Best Practice & Research Clinical Gastroenterology

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1 Best Practice & Research Clinical Gastroenterology 24 (2010) Contents lists available at ScienceDirect Best Practice & Research Clinical Gastroenterology 7 Gastrointestinal and liver adverse effects of drugs used for treating IBD Gerhard Rogler, MD, PhD, AGAF, Professor, Novartis Chair of Gastroenterology * Division of Gastroenterology and Hepatology, Department of Visceral Medicine, University Hospital Zürich, Rämistrasse 100, CH-8091 Zürich, Switzerland Keywords: Inflammatory bowel disease Treatment Adverse effects Hepatotoxicity Drugs used for treating inflammatory bowel disease are known to have a number of gastrointestinal and liver adverse effects. 5-ASA products are relatively safe and have few adverse events. In contrast sulfasalazine has side effects in 11 40% of treated patients including fatigue, nausea, abdominal pain and diarrhoea. Glucocorticoids can induce or propagate peptic ulcers and upper GI bleeding especially in combination with NSAIDs. Thioguanins may have severe gastrointestinal side effects including gastrointestinal complaints (in up to 12%), hepatotoxicity (up to 4%) and pancreatitis (1%). Nodular regenerative hyperplasia (NRH) is an important potential side effect of thiopurine therapy especially in men with Crohn s disease after ileocecal resection. NRH may ultimately lead to portal hypertension. A major concern of methotrexate therapy in IBD besides myelosuppression and pulmonary fibrosis is hepatotoxicity. 5 mg of folic acid substitution per week potentially decreases gastrointestinal side effects by 80% without interfering with the efficacy of methotrexate. Besides renal dysfunction, tremor, hirsutism, hypertension and gum hyperplasia cyclosporine is known to have a number of gastrointestinal side effects that occur with less frequency such as diarrhoea (up to 8%) nausea and vomiting (up to 10%) and hepatotoxicity in 1 4%. Rare gastrointestinal adverse events are gastritis and peptic ulcers. Paying attention to these potential deleterious side effects is mandatory for physicians treating IBD patients. Ó 2009 Elsevier Ltd. All rights reserved. * Tel.: þ ; fax: þ address: gerhard.rogler@usz.ch /$ see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi: /j.bpg

2 158 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) Introduction In recent years a huge number of clinical studies aimed to improve the treatment of patients with inflammatory bowel diseases (IBD) have been published. Much progress has been made and new drugs have been added to the standard treatment of IBD patients. The treatment is getting more individualized. Therefore, it becomes more important to know all the features of the drugs we use. We now have a tableau of alternatives if adverse effects of treatment occur. As there is a number of substances in the armamentarium used for IBD treatment that have gastrointestinal and hepatic side effects it may be useful to review these side effects but also the alternatives we have now to avoid negative influences of the treatment on the quality of live for our patients. Aminosalicylates All new ASA products are relatively safe and have similar AE rates as compared with placebo. Most frequent are diarrhoea (3%), headache (2%), nausea (2%), rash (1%) and thrombocytopenia (<1%) (Table 1). In most cases treatment with 5-ASA compounds can be continued (see Table 1). Sometimes a dose reduction may be necessary. Interestingly, side effects such as bloating or abdominal pain may improve or disappear when the 5-ASA compound is changed. This indicates that not 5-ASA but additional constituents may be responsible for those side effects. In contrast to 5-ASA, sulfasalazine has side effects in 11 40% of treated patients including fatigue, nausea, abdominal pain and diarrhoea (Table 1). These adverse effects are usually attributed to the activity of sulfapyridine in the gastrointestinal lumen, as well as that absorbed into the system. Glucocorticoids Glucocorticoids (GC) are used for the suppression or reduction of inflammation in a wide variety of diseases such