HMG Co-A reductase inhibitors, popularly known as CLINICAL LIVER, PANCREAS, AND BILIARY TRACT
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1 GASTROENTEROLOGY 2004;126: CLINICAL LIVER, PANCREAS, AND BILIARY TRACT Patients With Elevated Liver Enzymes Are Not at Higher Risk for Statin Hepatotoxicity NAGA CHALASANI,* HISHAM ALJADHEY, JOE KESTERSON, MICHAEL D. MURRAY,, and STEPHEN D. HALL* *Department of Medicine, Indiana University School of Medicine, Indianapolis; Regenstrief Institute for Health Care, Indianapolis; and Purdue University School of Pharmacy, West Lafayette, Indiana See editorial on page Background & Aims: Studies that evaluate the risk of hepatotoxicity from statins in hyperlipidemic subjects with elevated baseline serum transaminases are lacking. We conducted a study to test the hypothesis that patients with elevated baseline liver enzymes have higher risk of statin hepatotoxicity. Methods: Our study consisted of the following 3 cohorts of patients seen between January 1, 1998 and June 31, 2002: Cohort 1: 342 hyperlipidemic patients with elevated baseline enzymes (AST >40 IU/L or ALT >35 IU/L) who were prescribed a statin; cohort 2: 1437 hyperlipidemic patients with normal transaminases who were prescribed a statin; and cohort 3: 2245 patients with elevated liver enzymes but who were not prescribed a statin. The effect of statins on liver biochemistries was assessed over a 6-month period after statins were prescribed. Elevations in liver biochemistries during follow-up were categorized into mild-moderate or severe based on predefined criteria. Results: The incidence of mild-moderate elevations and severe elevations in liver biochemistries in cohort 1 were 4.7% and 0.6%, respectively. Compared with cohort 1, individuals in cohort 2 had lower incidence of mild-moderate elevations (1.9%, P 0.002) but not severe elevations (0.2%, P 0.2). However, between cohorts 1 and 3, there were no differences in the incidence of mild-moderate elevations (4.7% vs. 6.4%, respectively, P 0.2) or severe elevations (0.6% vs. 0.4%, respectively, P 0.6). Statin discontinuation during the follow-up was similar between cohorts 1 and 2 (11.1% vs. 10.7%, respectively, P 0.8). Conclusions: These data suggest that individuals with elevated baseline liver enzymes do not have higher risk for hepatotoxicity from statins. HMG Co-A reductase inhibitors, popularly known as statins, are the most potent lipid lowering agents and are among the most widely prescribed medications. 1 Statins are generally well tolerated but can occasionally lead to muscle and liver toxicity. Hepatotoxicity from statins is generally mild, leading to asymptomatic elevations in transaminases, but rare instances of marked liver injury have been reported in the literature. 2 9 Although it is unknown whether the risk of hepatotoxicity from statins is higher in patients with underlying liver disease, the third report of the National Cholesterol Education Program (NCEP) states that use of statin is contraindicated in patients with active liver disease. 10 Manufacturers recommend that serum liver enzymes should be checked prior to starting a statin and not to prescribe these drugs for patients with persistent elevated transaminases. 11 In clinical practice, gastroenterologists and hepatologists are often consulted to advise referring physicians about the safety of prescribing statins for hyperlipidemic individuals who are found to have elevated baseline serum transaminases. Previous studies have shown that low-dose cerivastatin or pravastatin can be used safely in liver transplant recipients, 12 and the pharmacokinetics of rosuvastatin are not significantly altered in individuals with compensated cirrhosis. 13 However, to our knowledge, there are no studies in the literature that systematically evaluated the effect of statin therapy on liver biochemistries in hyperlipidemic patients with elevated baseline serum transaminases as compared with those with normal baseline liver enzymes or liver disease controls who are not started on statins. We conducted the following study to address some of the uncertainties related to the use of statins in patients with elevated liver enzymes. The main objective of our study was to evaluate whether the individuals with ele- Abbreviations used in this paper: ALT, alanine aminotransferase; AST, aspartate aminotransferase by the American Gastroenterological Association /04/$30.00 doi: /j.gastro
