MMF is an effective alternate in treating patients who fail standard therapy, as well as for the first time we suggest that patients who present without cirrhosis are more likely to eventually need MMF therapy. Our study was not without limitations. Similar to others, ours was retrospective, and we did not use a standard protocol for treating AIH. Also, treatment of these patients by 5 different hepatologists could have led to caregiver bias regarding the choice of second-line therapy as well as the dosing. Consequently, doses of MMF varied between 500 and 2000 mg per day. However, the dose of MMF did not appear to impact on our results. Furthermore, having different hepatologists with their own practice methods caused some patients to have a second liver biopsy, whereas others were followed solely by symptoms and laboratory data. In addition, because improvements in histology correlated with improved aminotransferase levels, we felt comfortable evaluating the success of MMF by using laboratory data from follow-up visits in conjunction with the AASLD guidelines to declare biochemical remission. 14 We conclude that use of MMF in the treatment of AIH in those who were intolerant or not responsive to standard therapy with prednisone AZA was reasonably tolerated with a high rate of remission (84%), and that absence of cirrhosis on presentation was the only independent factor associated with eventual need for MMF. However, because of the high response and tolerance to standard therapy coupled with the high cost of MMF, its use cannot be recommended as initial therapy but can be considered a good choice for second-line therapy. References 1. Krawitt EL. Autoimmune hepatitis. N Engl J Med 2006;354: Czaja AJ, Bianchi FB, Carpenter HA, et al. Treatment challenges and investigational opportunities in autoimmune hepatitis. Hepatology 2005;41: Feld JJ, Dinh H, Arenovich T, et al. Autoimmune hepatitis: Effect of symptoms and cirrhosis on natural history and outcomes. Hepatology 2005;42: Czaja AJ, Carpenter HA. Sensitivity, specificity, and predictability of biopsy interpretations in chronic hepatitis. Gastroenterology 1993;105: Frazer IH, Mackay IR, Bell J, et al. The cellular infiltrate in the liver in auto-immune chronic active hepatitis: analysis with monoclonal antibodies. Liver 1985;5: Krawitt EL, Kilby AE, Albertini RJ. 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5 1040 HLIVKO ET AL CLINICAL GASTROENTEROLOGY AND HEPATOLOGY Vol. 6, No Galbraith RM, Smith M, Mackenzie RM, et al. High prevalence of seroimmunological markers in relatives of patients with active chronic hepatitis or primary biliary cirrhosis. N Engl J Med 1974; 290: Czaja AJ. Natural history, clinical features, and treatment of autoimmune hepatitis. Semin Liver Dis 1984;4: Alvarez F, Berg PA, Bianchi FB, et al. International Autoimmune Hepatitis Group report: review of criteria for diagnosis of autoimmune hepatitis. J Hepatol 1999;31: Cook GC, Mulligan R, Sherlock S. Controlled prospective trial of corticosteroid therapy in active chronic hepatitis. Q J Med 1971; 40: Soloway RD, Summerskill WH, Baggenstoss AH, et al. Clinical, biochemical, and histological remission of severe chronic active liver disease: a controlled study of treatments and early prognosis. Gastroenterology 1972;63: Murray-Lyon IM, Stern RB, Williams R. 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Transplantation 1998;66: Warrens AN. The evolving role of mycophenolate mofetil in renal transplantation. QJM 2000;93: Sollinger HW. Mycophenolate mofetil for the prevention of acute rejection in primary cadaveric renal allograft recipients: U.S. Renal Transplant Mycophenolate Mofetil Study Group. Transplantation 1995;60: Eckhoff DE, McGuire BM, Frenette LR, et al. Tacrolimus and mycophenolate mofetil combination therapy versus tacrolimus in adult liver transplantation. Transplantation 1998;65: Ferraris JR, Tambutti ML, Redal MA, et al. Conversion from azathioprine to mycophenolate mofetil in pediatric renal transplant recipients with chronic rejection. Transplantation 2000;70: Woodroffe R, Yao G, Meads C, et al. Clinical and cost-effectiveness of newer immunosuppressive regimens in renal transplantation: a systematic review and modelling study. Health Technol Assess 2005;9: Richardson PD, James PD, Ryder SD. Mycophenolate mofetil for maintenance of remission in autoimmune hepatitis in patients resistant to or intolerant of azathioprine. J Hepatol 2000;33: Devlin SM, Swain MG, Urbanski SJ, et al. Mycophenolate mofetil for the treatment of autoimmune hepatitis in patients refractory to standard therapy. Can J Gastroenterol 2004;18: Chatur N, Ramji A, Bain VG, et al. Transplant immunosupressive agents in non-transplant chronic autoimmune hepatitis: the Canadian Association for the Study of Liver (CASL) experience with mycophenolate mofetil and tacrolimus. Liver Int 2005;25: Inductivo-Yu I, Adams A, Gish RG, et al. Mycophenolate mofetil in autoimmune hepatitis patients not responsive or intolerant to standard immunosuppressive therapy. Clin Gastroenterol Hepatol 2007;5: Czaja AJ, Carpenter HA. Empiric therapy of autoimmune hepatitis with mycophenolate mofetil: comparison with conventional treatment for refractory disease. J Clin Gastroenterol 2005;39: Czaja AJ, Wolf AM, Baggenstoss AH. Laboratory assessment of severe chronic active liver disease during and after corticosteroid therapy: correlation of serum transaminase and gamma globulin levels with histologic features. Gastroenterology 1981;80: Heneghan MA, McFarlane IG. Current and novel immunosuppressive therapy for autoimmune hepatitis. Hepatology 2002;35: Dooley MA, Cosio FG, Nachman PH, et al. Mycophenolate mofetil therapy in lupus nephritis: clinical observations. J Am Soc Nephrol 1999;10: Karim M, Alba P, Cuadrado M, et al. Mycophenolate mofetil for systemic lupus erythematosus refractory to other immunosuppressive agents. Rheumatology 2002;41: Goldblum R. Therapy of rheumatoid arthritis with mycophenolate mofetil. Clin Exp Rheumatol 1993;11(Suppl 8):S117 S Nowack R, Gobel U, Klooker P, et al. Mycophenolate mofetil for maintenance therapy of Wegener s granulomatosis and microscopic polyangiitis: a pilot study in 11 patients with renal involvement. J Am Soc Nephrol 1999;10: Zimmer-Molsberger B, Knauf W, Thiel E. Mycophenolate mofetil for severe autoimmune hemolytic anemia. Lancet 1997;350: Address requests for reprints to: Richard K. Sterling, MD, MSc, Professor of Medicine, Division of Gastroenterology, Hepatology, and Nutrition, Virginia Commonwealth University Medical Center, 1200 E Broad Street, West Hospital, Room 1492, Richmond, Virginia rksterli@hsc.vcu.edu; fax: (804) This work was presented at the Annual Meeting of the American College of Gastroenterology, Philadelphia, PA, October 13 16, 2007.
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