Childhood initiated statin therapy in familial hypercholesterolemia Avis, H.J.
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1 UvA-DARE (Digital Academic Repository) Childhood initiated statin therapy in familial hypercholesterolemia Avis, H.J. Link to publication Citation for published version (APA): Avis, H. J. (2013). Childhood initiated statin therapy in familial hypercholesterolemia. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam ( Download date: 12 Apr 2019
2 Chapter 9 EARLY INITIATION OF STATIN THERAPY AND THE NATURAL HISTORY OF FAMILIAL HYPERCHOLESTEROLEMIA: A TEN YEAR FOLLOW-UP STUDY Meeike (D.M.) Kusters, Hans J. Avis, Maud N. Vissers, Marjet (J.A.M.) Braamskamp, Eric de Groot, Frits Wijburg, John J.P. Kastelein, Albert Wiegman* and Barbara A. Hutten*. * Both authors contributed equally Manuscript in preparation
3 Abstract Background: Familial Hypercholesterolemia (FH) is a prevalent disorder of metabolism resulting in high cholesterol levels and premature cardiovascular events. To halt enhanced atherosclerosis progression in FH, treatment guidelines advocate initiation of statin therapy during childhood already. The short-term efficacy and safety of statin therapy in children is well established, but long-term follow-up studies do not exist. Therefore, we performed a 10-year follow-up of statin therapy in children with FH. Methods & Results: All 214 FH children, who were randomized between 1997 and 1999 (age 8-18 years) into a placebo-controlled trial evaluating the 2-year efficacy and safety of pravastatin, were eligible. After the study, all children were continued on statins and were followed for 10 years, together with their 95 unaffected siblings as a control group. Follow-up was successful in 90% of subjects (age years). After ten years of statin treatment LDL-C levels were higher in FH subjects (mean (±SD) 173 ± 66 versus 124 ±32 mg/dl; P<0.001) than in siblings. Although c-imt was significantly greater in FH patients (mean 0.48 ± versus 0.47 ± mm; P=0.015) than in siblings, mean IMT progression was similar in both groups (0.039 ± versus ± mm; P=0.52). No differences were observed in length, BMI, blood pressure, muscle- or liver enzymes, menarche or education. Major adverse events were not reported. Conclusion: Long-term statin treatment initiated in childhood is safe and normalizes c-imt progression in FH patients. Furthermore, our findings suggest that more robust lipid-lowering therapy or even earlier initiation may be required to restore arterial wall morphology to non-fh values in order to avert cardiovascular events in this very high-risk population. 140
4 Childhood initiated statin therapy in FH: ten years of follow-up Introduction Familial hypercholesterolemia (FH) is the most common dominantly inherited metabolic disorder. 1 Individuals heterozygous for FH have severely elevated low-density lipoprotein cholesterol (LDL-C) levels and suffer premature atherosclerotic consequences. Untreated, cardiovascular events occur in 85% of males and 58% of females before the age of Cardiovascular disease in the first two decades of life in FH is rare, but enhanced atherosclerosis progression is already prominent in childhood. 3 Before, FH was estimated to affect approximately 1 in 500 individuals 1, but recent studies report a prevalence of up to 1 per This implicates over 1.5 million patients in the USA alone. Thus, both the prevalence and natural history of untreated FH constitute a significant public health issue. Statin treatment for the prevention of cardiovascular events is supported by robust evidence in a wide range of patients. 5 Indeed, although not randomized and controlled, retrospective cohort studies in adult FH also suggest an impressive reduction in cardiovascular events after statin initiation 6,7,8. In children with FH, a two year randomized, placebo-controlled trial revealed regression of carotid intima media thickness (c-imt) upon statin treatment. 9 Since then, several trials in FH children have confirmed the short-term efficacy and safety of statin therapy Partly based on our observations, the NHLBI guidelines advocate initiation of statins from as young as 8 years onwards in FH. 11 However, long-term follow-up of statin therapy, initiated in childhood, does not exist. Therefore, we decided to follow-up the children from our first randomized controlled trial together with their age-matched unaffected siblings all the way into adulthood. Here we show the efficacy and safety of more than ten years of statin therapy initiated in children, who now all have reached adult life. Materials and Methods Study population and design The study cohort comprised all 214 children who were randomized between 1997 and 1999 into a single-center double-blind and placebo-controlled trial, evaluating the efficacy and safety of pravastatin. This trial has been described elsewhere. 9 Briefly, children were enrolled when they met the following criteria: one parent with a definite clinical or molecular diagnosis of familial hypercholesterolemia; age between 8 and