2 1288 CHALASANI ET AL. GASTROENTEROLOGY Vol. 126, No. 5 vated baseline liver enzymes are at higher risk for hepatotoxicity from statins by comparing the course of their liver biochemistries over a 6-month period with individuals with normal baseline liver enzymes who were prescribed a statin and individuals with elevated baseline liver enzymes but who were not prescribed a statin. Two secondary objectives of this study were (1) to compare the frequency of statin discontinuation between individuals with elevated baseline liver enzymes and normal baseline liver enzymes within 6-months after prescribing statins and (2) to evaluate how often practicing physicians comply with the recommendation that liver biochemistries be checked prior to initiating statin therapy. Materials and Methods Patients The Institutional Review Board at Indiana University School of Medicine has approved and administered this study in concordance with the principles of the Declaration of Helsinki. Data were collected from a large academic medical practice located in Indianapolis, which uses the Regenstrief Medical Record System (RMRS). 14 This practice-based electronic record system captures patient information from 3 hospitals on the Indiana University Medical Center campus (Wishard Memorial Hospital, Indiana University Hospital, and Riley Hospital for Children) and from 30 clinics scattered around the inner city of Indianapolis. 14 It captures all diagnostic studies (labs, EKGs, radiology reports, surgical pathology, and others), discharge summaries, and all orders (including prescriptions) in a coded form. 14 This database links patient s prescriptions and their laboratory test results using a unique patient identifier. In so doing, the system can be programmed to identify every patient who develops elevations in liver enzymes after initiating therapy with specified medications. Using the RMRS, we identified 3 cohorts of patients who attended Wishard Memorial Hospital and affiliated primary care clinics between January 1, 1998 and June 31, Wishard Memorial Hospital is a 400-bed academic inner-city hospital located on the Indiana University Medical Center campus. Cohort 1 consisted of individuals with elevated baseline liver enzymes who were prescribed a statin between January 1, 1998 and June 31, 2002 and had serum alanine aminotransferase (ALT) and/or aspartate aminotransferase (AST) values within 6 months before and 6 months after starting the statin agent and absence of any evidence of alcohol abuse, hepatitis B surface antigen, or hepatitis C antibody. Cohort 2 consisted of individuals with normal liver enzymes who were prescribed a statin between January 1, 1998 and June 31, 2002 and had ALT and/or AST values within 6 months before and 6 months after starting the statin agent and absence of any evidence of alcohol abuse, hepatitis B surface antigen, or hepatitis C antibody. Cohort 3 consisted of individuals with elevated liver enzymes seen between January 1, 1998 and June 31, 2002 and who had follow-up ALT and/or AST values measured within the next 6 months and absence of any evidence of alcohol abuse, hepatitis B surface antigen, or hepatitis C antibody and who were not prescribed a statin. In addition, for confirmatory comparative purposes, 2 other control groups were constructed, and the details of these 2 confirmatory cohorts are described in the Results section. Patients with serum AST 40 IU/L or ALT 35 IU/L were considered to have elevated transaminases because the upper limit of normal (ULN) for AST and ALT for our laboratory were 40 IU/L and 35 IU/L, respectively. Absence of alcohol abuse was determined based on the clinic notes, discharge summaries, and other encounter transcripts. The elevations in liver biochemistries during the follow-up were defined and categorized depending on the patient s baseline levels of serum aminotransferases. For this study s purposes, mild-moderate elevations in liver biochemistries were defined as elevations of AST and/or ALT up to 10 times ULN in patients with normal baseline enzymes or up to 10-fold elevations from their