as rheumatoid diseases, allergic diseases, IBD and autoimmune diseases in general [1 4]. GC have been proven to be the first choice in the treatment of acute flares of inflammatory bowel disease in several major studies [4 8,9,10] The systemic administration of GC (oral or iv.) during acute flares of Crohn s disease or ulcerative colitis is followed by a multitude of different effects in different body cells. Among the intended effects of therapeutically administrated GC is the downregulation of the expression of multiple cytokines and their receptors [11], chemokines and their receptors [12,13], kinins and their receptors, adhesion molecules and inflammation associated enzymes like inducible nitric oxide synthase (inos) and the inducible cyclooxygenase (COX-2) [14]. GC influence about 20% of the human genome and their effects spare no organs and tissues. From those facts it is obvious that they must have side effects relevant in gastroenterology. The underlying molecular mechanisms for GC-mediated side effects are complex, and only partly understood. Data suggest that certain side effects are predominantly mediated via transactivation (e.g., diabetes, glaucoma), whereas others are predominantly mediated via transrepression (e.g., suppression of the hypothalamic pituitary adrenal axis). The literature on the gastrointestinal safety of oral GCs is controversial. It has been discussed (but has become less important in the era of PPIs) that GCs can induce or propagate peptic ulcers and upper GI bleeding (Tables 1 and 2). Results from clinical trials and epidemiological studies have been somewhat heterogeneous, either indicating a dose-dependent increased risk of peptic ulcers in the groups treated with GCs or no difference to controls. The highest reported pooled relative risk for peptic ulcers in a meta-analysis had been 2.3. However, clear data exist regarding the enhancement of risk associated with NSAIDs by concomitant GC therapy. The incidence of upper GI bleeding in a cohort of 19,880 ambulant patients with dermatitis or asthma systemically treated with GCs was increased if the patients were additionally receiving anticoagulants [15]. In comparison with patients receiving NSAIDs without GCs, the relative risk for peptic ulcers increased with simultaneous GC therapy by a factor of 14.6 (95% confidential interval, ) [16]. In distinct patient populations, such as in patients with rheumatoid arthritis, GC therapy (relative risk, 2.9) may represent an even more important risk factor for gastrointestinal complications than NSAIDs (relative risk, 1.4) [17]. In addition, there have been case reports that GCs may induce acute pancreatitis [18].(Tables 1 and 2).

3 Table 1 Drugs used for the treatment, their gastrointestinal and hepatic side effects and measures to be taken upon adverse effects (brand names given are just examples and not a complete list). Drug Brand names Adverse effect Frequency of AE Measures recommended upon AEs 5-ASA Asacol Ò diarrhoea rare a reduce dosage or stop treatment Mesazin Ò abdominal pain rare reduce dosage or stop treatment Pentasa Ò nausea rare reduce dosage or stop treatment Salofalk Ò vomiting rare reduce dosage or stop treatment Sulfasalazine Glucocorticoids Azathioprine Salazopyrine Ò diarrhoea up to 30% reduce dosage or switch to 5-ASA Azulfidine Ò abdominal pain 8 25% reduce dosage or switch to 5-ASA nausea 19 33% reduce dosage or switch to 5-ASA vomiting 8% reduce dosage or switch to 5-ASA dypepsia 13% reduce dosage or switch to 5-ASA stomatitis 4% reduce dosage or switch to 5-ASA abnormal liver function test 4% switch to 5-ASA Decortin Ò Medrol Ò Orapred Ò Prednisol Ò Spiricort Ò Sterapred Ò Azafalk Ò Azamun Ò Azarek Ò Azasan Ò Imuran Ò Imurek Ò gastritis, peptic ulcer rare add PPI; stop NSAIDs pancreatitis very rare stop treatment hepatic steatosis? diet? nausea 12% switch to 6-MP or try increasing dosage regimen vomiting 12% switch to 6-MP or try increasing dosage regimen abdominal pain 15% slow increase of dosage; take drug with meals; if no improvement: switch to 6-MP severe diarrhoea rare associated with fever and malaise: stop treatment pancreatitis