5 years; at least 3 months on a fat-restricted diet; 2 fasting samples with plasma LDL-C levels 4.0 mmol/l and triglyceride levels <4.0 mmol/l; adequate contraception in sexually active girls; and no drug treatment for familial hypercholesterolemia or use of plant sterols. Reasons for exclusion were homozygous familial hypercholesterolemia, hypothyroidism, and abnormal levels of muscle or liver enzymes. Children were randomly assigned to receive either pravastatin or placebo for two years. After the end of the placebo-controlled trial, pravastatin was given to all participants (<14 years: 20 mg, 14 years: 40 mg). Patients were subsequently followed at our outpatient clinic until referral to an adult lipid-clinic or general practitioner for further follow-up. Although not described in the trial, 95 unaffected siblings were enrolled at baseline as a control group, for measurement of lipid profile, safety parameters, and carotid IMT. 3 These subjects were also eligible for our current study. Ten years after the trial was initiated, the research physician contacted all eligible subjects, and those who agreed to participate were invited for a single visit at our clinic. Before this visit we sent a questionnaire including items about current- and past statin use, medical history, family history and possible side-effects. The questionnaire was discussed during the visit and subjects were physically examined, a fasted blood sample was taken and c-imt was measured. The protocol of the study was approved by the Institutional Review Board and all subjects gave written informed consent. The primary efficacy outcome was c-imt at the end of follow-up. Secondary outcomes were levels of LDL cholesterol, total cholesterol, HDL cholesterol, triglycerides, apolipoprotein A-I and apolipoprotein B. Safety assessment included growth, maturation, reported level of education, reported adverse events and laboratory tests, including liver-function tests, CK-levels, egfr, fasting glucose levels, CRP and hormone levels (TSH, ACTH, DHEAS, LH, FSH testosterone, oestradiol). Carotid IMT Carotid ultrasound measurements of intima-media thickness were performed according to a standardized and validated methodology as described in detail before. 12 Ultrasound measurements of all participants were made by a single experienced sonographer who also made all the measurements for the RCT as well as the control group. 3,9 For the current study, the Acuson Sequoia 512 instrument (Siemens AG, Malvern, Pa, and Erlangen, Germany) equipped with an 85 MHz linear array transducer was used. Still images were saved as DICOM files. One certified image analyst analyzed these images off line. In order to minimize intra-observer variation, the same image analyst re-analyzed the baseline images. The sonographer and the image analyst were blinded for all demographic and 142
6 Childhood initiated statin therapy in FH: ten years of follow-up clinical information of the participants. Mean carotid IMT was defined as the mean IMT of the right and left common carotid, the carotid bulb, and the internal carotid far wall segments. Statistical analysis Differences in demographic and clinical characteristics at baseline and after ten years of follow-up between patients with FH and their unaffected siblings were evaluated using linear or logistic regression analysis. To compare carotid IMT and the mean change in carotid IMT after ten years between FH patients and unaffected siblings, we used a linear regression model. We adjusted for potential confounders by means of stepwise backward elimination. All these analyses were performed using the generalized estimating equation method to account for correlations within families. The exchangeable correlation structure was used for these models. In the group of FH patients we explored the univariate association between the mean carotid IMT after ten years and the following variables: sex, age at statin initiation, carotid IMT at statin initiation, current statin use, duration of statin treatment, body mass index, systolic blood pressure, LDL-C reduction and smoking. Using multivariate analysis, we identified independent predictors after stepwise backward selection. Variables with a skewed distribution were log transformed before analysis. Statistical analyses were performed with SPSS 11.5 for Windows (SPSS Inc, Chicago, Ill) software. 