baseline values of AST and/or ALT in patients with elevated liver enzymes at baseline. Severe elevations in liver biochemistries were defined as the development of serum bilirubin 3 mg/dl (regardless of their baseline transaminases) or elevations of AST and/or ALT greater than 10 times ULN in patients with normal baseline enzymes or 10-fold elevations from their baseline values of AST and/or ALT in patients with elevated liver enzymes at baseline. We used the RMRS prescription records to determine whether patients continued to take statins during the follow-up period (i.e., 6-month period immediately after starting the statins). Subjects were considered to have discontinued the use of statins if there was no evidence of a prescription refill after their supply of statins ran out and if there was no prescription for an alternate statin. It previously has been shown that most patients attending Wishard Memorial Hospital and the affiliated primary care clinics fill their medicine prescriptions exclusively at the Wishard Hospital pharmacies. 15 During the study period, atorvastatin, simvastatin, pravastatin, and fluvastatin were available at Wishard Hospital pharmacies. To examine how often practicing physicians within our health care system comply with the recommendation that baseline liver enzymes should be checked before starting statins, we examined the proportion of patients in whom AST or ALT levels were available within the prior 6-month period before starting statin therapy. Statistical Analyses Data validity procedures, database management, and statistical analyses were performed using SAS software. Basic descriptive statistics, including means, standard deviations (SD), ranges, and percentages, were used to characterize the study patients. 2 tests for categorical variables and Student t tests or Mann Whitney U tests for continuous variables were
3 May 2004 STATINS IN PEOPLE WITH ELEVATED LIVER ENZYMES 1289 Table 1. Demographic and Selected Characteristics of the Study Cohorts Cohort 1 (n 342) Cohort 2 (n 1437) Cohort 3 (n 2245) Age (yr) Females (%) Ethnicity (B/W) (%) 34/59 42/54 35/48 Weight (lb) AST at baseline (IU/L) ALT at baseline (IU/L) Cholesterol (mg/dl) LDL (mg/dl) HDL (mg/dl) Triglyceride (mg/dl) Serum creatinine (mg) Statin prescribed (%) Atorvastatin Simvastatin Fluvastatin 2 3 NOTE. Data presented as mean SD unless specified otherwise. Cohort 1: individuals with elevated baseline liver enzymes who were placed on a statin; cohort 2: individuals with normal baseline liver enzymes who were placed on a statin; cohort 3: individuals with elevated liver enzymes but not placed on a statin. made for univariate comparisons between the groups. The primary comparisons are between cohort 1 vs. cohort 2 and cohort 1 vs. cohort 3. A P value 0.05 was considered statistically significant. Results Cohort 1 contained 342 patients; cohort 2 contained 1437 patients; and cohort 3 contained 2245 patients. Demographics and selected characteristics of these 3 cohorts are shown in Table 1. Although there were some statistical differences in the demographics among the 3 groups, they did not appear to be clinically significant. Generally, all 3 cohorts consisted of a hyperlipidemic, middle-aged population with a female and white preponderance. Although the body weight, LDL, HDL, and creatinine were similar among the 3 groups, cohort 3 had significantly lower triglyceride and cholesterol levels. As expected, individuals in cohorts 1 and 3 had significantly higher AST and ALT values than those in cohort 2. The mean duration of statin exposure in patients belonging to cohorts 1 and 2 was similar ( and years, respectively, P 0.7). The course of transaminases during the 6-month follow-up period in patients belonging to all 3 cohorts is shown in Table 2. The incidence of mild-moderate elevations and severe elevations in liver biochemistries in cohort 1 was 4.7% and 0.6%, respectively. Compared with cohort 1, individuals in cohort 2 had lower incidence of mild-moderate elevations (1.9%, P 0.002) but not severe elevations (0.2%, P 0.2). However, between cohorts 1 and 3, there were no differences in the incidence of mild-moderate elevations (4.7% vs. 6.4%, respectively, P 0.2) or severe elevations in liver biochemistries (0.6% vs. 