rare stop treatment; don t switch to another thiopurine hepatotoxicity (elevation of serum alkaline phosphatase, bilirubin, and/or serum transaminases 1 3% stop treatment; don t switch to another thiopurine 6-MP Purinethol Ò nausea common reduce dosage, consider 6-TG or switch to non-thiopurine immunosuppressant vomiting common reduce dosage, consider 6-TG or switch to non-thiopurine immunosuppressant pancreatitis rare switch to non-thiopurine immunosuppressant intestinal ulceration very rare switch to non-thiopurine immunosuppressant biliary stasis; hepatotoxicity common (dosage dependent) switch to non-thiopurine immunosuppressant hepatic necrosis very rare in IBD patients switch to non-thiopurine immunosuppressant (continued on next page) G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010)

4 Table 1 (continued) Drug Brand names Adverse effect Frequency of AE Measures recommended upon AEs Thioguanine Lanvis Ò nausea common reduce dosage, or switch to non-thiopurine immunosuppressant vomiting common reduce dosage, or switch to non-thiopurine immunosuppressant pancreatitis rare switch to non-thiopurine immunosuppressant biliary stasis; hepatotoxicity common (dosage dependent) switch to non-thiopurine immunosuppressant Methotrexate Cyclosporine hepatotoxicity (elevation of liver enzymes frequent the day after administration; not predictive for liver fibrosis) common (up to 25%) in patients with psoriasis; less frequent (?) in IBD stop treatment (?) nausea common use folic acid or stop treatment vomiting rare use folic acid or stop treatment diarrhoea common use folic acid or stop treatment Neoral Ò diarrhoea 1 8% stop treatment Sandimmun Ò nausea 1 10% reduce dosage or switch to tacrolimus vomiting 1 5% reduce dosage or switch to tacrolimus hepatotoxicity 1 4% reduce dosage or switch to tacrolimus gastritis rare reduce dosage or switch to tacrolimus peptic ulcers rare reduce dosage or switch to tacrolimus Tacrolimus Prograf Ò diarrhoea 27 47% reduce dosage or stop treatment nausea 27 46% (not as common in UC) reduce dosage or stop treatment constipation up to 25% usually not a problem in IBD a According to the WHO standard definition for drug and vaccine adverse events: very common (>1/10); common (>1/100); uncommon (>1/1000); rare (>1/10,000); very rare (<1/10,000). 160 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010)

5 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) Table 2 Gastrointestinal side effects and drugs inducing these side effects. Side effect Induced by Diarrhea 5-ASA (rare a ), Sulfasalazine (common), AZA (rare), Methotrexate (common, dosage dependent), Cyclosporine (rare), Tacrolimus (common) Nausea 5-ASA (rare), Sulfasalazine (common, 19 33%), AZA (common, up to 12%), 6-MP (common), 6-TGN (common), Methotrexate (common), Cyclosporine (1 10%), Tacrolimus (27 46%) Vomiting 5-ASA (rare), Sulfasalazine (8%), AZA (12%), 6-MP (common), 6-TGN (common), Methotrexate (rare), Cyclosporine (1 5%); Tacrolimus (common) Hepatotoxicity Sulfasalazine (abnormal liver function tests 4%), AZA (severe 1 3%), 6-MP (common), 6-TGN (common), Methotrexate (common, up to 25% in psoriasis patients), Cyclosprine (1 4%), Tacrolimus (rare) NRH AZA (rare), 6-MP (rare), 6-TGN (common; however, dosage in respective studies too high; may be rare with adequate dosage) Steatosis Glucocorticoids (?) Pancreatitis 5-ASA (very rare), Sulfasalazine (very rare), Glucocorticoids (very rare), Azathioprine (rare), 6-MP (rare), 6-TGN (rare), Gastritis, peptic ulcers Sulfasalazine (very rare), Glucocorticoids (rare, in combination with NSAIDs), 6-MP (very rare), 6-TGN (very rare), Cyclosporine (rare) Constipation Tacrolimus (common) a according to the WHO standard definition for drug and vaccine adverse events: very common (>1/10); common (>1/100); uncommon (>1/1000); rare (>1/10,000); very rare (<1/10,000). Chronic exposure to GC treatment further is associated with central adiposity, dyslipidaemia, insulin resistance, glucose intolerance and overt diabetes. GC-induced hepatic insulin resistance results in impaired suppression of hepatic glucose production by insulin. These changes in hepatic lipid