9 Results Description of cohort From the original cohort of 214 children with FH, 20 children could not be enrolled in the present study. One adolescent had died after a traffic accident, 5 lived abroad and 14 declined participation. Of the 95 healthy siblings, 12 declined participation. Thus, in total 90% of the original cohort was included in the present safety and efficacy analysis (Figure 1). General characteristics and lipid profiles at baseline of the trial and after ten years of follow-up are shown in Table 1. Mean age at follow-up was 24.0 ± 3.2 years in FH patients and 23.8 ± 3.1 years in siblings. Duration of follow-up was on average 11.0 years (range years). Of the subjects with FH, 159 (86%) were still using a statin, of which 31% pravastatin, 15% simvastatin, 27% atorvastatin and 27% rosuvastatin. Ezetimibe as add-on therapy was used by 56 subjects (35% of the statin users), and colesevelam by 2 subjects. Self-reported adherence was 79%. Mean LDL-C 143
7 level at follow-up was ± 66.0 mg/dl in FH patients, and ± 32.0 mg/dl in siblings (P<0.001). LDL-C decreased with 27% from baseline in FH patients, while in siblings a LDL-C increase of 24% was seen (P<0.001). Of the FH patients, 59 (30%) had a first degree relative who experienced a premature cardiovascular event. Figure 1. Study flow-chart. Efficacy None of the FH patients or siblings had cardiovascular complaints or suffered a cardiovascular event during follow-up, including those who could not be enrolled as they were contacted by phone or . In fact, 7 FH patients survived the age of the first cardiovascular event of one of their parents. At baseline of the original trial as well as after ten years of follow-up, FH subjects had a greater c-imt as compared to their healthy siblings (0.48 ± vs 0.47 ± , P = after ten years of follow-up, Figure 2), but the progression of c-imt over ten years was similar for FH subjects and healthy siblings (0.039 ± vs ± , P=0.52). The relationship between age and c-imt after ten years of treatment is shown in Figure 3. The results of univariate and multivariate analysis of the association 144
8 Childhood initiated statin therapy in FH: ten years of follow-up Table 1. Patient Characteristics at Baseline and after 10 years of Follow-up of Statin Therapy*. Characteristic At baseline After 10 years follow-up FH (n=194) Sibling (n=83) P Value FH (n=194) Sibling (n=83) P Value Age yr 12.9 ± ± ± ± Male sex no. (%) 90 (46.4) 46 (55.4) (46.4) 46 (55.4) 0.17 Height m 1.56 ± ± ± ± Weight kg 48.8 ± ± ± ± Body-mass index ± ± Blood pressure mm Hg Systolic ± ± ± ± Diastolic 61.5 ± ± ± ± Risk factors no.(%) Diabetes 0 (0) 0 (0) - 1 (0.5) 1 (1.2) 0.55 Hypertension 0 (0) 0 (0) - 7 (3.6) 5 (6.2) 0.36 Current smoking 22 (11) 6 (7) (27.3) 27 (32.5) Statin use no. (%) 0 (0) 0 (0) (86) 0 (0) <0.001 Cholesterol Total (mg/dl) ± ± 24.1 < ± 69.1 LDL (mg/dl) ± ± 22.1 < ± ± ± 32.0 <0.001 <0.001 HDL (mg/dl) 48.4 ± ± 14.0 < ± ± Triglycerides mg/dl Median Interquartile range Apolipoprotein B (mg/dl) ± ± 16.3 < ± ± 19.7 <0.001 A-1 (mg/dl) ± ± 21.0 < ± ± * Plus-minus values are means ± SD. Medians and interquartile ranges for variables that were not distributed normally were calculated with the use of the Wilcoxon rank-sum test. To convert the values for cholesterol to millimoles per liter, multiply by To convert the values for triglycerides to millimoles per liter, multiply by LDL denotes low-density lipoprotein and HDL high-density lipoprotein. The body-mass index is the weight in kilograms divided by the square of the height in meters. Lipoprotein values after 10 years follow-up were available for 185 subjects in the FH group and 83 in the siblings group. 145
9 between c-imt after ten years of follow up and clinical variables are shown in Table 2. The following independent predictors for c-imt after ten years of follow-up were identified: c-imt at statin initiation (β=0.500 ± 0.105, P<0.001), age at statin initiation (β=0.003 ± 0.001, P=0.04), male sex (β=0.021 ± 0.010, P=0.03), systolic blood pressure (β=0.001 ± 0.001, P=0.005) and current statin use (β= ± 0.012, P=0.01). Figure 2. Mean c-imt at baseline and after 10 years of follow-up of statin therapy in FH and untreated siblings. Safety Three FH patients discontinued statin therapy due to side effects. Other reported reasons to discontinue statin therapy were pregnancy / lactation, or unwillingness to take medication on daily basis. Rhadbomyolysis or other major adverse events were not reported. Other safety parameters are depicted in Table 3. There were two siblings with a higher than 10-fold elevation of CK levels, versus none in the FH group (P=0.03). egfr was higher in the FH group than in the siblings group (126.7 (IQR ) vs (IQR ), P=0.05). Figure 3. Relationship between age and c-imt at baseline and after 10 years of follow-up of statin therapy in FH and siblings. 146