0.4%, respectively, P 0.6). For confirmatory purposes and to enhance the generalizability, we have compared the frequency of liver biochemistry abnormalities in cohort 1 to 2 additional control groups. One of them consisted of a subgroup of cohort 3 patients who were age and gender matched to cohort 1 (n 326). Their frequency of mild-moderate elevations (6.1%, P 0.4) or severe elevations (0.9%, P 0.6) was not significantly different than cohort 1 patients. The additional confirmatory cohort consisted of 1111 individuals with detectable hepatitis C antibody with a minimum of 2 or more AST or ALT values and elevated baseline AST or ALT but who were not placed on statins or interferon and were seen during the same period. Compared with cohort 1, individuals in this hepatitis C control group had a significantly higher frequency of mild-moderate (11.1%, P 0.001) or severe elevations in liver biochemistries (5.9%, P 0.001). The likelihood of discontinuing a statin in the 6-month follow-up period was not different between cohorts 1 and 2 (11.1% vs. 10.7%, respectively, P 0.8) (Table 3). The mean duration of exposure ( vs years, respectively, P 0.7) and the Table 2. Frequency of Varying Degrees of Elevations in Liver Biochemistries Over a 6-Month Period in 3 Study Cohorts Cohort 2 (n 1437) Cohort 1 (n 342) Cohort 3 (n 2245) Mild-moderate elevations in liver biochemistries a 1.9% 4.7% 6.4% P P 0.2 Severe elevations in liver biochemistries a 0.2% 0.6% 0.4% NOTE. Cohort 1: individuals with elevated baseline liver enzymes who were placed on a statin. Cohort 2: Individuals with normal baseline liver enzymes who were placed on a statin. Cohort 3: Individuals with elevated liver enzymes but not placed on a statin. a See Materials and Methods section for definitions. P 0.2 P 0.6
4 1290 CHALASANI ET AL. GASTROENTEROLOGY Vol. 126, No. 5 Table 3. Doses and Duration of Statin Therapy Between Cohorts 1 and 2 Cohort 1 (n 342) Cohort 2 (n 1437) P value Atorvastatin (mg/d) Mean dose Median dose Simvastatin (mg/d) Mean dose Median dose Fluvastatin (mg/d) Mean dose Median dose Duration of therapy (yr) Statin discontinuation during follow-up 11.1% 10.7% 0.8 median duration of exposure to statins (0.5 years vs. 0.5 years, respectively) was not different between cohorts 1 and 2. Similarly, the frequency of liver biochemistry monitoring during statin therapy between these 2 cohorts was similar ( vs , respectively, P 0.7) (Table 3). During the study period, atorvastatin (46%) and simvastatin (51%) were the 2 most commonly prescribed statins, and fluvastatin or pravastatin were prescribed for the remaining 3% of the patients (Tables 3 and 4). The median doses of different statins prescribed during the study period are shown in Table 3. Fifty-seven percent of the cohort received the median doses of statin, whereas 17% received the doses that were greater than the median doses. The mean and median doses of various statins were similar between patients belonging to cohorts 1 and 2 (Table 4). We failed to detect any association between the statin used and the proportion of patients developing elevations in liver enzymes or mean change in AST or ALT values or the proportion discontinuing the statin during the follow-up period (Table 4). Furthermore, there was no statistical difference in the incidence of liver enzyme elevations among the patients who received the median dose of the statins and those who received more than the median dose. The incidence of mild-moderate elevations in liver biochemistries in patients prescribed median doses of statins and those prescribed higher doses were 2.5% and 2.9%, respectively (P 0.6). Similarly, the incidence of severe elevations in liver biochemistries in patients on median doses or higher doses of statins was 0.3% and 0.3%, respectively (P 0.9). To determine how often practicing physicians comply with the recommendation that baseline liver enzymes should be checked before starting statins, we have examined the proportion of patients in whom AST or ALT levels were available within the prior 6-month period before starting a statin agent. The proportion of patients in whom transaminase levels were available within 6 months prior to starting a statin were 58% in year 1998, 57% in year 1999, 58% in year 2000, 66% in