metabolism may induce hepatic steatosis, however, the currently available data are not conclusive yet. Azathioprine, 6-mercaptopurine, 6-thioguanine The immunosuppressive thiopurines azathioprine (AZA) and 6-mercaptopurine (6-MP) are widely used for the treatment of IBD. Their final effector-metabolite 6-thioguanine nucleotides (6-TGN) can also be given as a drug, however further clinical evaluation unfortunately has been stopped due to hepatic adverse effects (which were due to high dosages). Thiopurines have demonstrated efficacy in the induction as well as in the maintenance of remission of both Crohn s disease and ulcerative colitis. Mainly AZA has been evaluated in clinical studies with IBD patients and subsequently approved for IBD treatment. In Europe 6-MP has only been approved for haematological disease (leukemia) and is less well established despite the fact that azathioprine is metabolized to 6-MP in the human body and studies on efficacy of azathioprine therefore of course also have proven the efficacy of 6-MP. In clinical practise up to 40% of patients with IBD have to discontinue using AZA because of adverse effects and/or therapeutic failure [19] (see Table 1). Both AZA and 6-MP undergo metabolic transformations to 6-TG which is the final effectormetabolite as mentioned and exerts immunosuppressive activity. The liver is an important organ for AZA metabolism. Around 90% of absorbed AZA is transformed in the liver to 6-MP and 1-methyl-4- nitro-5-thioimidazole. The remaining 10% of AZA, is transformed to other compounds such as hypoxanthine and S-methyl-4-nitro-5-thioimidazole. The absorption of AZA is variable, both interindividually and intraindividually. Subsequently the bioavailability of AZA varies from 16% to 72%. The plasma half-life of 6-MP is in the range of 1 2 h. 6-MP is metabolized by xanthine oxidase, thiopurine S- methyltransferase (TPMT) and hypoxanthine phosphoribosyltransferase (HPRT). TPMT methylates 6- MP to form 6-methylmercaptopurine (6-MMP). 6-MMP is responsible for many side effects of treatment having no desired pharmacological activity. The first step for the formation of the effector molecule 6-TGN is mediated by HPRT. 6-TGNs have an average half-life of approximately five days (range 3 13 days). The metabolism of 6-TG obviously must be less complex than that of 6-MP and AZA as it is the final product of AZA and 6-MP degradation. The absorption of orally administered 6-TG is incomplete and

6 162 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) variable, leading to a bioavailability of 14 46%. Plasma concentrations of 6-TG generally become undetectable after 6 h due to its rapid intracellular transport. Gastrointestinal adverse effects of thiopurine therapy are hepatitis, abdominal pain/and pancreatitis. Most commonly side effects and adverse events occur within four weeks after initiation of thiopurine therapy. Some studies have demonstrated that some adverse effects of AZA therapy such as flu-like symptoms, fever and arthralgia can partially be avoided by switching to 6-MP therapy, however gastrointestinal side effects usually do not improve upon change from AZA to 6-MP treatment [20]. The incidence of 6-TG-induced dose-independent adverse effects is reported to be around 20% [21]. In a 1-year trial of 6-TG therapy that included a series of 95 patients, the gastrointestinal adverse effects that led to withdrawal of 6-TG were gastrointestinal complaints (8.4%), hepatotoxicity (4%) and pancreatitis (1%) [21]. Especially hepatotoxicity has been a concern for physicians prescribing thioguanins to IBD patients. A variety of abnormal liver tests have been described interpreted as signs of hepatotoxicity. The mechanisms by which thiopurines cause hepatotoxicity are unknown. Thiopurine-induced hepatotoxicity can be dose-independent or dose-dependent. The definition of hepatotoxicity varied in the respective studies as did the reported frequency of elevated liver enzymes under treatment with AZA or 6-MP (between 0% and 17%) [22 24]. In general, elevated liver enzyme levels normalize after cessation of thiopurine therapy. Elevated liver enzymes and