10 Childhood initiated statin therapy in FH: ten years of follow-up Table 2. Predictors of c-imt after 10 Years of Follow-up of Statin Therapy. Univariate Multivariate Regression coefficient (SE) P Regression coefficient (SE) P Male sex (0.008) < (0.010) 0.03 Systolic blood pressure (0.000) < (0.000) Body-mass index (0.001) Age start statin (0.001) (0.001) 0.04 IMT at statin initiation (0.087) < (0.105) <0.001 Duration of follow-up (0.004) (0.479) LDL-C reduction -0,001 (0.002) 0.8 Current statin use (0.012) (0.012) Current smoking (0.007) Height, weight and body-mass index after ten years of follow-up were the same in the FH groups as compared with the siblings group (Table 1). Age at menarche was 13.1 ± 1.7 for the FH subjects versus 13.2 ± 2.3 for the siblings (P=0.72) and hormone levels showed no clinically relevant differences. Levels of education were similar; 17.1% of the subjects with FH had lower education, 39.2% middle level education and 43.6% higher education, versus respectively 16.0%, 40.7% and 43.2% in the siblings group (P=0.964). We perfomed separate safety analyses for those who were pre-pubertal (Tanner stage 1 or 2) at statin initiation, which showed similar results. 147
11 Table 3. Safety Parameters after 10 Years of Follow-up of Statin Therapy*. Variable FH (n=194) Sibling (n=83) P Value Aspartate aminotransferase IU/l Median Interquartile range > 3x ULN no. (%) 1 (0.5%) 1 (1.1%) 0.55 Alanine aminotransferase IU/l Median Interquartile range > 3x ULN no. (%) 1 (0.5%) 0 (0.0%) 0.51 Creatine kinase IU/l Median Interquartile range > 10x ULN no. (%) 0 (0.0%) 2 (2.1%) 0.03 egfr ml/min per 1.73m 2 Median Interquartile range C-reactive protein mg/l Median Interquartile range Glucose 86.7 ± ± * Medians and interquartile ranges for variables that were not distributed normally were calculated with the use of the Wilcoxon rank-sum test. Plus-minus values are means ± SD. To convert the values for glucose to millimoles per liter, multiply by Laboratory values were available for 185 subjects in the FH group and 83 in the siblings group. 148
12 Childhood initiated statin therapy in FH: ten years of follow-up Discussion In this prospective follow-up study we demonstrate that early initiation of statin therapy reduces c-imt progression in FH patients to a level similar to their unaffected siblings. Moreover, we confirmed our previous finding that the age of statin initiation is positively correlated with c-imt, which implicates that earlier statin initiation leads to smaller c-imt in later life. 13 Last, and perhaps most important, statin therapy was well tolerated without any untoward long-term safety effects during follow-up into adulthood such as disturbances in psychological wellbeing, maturation, growth, liver or muscle. Our results extend with previous uncontrolled observational data. The Simon Broome register, which included adult FH patients that were followed during a period that overlapped the introduction of statins in the nineties of the previous century, demonstrated a decline in the relative risk for coronary mortality from 1992 onwards. 6,7 In a Dutch cohort, a large risk reduction of coronary artery disease events was observed in FH patients on statin treatment also. 8 In homozygous patients, statin therapy was shown to be associated with a delay in the occurrence of major cardiovascular events and death as well. 14 Furthermore, a recent chart-review of 89 FH patients with severe hypercholesterolemia at baseline (mean LDL-C 250±49 mg/dl) in whom lipid-lowering treatment was initiated during childhood, did not reveal any cardiovascular events during a follow-up period of 13±8 years (range 1 to 38 years) The safety of statin therapy is supported by a large body of evidence in adult patients. 5 In children, randomized-controlled studies have established short-term safety, with maximum follow-up being limited to 2 years of treatment. 10 Our study does not only report the longest follow-up in statin treated children, but is also the first to include a control group of non-affected siblings. By including these siblings, genetic and environmental differences between the FH children and controls are kept to a minimum. The main difference will be the presence of FH, now treated with statins, that affect the principle disease pathway. The subjects studied were born in FH families with a severe phenotypic expression. This is illustrated by high LDL-C levels despite lifestyle-intervention and statin treatment, and the fact that 30% had a first-degree family member who suffered a cardiovascular event. Auspiciously, none of the patients in our cohort had such an event up until now. In fact, 7 of them have already survived the age at which their parent with FH had a first cardiovascular event. 149