year 2001, and 63% in year There were no demographic differences between the patients with and without baseline transaminases available prior to starting statins. Interestingly, the proportion of patients who exhibited a serum bilirubin 3 mg/dl during the follow-up period or the proportion of patients who discontinued statins during the follow-up period was similar between patients with and without baseline liver enzymes available prior to starting statins. Furthermore, in comparing the patients who received statins with those who did not, there was not a significant difference in the follow-up levels of AST (P 0.4) or ALT (P 0.8). Discussion To our knowledge, this is the first study to specifically address the question of whether patients with elevated baseline liver enzymes are at higher risk to develop hepatotoxicity from statins. In this study, we have addressed this question by comparing the changes Table 4. Change in Transaminases Within 6 Months After Starting a Statin Stratified by Type of Statin Prescribed Atorvastatin (n 819) Simvastatin (n 904) Other statins a (n 56) P value Median dose per day 10 mg 20 mg 20 mg Mean dose per day Baseline AST (IU/L) Baseline ALT (IU/L) Proportion with elevated AST and/or ALT at baseline 18% 21% 13% 0.2 Incidence of liver biochemistries elevations b 2% 3.1% 4.3% 0.4 Change in AST (IU/L) Change in ALT (IU/L) Proportion that discontinued statin during follow-up (%) 10% 11.5% 8.5% 0.5 NOTE. Table represents cohorts 1 and 2 combined. a Other statins include fluvastatin in 49 patients and pravastatin in 7 patients. b This represents the combination of mild-moderate and severe elevations in liver biochemistries.
5 May 2004 STATINS IN PEOPLE WITH ELEVATED LIVER ENZYMES 1291 in liver biochemistries of individuals with elevated liver enzymes and who were prescribed statins to controls. We found that patients with elevated baseline liver enzymes had higher incidence of mild-moderate but not severe elevations in liver biochemistries than those with normal baseline liver enzymes who were prescribed statins. However, the frequency of mild-moderate or severe elevations in patients with elevated liver enzymes who were prescribed statins was not significantly higher than that of the patients with elevated liver enzymes who were not prescribed a statin. These data show that some individuals with elevated liver enzymes have elevations in their liver biochemistries, regardless of whether or not statins were prescribed (possibly because of the activity of underlying liver disease or because of unknown coexisting pathology). This suggests that individuals with elevated liver enzymes do not have increased susceptibility to hepatotoxicity from statins. We failed to find a relationship between the type of statin used and the frequency of elevations in liver biochemistries among those who were placed on statin therapy. In more than one third of the patients who were initiated on statins, the baseline transaminases were not checked prior to starting statins, and the risk of hepatotoxicity in this group did not appear to be different from those who had their transaminases checked prior to starting statins. Although this observation questions the utility of checking baseline liver enzymes prior to starting statins, it is not sufficient to suggest a change in this recommendation. As long as the recommendation is to periodically monitor transaminases after statins are started, it is then essential to have baseline liver enzymes available for comparative purposes. Because this is a retrospective study of an electronic medical record system, it carries several limitations that require further discussion. First, our definition of statin discontinuation is based on the prescription records rather than actual documentation that a prescribing physician or a patient has discontinued statin therapy because of side effects. In general, a majority of the patients attending our facilities use our outpatient and inpatient pharmacies exclusively and are not likely to take prescription medications obtained from outside pharmacies. Second, our study examined the course of serum transaminases within 6 months after starting statins and therefore may not shed light on what happens to liver enzymes after the 6-month period. However, hepatotoxicity from statins appears to be an early event rather than late phenomenon. 