hepatotoxicity have been associated with certain metabolites of thiopurines, the 6-methylmercaptopurine-ribonucleotides (consisting of 6-methyl thioinosine 5 0 -monophosphate, 6-methyl thioinosine 5 0 -diphosphate and 6-methyl thioinosine 5 0 -triphosphate). However, as 6-MMPRs are not routinely quantified in specialized labs this is not really helpful for the daily practise. In addition, this association has been found inconsistent in some studies. In addition to elevated liver enzymes, anatomical changes of the liver structure have been described under thiopurine therapy: Sinusoidal dilatation, nodular regenerative hyperplasia (NRH), fibrosis, peliosis hepatis and veno-occlusive disease (VOD) are considered to be signs of dose-dependent hepatotoxicity of thiopurines. These histopathological changes often appear after months to years of thiopurine therapy. Whether these histological liver alterations are reversible is unknown [25]. However, there are reports of NRH with portal hypertension that disappeared after discontinuation of AZA/6-MP. NRH may ultimately lead to noncirrhotic portal hypertension with splenomegaly [26]. The frequency of NRH cause by thiopurine therapy is still a matter of discussion. By a systematic survey of patients in 11 centres thirtyseven cases of NRH were identified between 1994 and 2005 [27]. Male sex and ileocecal resection upon stricturing disease behaviour were associated with NRH in those patients treated with thiopurines [27]. Overall the frequency of symptomatic NRH in this study was low, however, the prevalence of asymptomatic forms of NRH was high [27]. The use of 6-TG especially has been associated with the development of NRH [26,28]. However, the mg of 6-TG were administered in those studies resulting in 6-TGN levels in RBCs above 1000 pmol/8 108, whereas with AZA or 6-MP we aim to reach levels around pmol/ RBCs. In studies with such high 6-TGN levels NRH was diagnosed in 18 62% of liver biopsy samples. [26,28,29] In smaller studies and recent reports of low dose 6-TG treatment reaching 6-TGN-levels as usual for AZA or 6-MP no increased rate of NRH was observed [30 32]. It seems to be very likely that studies on 6-TG have been stopped because of inadequate dosing in those studies [31,32]. Thus an AZA/6-MP metabolite with much less side effects will probably never be approved for IBD treatment. Methotrexate Methotrexate is used with long lasting experience in rheumatology and has been introduced into IBD therapy by the studies of Feagan and coworkers [33,34]. MTX acts as a dihydrofolic acid analogue that binds to the dihydrofolic acid reductase enzyme by inhibiting the synthesis of tetrahydrofolate, which is required for DNA synthesis. De novo inhibition of purine and pyrimidine synthesis leads to DNA defects, which results in apoptosis. Rapidly proliferating tissues such as expanding T-cells are susceptible to the effects of methotrexate without irreversible damage to normal tissues. Use of

7 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) methotrexate is restricted by the risk of organ toxicity (Table 1). Major concerns are myelosuppression, hepatotoxicity and pulmonary fibrosis. Early recommendations for periodic liver biopsies were based on the experience in patients with psoriasis who were given MTX. Among patients with psoriasis receiving methotrexate, rates of hepatic fibrosis as high as 25 50% have been published [35 37] The cause of methotrexate-induced hepatic fibrosis is unknown. In psoriasis patients it has been recommended that liver enzymes should be measured several days after the weekly dose of methotrexate so that a transient rise in liver enzymes will not be detected [38]. Unfortunately, the timing of liver enzyme measurement in relation to dosing is often not recorded either in clinical practise or in scientific papers. Various modalities of imaging the liver have been evaluated in the past. Ultrasound and magnetic resonance imaging are ineffective for detecting fibrosis. Therefore, liver biopsy is usually recommended as the gold standard for detecting methotrexate-induced hepatic fibrosis, however, it cannot be routinely performed