13 Furthermore, this is the only long-term follow-up study of FH patients that evaluates c-imt progression as the primary outcome. The fact that statin therapy in our FH children reduces such c-imt progression down to a level observed in their siblings, is reassuring in terms of cardiovascular risk reduction. Nevertheless, absolute c-imt values in our patients have not reached normal levels, which leaves the option of more aggressive LDL-C lowering treatment to be tested in future trials. Some methodological aspects of our study merit discussion. First, the study is not randomized and the control group includes unaffected siblings instead of untreated FH patients, who ideally would have to be enrolled for comparison of treatment effects. However, a long-term randomized-controlled trial would be unethical, given the established efficacy of statin therapy in non-fh patients. 5 Since this is a prospective study, with a very high follow-up rate of 90%, and subjects who discontinued statin therapy during follow-up were included, selection- and inflation-of-effect bias associated with observational studies is probably small. Second, the primary outcome parameter, c-imt, is a surrogate for future cardiovascular events. Because such events are rare in FH patients in the age range of our cohort, we feel c-imt was the best surrogate outcome available. Finally, although the number of subjects included in our study is large for a paediatric statin trial, it is small in comparison to adult trials. We realize this study lacks statistical power to detect subtle differences in safety parameters with a large variation such as growth, maturation and educational achievements. Nevertheless, the study spans over 2000 treatment years and no untoward effects became obvious. Furthermore, the high LDL-C levels in our patients underline the need for more efficacious LDL-C lowering agents. In conclusion, our data show that early initiation of statin therapy changes the natural history of FH in subjects from severely affected families. Moreover, no adverse effects were observed in statin treated children during follow-up into adulthood. These results strongly support the current NHLBI treatment guidelines for FH
14 Childhood initiated statin therapy in FH: ten years of follow-up References 1. Marks D, Thorogood M, Neil HA, Humphries SE: A review on the diagnosis, natural history, and treatment of familial hypercholesterolaemia. Atherosclerosis 2003; 168(1): Slack J. Risks of ischaemic heart-disease in familial hyperlipoproteinaemic states. Lancet 1969; 2(7635): Wiegman A, de Groot E, Hutten BA et al: Arterial intima-media thickness in children heterozygous for familial hypercholesterolaemia. Lancet 2004; 363(9406): Benn M, Watts GF, Tybjaerg-Hansen A and Nordesgaard BD. Familial hypercholesterolemia in the Danish general population: prevalence, coronary artery disease, and cholesterol-lowering medication. J Clin Endocrinol Metab 2012; 7(11): Baigent C, Keech A, Kearney PM, Blackwell L, Buck G, Pollicino C, Kirby A, Sourjina T, Peto R, Collins R, Simes R: Efficacy and safety of cholesterol-lowering treatment: Prospective meta-analysis of data from 90,056 participants in 14 randomised trials of statins. Lancet 2005; 366(9493): Risk of fatal coronary heart disease in familial hypercholesterolemia. Scientific Steering Committee on behalf of the Simon Broome Register Group. BMJ 1991;303(6807): Mortality in treated heterozygous familial hypercholesterolemia: implications for clinical management. Scientific Steering Committee on behalf of the Simon Broome Register Group. Atherosclerosis 1999; 142(1): Versmissen J, Oostveer DM, Yazdanpanah M et al. Efficacy of statins in familial hypercholesterolemia: a long term cohort study. BMJ 2008; 337:a Wiegman A, Hutten BA, de Groot E, et al: Efficacy and safety of statin therapy in children with familial hypercholesterolemia: a randomized controlled trial. JAMA 2004; 292(3): Vuorio A, Kuoppala J, Kovanen PT et al. Statins for children with familial hypercholesterolemia. Cochrane Database Syst Rev Jul 7;(7):CD Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents; National Heart, Lung, and Blood Institute. Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: summary report. Pediatrics 2011; 128 (Suppl 5): S de Groot E, Hovingh GK, Wiegman A et al. Measurement of arterial wall thickness as a surrogate marker for atherosclerosis. Circulation 2004; 109: III33-III Rodenburg J, Vissers MN, Wiegman A et al: Statin treatment in children with familial hypercholesterolemia: The younger, the better. Circulation 2007; 116(6): Raal FJ, Pilcher GJ, Panz VR et al. Reduction in mortality in subjects with homozygous familial hypercholesterolemia associated with advances in lipid-lowering therapy. Circulation 2011; 124(20): Elis A, Zhou R, Stein EA. Treatment of familial hypercholesterolaemia in children and adolescents in the last three decades. Cardiol Young 2013; 10:
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