10 Finally, because Wishard Hospital has a formulary, we were restricted to study only those statins approved by the Pharmacy and Therapeutic Committee and were commonly prescribed by the practicing physicians. Despite all these limitations, we believe that our study provides valuable information that is clinically pertinent and provides guidance to clinicians and the policy makers. The regulatory authorities are currently considering whether to make some statins available without a prescription to target patient populations in the United States (lovastatin) and the United Kingdom (simvastatin), 16,17 and our data may assist rational decision making for this important public health issue. In summary, mild-moderate or severe elevations in patients with elevated baseline liver enzymes who were placed on a statin are not significantly higher than those with elevated liver enzymes who were not placed on statin therapy. This shows that some individuals with elevated liver enzymes will have varying degrees of elevations in their liver biochemistries during the follow-up period, regardless of whether or not they were placed on statins. These data suggest that individuals with elevated liver enzymes do not have increased susceptibility to hepatotoxicity from statins. References 1. Kreisberg RA, Oberman A. Medical management of hyperlipidemia/ dyslipidemia. J Clin Endocrinol Metab 2003;88: Bolego C, Baetta R, Bellosta S, Corsini A, Paoletti R. Safety considerations for statins. Curr Opin Lipidol 2002;13: Chitturi S, George J. Hepatotoxicity of commonly used drugs: nonsteroidal anti-inflammatory drugs, antihypertensives, antidiabetic agents, anticonvulsants, lipid-lowering agents, psychotropic drugs. Semin Liver Dis 2002;22: Kinnman N, Hultcrantz R. Lipid lowering medication and hepatotoxicity. J Intern Med 2001;250: Nakad A, Bataille L, Hamoir V, Sempoux C, Horsmans Y. Atorvastatin-induced acute hepatitis with absence of cross-sensitivity with simvastatin. Lancet 1999;353: England JD, Viles A, Labib S. Liver side effects associated with simvastatin therapy. Aust Med J 1991;155: Grimbert S, Pessayre D, Degott C, Benhamou JP. Acute hepatitis induced by HMG-CoA reductase inhibitor, lovastatin. Dig Dis Sci 1994;39: Hartleb M, Rymarczyk G, Januszewski K. Acute cholestatic hepatitis associated with pravastatin. Am J Gastroenterol 1999;94: Raveh D, Arnon R, Israeli A, Eisenberg S. Lovastatin induced hepatitis. Isr J Med Sci 1992;28: National Cholesterol Education Program. Third report of the expert panel on detection, evaluation, and treatment of high cholesterol in adults (Adult Treatment Panel III). Website: Accessed July 10, Physician Desk Reference (PDR), 57th edition, Zachoval R, Gerbes AL, Schwandt O, Parhofer KG. Short-term effects of statin therapy in patients with hyperlipoproteinemia after liver transplantation: results of a randomized cross-over trial. J Hepatol 2001;35: Simonson SG, Martin PD, Mitchell P, Schneck DW, Lasseter KC, Warwick MJ. Pharmacokinetics and pharmacodynamics of rosuvastatin in subjects with hepatic impairment. Eur J Clin Pharmacol 2003;58:
6 1292 CHALASANI ET AL. GASTROENTEROLOGY Vol. 126, No McDonald CJ, Overhage JM, Tierney WM, Dexter PR, Martin DK, Suico JG, Zafar A, Schadow G, Blevins L, Glazener T, Meeks- Johnson J, Lemmon L, Warvel J, Porterfield B, Warvel J, Cassidy P, Lindbergh D, Belsito A, Tucker M, Williams B, Wodniak C. The Regenstrief Medical Record System: a quarter century experience. Int J Med Inform 1999;54: Murray MD, Loos B, Tu W, Eckert GJ, Zhou XH, Tierney WM. Work patterns of ambulatory care pharmacists with access to electronic guideline-based treatment suggestions. Am J Health Syst Pharm 1999;56: Accessed December 23, Anonymous. Statin set to become next big POM-to-P switch: is this good news for patients? Pharm J 2003:271:705. Received August 28, Accepted February 5, Address requests for reprints to: Naga Chalasani, M.D., Indiana University School of Medicine, WD OPW 2005, 1001 West 10th Street, Indianapolis, Indiana nchalasa@iupui.edu; fax: (317) Supported in part by FDA (FD-T to S.D.H.) and NIH grants (UO-1 DK to N.C.).
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