in IBD patients treated with methotrexate. The MTX effects on liver histology upon chronic MTX administration are fatty infiltration, inflammation, cellular necrosis, and finally fibrosis. However, clinically, or even biochemically, these findings may be silent for years. A recent Cochrane review [39] suggested that 5 mg/week of folic acid could decrease gastrointestinal side effects by 80% without interfering with the efficacy of methotrexate. No significant benefit was seen with higher doses of folic acid. To not interfere with the intended methotrexate effect patients may take methotrexate on Monday and folic acid on Friday. One study examined longitudinal liver MTX and metabolite concentrations and attempted to correlate those with liver histology, liver function test abnormalities, measures of disease activity, and concomitant medications [40]. While relatively frequent transient liver test abnormalities were found, no mean changes in liver function tests no changes in liver histology were seen and no progression to cirrhosis was observed over three years. However, the progression of liver disease was associated with the cumulative dose of MTX. Additional alcohol consumption may aggravate hepatotoxicity of MTX. Cyclosporine and tacrolimus Approximately 15% of patients with ulcerative colitis experience one ore more severe attacks of their disease requiring hospitalization [41,42]. According to existing guidelines these patients are treated with intravenous GCs, with a response rate of around 60% [43,44]. Cyclosporine and tacrolimus offer an alternative to colectomy for these patients [45,46]. Intravenous cyclosporine has been shown to induce remission in 50 80% of patients who fail GCs treatment. The long-term response rates are 40 60%. This means that at least in half of the patients that otherwise would have to undergo colectomy surgery can be avoided. Toxicity occurs frequently in patients treated with high dose calcineurin inhibitors. The principal adverse reactions of cyclosporine therapy are renal dysfunction, tremor, hirsutism, hypertension and gum hyperplasia [43]. Hypomagnesemia has been reported in some patients exhibiting convulsions while on cyclosporine therapy. Besides those adverse effects, that frequently limit the therapeutic use of cyclosporine, a number of gastrointestinal side effects occur with less frequency (Table 1) [43]. Most data on side effects have been obtained in studies on kidney or liver transplantation. Diarrhea was reported in the cyclosporine treatment groups of several studies in a frequency of 1% 8%. Nausea and vomiting were reported in 1% 10%, hepatotoxicity in 1% 4%. Rare gastrointestinal adverse events are gastritis and peptic ulcers (Tables 1 and 2). Tacrolimus has been established as a potential alternative to cyclosporine in patients with severe UC [47 50]. The principal adverse events of tacrolimus are tremor in 25 40% of patients, headache in up to 50% and hypertension [51 54]. But also diarrhoea (27 47%) and nausea (27 46%) are frequently reported in studies on kidney and liver transplantation. In contrast approximately 25% of tacrolimus treated patients report about constipation. Diarrhoea was sometimes associated in these studies with other gastrointestinal complaints such as nausea and vomiting. These side effects occur with both oral and i.v. administration of tacrolimus and may respond to a reduction in dosing.

8 164 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) Disclosures Gerhard Rogler has received research support from Abbott, Ardeypharm, Essex, Falk, Novartis and UCB. He is participating in advisory boards for Abbott, Essex, Novartis and UCB. Conflict of interest statement None References [1] Schafer-Korting M, Kleuser B, Ahmed M, et al. Glucocorticoids for human skin: new aspects of the mechanism of action. Skin Pharmacol Physiol 2005;18: [2] Ross AS, Cohen RD. Medical therapy for ulcerative colitis: the state of the art and beyond. Curr Gastroenterol Rep 2004;6: [3] Gold R, Buttgereit F, Toyka KV. Mechanism of action of glucocorticosteroid hormones: possible implications for therapy of neuroimmunological disorders. J Neuroimmunol 2001;117:1 8. [4] Scribano M, Prantera C. Review article: medical treatment of moderate to severe Crohn s disease. Aliment Pharmacol Ther 2003;17(Suppl. 2): [5] Truelove SC, Witts LJ. Cortisone and corticotrophin in ulcerative colitis. Br Med J 1959;1: [6] Jones FA. Medical treatment of Crohn s disease of the colon. Bibl Gastroenterol 1970: [7] Lennard-Jones JE. Medical aspects of Crohn s disease. Proc R Soc Med 1968;61:81 3. [8] Jones JH, Lennard-Jones JE. Corticosteroids and corticotrophin in the treatment of Crohn s disease. Gut 1966;7: [9] Jewell DP. Corticosteroids for the management of ulcerative colitis and Crohn s disease. Gastroenterol Clin North Am 1989; 18: [10] Malchow H, Ewe K, Brandes JW, et al. European Cooperative Crohn s Disease Study (ECCDS): results of drug treatment. Gastroenterology 1984;86: [11] Brattsand R, Linden M. Cytokine modulation by glucocorticoids: mechanisms and actions in cellular studies. Aliment Pharmacol Ther 1996;10(Suppl. 2): discussion [12] Fiocchi C. Inflammatory bowel disease. Current concepts of pathogenesis and implications for therapy. Minerva Gastroenterol Dietol 2002;48: [13] de Haij S, Daha MR, van Kooten C. Mechanism of steroid action in renal epithelial cells. Kidney Int 2004;65: [14] Fiocchi C. Inflammatory bowel disease: dogmas and heresies. Dig Liver Dis 2002;34: [15] Carson JL, Strom BL, Schinnar R, et al. The low risk of upper gastrointestinal bleeding in patients dispensed corticosteroids. Am J Med 1991;91: [16] Piper JM, Ray WA, Daugherty JR, et al. Corticosteroid use and peptic ulcer disease: role of nonsteroidal anti-inflammatory drugs. Ann Intern Med 1991;114: [17] Wolfe F, Hawley DJ. The comparative risk and predictors of adverse gastrointestinal events in rheumatoid arthritis and osteoarthritis: a prospective 13 year study of 2131 patients. J Rheumatol 2000;27: [18] Di Fazano CS, Messica O, Quennesson S, et al. Two new cases of glucocorticoid-induced pancreatitis. Rev Rhum Engl Ed 1999;66:235. [19] Sandborn WJ. Azathioprine: state of the art in inflammatory bowel disease. Scand J Gastroenterol Suppl 1998;225: [20] Lees CW, Maan AK, Hansoti B, et al. Tolerability and safety of mercaptopurine in azathioprine-intolerant patients with inflammatory bowel disease. Aliment Pharmacol Ther 2008;27: [21] de Boer NK, Mulder CJ, van Bodegraven AA. Myelotoxicity and hepatotoxicity during azathioprine therapy. Neth J Med 2005;63: [22] Dubinsky MC, Lamothe S, Yang HY, et al. Pharmacogenomics and metabolite measurement for 6-mercaptopurine therapy in inflammatory bowel disease. Gastroenterology 2000;118: [23] Fraser AG, Orchard TR, Jewell DP. The efficacy of azathioprine for the treatment of inflammatory bowel disease: a 30 year review. Gut 2002;50: [24] Schwab M, Schaffeler E, Marx C, et al. Azathioprine therapy and adverse drug reactions in patients with inflammatory bowel disease: impact of thiopurine S-methyltransferase polymorphism. Pharmacogenetics 2002;12: [25] Reshamwala PA, Kleiner DE, Heller T. Nodular regenerative hyperplasia: not all nodules are created equal. Hepatology 2006;44:7 14. [26] Dubinsky MC, Vasiliauskas EA, Singh H, et al. 6-thioguanine can cause serious liver injury in inflammatory bowel disease patients. Gastroenterology 2003;125: [27] Vernier-Massouille G, Cosnes J, Lemann M, et al. Nodular regenerative hyperplasia in patients with inflammatory bowel disease treated with azathioprine. Gut 2007;56: [28] Geller SA, Dubinsky MC, Poordad FF, et al. Early hepatic nodular hyperplasia and submicroscopic fibrosis associated with 6-thioguanine therapy in inflammatory bowel disease. Am J Surg Pathol 2004;28: [29] Seiderer J, Zech CJ, Reinisch W, et al. A multicenter assessment of liver toxicity by MRI and biopsy in IBD patients on 6- thioguanine. J Hepatol 2005;43: [30] de Boer NK, van Bodegraven AA, Jharap B, et al. Drug insight: pharmacology and toxicity of thiopurine therapy in patients with IBD. Nat Clin Pract Gastroenterol Hepatol 2007;4: [31] Derijks LJ, Gilissen LP, de Boer NK, et al. 6-Thioguanine-related hepatotoxicity in patients with inflammatory bowel disease: dose or level dependent? J Hepatol 2006;44:821 2.

9 G. Rogler / Best Practice & Research Clinical Gastroenterology 24 (2010) [32] Gilissen LP, Derijks LJ, Driessen A, et al. Toxicity of 6-thioguanine: no hepatotoxicity in a series of IBD patients treated with long-term, low dose 6-thioguanine. Some evidence for dose or metabolite level dependent effects? Dig Liver Dis 2007;39: [33] Feagan BG, Alfadhli A. Methotrexate in inflammatory bowel disease. Gastroenterol Clin North Am 2004;33: [34] Feagan BG, Rochon J, Fedorak RN, et al. Methotrexate for the treatment of Crohn s disease. The North American Crohn s Study Group Investigators. N Engl J Med 1995;332: [35] Themido R, Loureiro M, Pecegueiro M, et al. Methotrexate hepatotoxicity in psoriatic patients submitted to long-term therapy. Acta Derm Venereol 1992;72: [36] Boffa MJ, Chalmers RJ, Haboubi NY, et al. Sequential liver biopsies during long-term methotrexate treatment for psoriasis: a reappraisal. Br J Dermatol 1995;133: [37] Whiting-O Keefe QE, Fye KH, Sack KD. Methotrexate and histologic hepatic abnormalities: a meta-analysis. Am J Med 1991;90: [38] Roenigk Jr HH, Auerbach R, Maibach H, et al. Methotrexate in psoriasis: consensus conference. J Am Acad Dermatol 1998; 38: [39] Ortiz Z, Shea B, Suarez Almazor M, et al. Folic acid and folinic acid for reducing side effects in patients receiving methotrexate for rheumatoid arthritis. Cochrane Database Syst Rev 2000:CD [40] Fathi NH, Mitros F, Hoffman J, et al. Longitudinal measurement of methotrexate liver concentrations does not correlate with liver damage, clinical efficacy, or toxicity during a 3.5 year double blind study in rheumatoid arthritis. J Rheumatol 2002;29: [41] Schwartz M, Cohen R. Optimizing conventional therapy for inflammatory bowel disease. Curr Gastroenterol Rep 2008;10: [42] Van Assche G, Vermeire S, Rutgeerts P. Treatment of severe steroid refractory ulcerative colitis. World J Gastroenterol 2008;14: [43] Garcia-Lopez S, Gomollon-Garcia F, Perez-Gisbert J. Cyclosporine in the treatment of severe attack of ulcerative colitis: a systematic review. Gastroenterol Hepatol 2005;28: [44] Shibolet O, Regushevskaya E, Brezis M, et al. Cyclosporine A for induction of remission in severe ulcerative colitis. Cochrane Database Syst Rev 2005:CD [45] Hare NC, Arnott ID, Satsangi J. Therapeutic options in acute severe ulcerative colitis. Expert Rev Gastroenterol Hepatol 2008;2: [46] Baumgart DC, Macdonald JK, Feagan B. Tacrolimus (FK506) for induction of remission in refractory ulcerative colitis. Cochrane Database Syst Rev 2008:CD [47] Yamamoto S, Nakase H, Mikami S, et al. Long-term effect of tacrolimus therapy in patients with refractory ulcerative colitis. Aliment Pharmacol Ther 2008;28: [48] Benson A, Barrett T, Sparberg M, et al. Efficacy and safety of tacrolimus in refractory ulcerative colitis and Crohn s disease: a single-center experience. Inflamm Bowel Dis 2008;14:7 12. [49] Ullman TA. Tacrolimus for active ulcerative colitis? Yes! (Even though Cochrane says "no"). Gastroenterology 2007;132: [50] Ogata H, Matsui T, Nakamura M, et al. A randomised dose finding study of oral tacrolimus (FK506) therapy in refractory ulcerative colitis. Gut 2006;55: [51] Klintmalm GB. Clinical use of FK 506 in liver transplantation. Transplant Proc 1996;28: [52] Keogh A. Calcineurin inhibitors in heart transplantation. J Heart Lung Transplant 2004;23:S [53] Chow DK, Leong RW. The use of tacrolimus in the treatment of inflammatory bowel disease. Expert Opin Drug Saf 2007;6: [54] Baumgart DC, Pintoffl JP, Sturm A, et al. Tacrolimus is safe and effective in patients with severe steroid-refractory or steroid-dependent inflammatory bowel disease a long-term follow-up. Am J Gastroenterol 2006;101:

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