Article

Effects of Reconstituted High-density Lipoprotein Infusions on Coronary Atherosclerosis

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Atherosclerotic cardiovascular disease is the result of a continuous and deleterious interaction between components of the vascular wall and the circulating blood. Circulating lipids and lipoproteins play a significant role in the initiation of fatty streaks and the subsequent progression to complex and vulnerable atherosclerotic plaques. The important role that circulating lipids play in altering the risk for cardiovascular disease has resulted in the development of strategies for altering these blood components through dietary changes, behavioral modifications, and pharmacological interventions. A greater understanding of the molecular relationships between lipid components and atherosclerosis initiation and progression has led to the identification of many effective medications to treat or prevent heart disease. These lipid-altering interventional strategies have resulted in a demonstrable decrease in the burden of atherosclerosis in individual patients, a decrease in the risk for subsequent cardiovascular morbidity and mortality, and a subsequent decrease in the overall societal burden of cardiovascular disease worldwide.1,2

While these therapies have proved effective for millions of patients, atherosclerotic cardiovascular disease is still a major contributor to global disease and disability. In fact, cardiovascular disease remains the primary cause of morbidity and mortality in developed and developing nations.3 Furthermore, the incidence of atherosclerotic cardiovascular disease is expected to remain high due to the increased proportion of elderly in the population, the rise of contributing conditions such as diabetes and obesity, and the trend toward decreased physical activity and increased caloric intake so prevalent in our society.

Therefore, strategies to decrease further the progression and burden of atherosclerosis remain necessary. The effect of high-density lipoprotein (HDL) levels on atherosclerotic disease has been an intriguing area of scientific evaluation. There is a strong inverse relationship between HDL cholesterol and risk of coronary heart disease, as demonstrated in several epidemiological studies.4,5 As a result, strategies to develop pharmacological interventions that confer protective effects on the circulatory system are important and relevant, and are actively being pursued by the scientific community. Efforts to raise HDL cholesterol levels have included the administration of oral agents that modify the lipid metabolic pathway in a manner that sustains HDL increases over time.6 Other strategies include short-term infusions of reconstituted HDL (rHDL), which utilizes native HDL biological properties.

One small clinical pilot study, apoA-I Milano, which assessed the effects of short-term infusions of HDL containing a naturally occurring variant of the apolipoprotein A-I, recognized the potential of this strategy to induce regression of coronary atherosclerosis in patients following acute coronary syndromes.7

Recently, the results from a clinical trial assessing the effect of rHDL therapy (CSL-111/CSL Ltd) provided further support for the viability of HDL-infusion therapy.8 CSL-111 is reconstituted HDL consisting of apoA-I derived from human plasma and combined with soybean phosphatidylcholine. The resulting rHDL resembles native HDL both chemically and biologically. Based on prior observations of biological activity in several animal models and small clinical trials,9–11 a clinical trial was conducted to demonstrate whether rHDL would rapidly decrease atherosclerotic plaque burden following administration as a weekly infusion to patients with recent acute coronary syndromes. The study was designed to assess the safety of rHDL administered in this manner, to assess the efficacy of rHDL on coronary atherosclerosis as assessed by intravascular ultrasonography (IVUS) and quantitative coronary angiography (QCA), and to identify an appropriate dose range for further clinical evaluation.

At 17 Canadian study centers 183 total patients scheduled for a clinically indicated coronary angiographical procedure (with or without percutaneous intervention) were randomized to receive either weekly placebo (saline) or rHDL infusions for four consecutive treatments. Patients included men and women between the ages of 30 and 75 years with at least one narrowing of 20% or more on coronary angiography at baseline. Patients with greater than 50% stenosis in the left main coronary artery, renal insufficiency, liver disease, active cholecystitis or gallbladder symptoms, uncontrolled diabetes mellitus, class III or IV heart failure, known soybean allergy, history of alcohol or drug abuse, planned treatment with warfarin or heparin during the study infusion period, or previous or planned coronary bypass surgery were excluded from the study.

The study design was double-blind and placebo-controlled and included the evaluation of two doses of rHDL — 40mg/kg and 80mg/kg. Prior to the first infusion of treatment, baseline IVUS examinations of a designated target coronary artery were performed and submitted to the IVUS core laboratory (Montréal Heart Institute) for verification and quality assessment.

Following rHDL administration as four weekly infusions, follow-up coronary IVUS was performed in the same segment of the target artery studied at baseline. QCA was also performed in all patients at baseline and follow-up in order to obtain an assessment of the entire coronary tree. Patients were monitored for safety with a particular emphasis on indices of liver toxicity. An independent unblinded safety review committee evaluated the data while the trial was ongoing.

IVUS examinations were performed as previously described,12–16 using 40MHz catheters. Meticulous care was used to ensure that all IVUS examinations utilized identical procedures during baseline and follow-up procedures. All IVUS examinations were analyzed at the Montréal Heart Institute core laboratory by experienced technicians supervised by a cardiologist blinded to treatment assignment, according to published standards.17 The lumen and external elastic membrane borders were manually traced on digitized cross-sections at every 1mm in the 30mm segment of interest on both the baseline and follow-up images. Plaque, lumen, and total vessel volumes were computed for the entire length of the analyzed segments. Analyses of plaque characterization were also conducted as previously described.14,16,18 Similarly, QCA examinations were performed at baseline and follow-up, with meticulous care being taken to ensure identical conditions during each evaluation. The segments of interest were visualized in multiple transverse and sagital views to separate stenoses from branches, minimize foreshortening, and obtain views as perpendicular as possible to the long axis of the segments to be analyzed. All angiograms were analyzed at the Montréal Heart Institute core laboratory by means of the CMS (MEDIS, Leiden, The Netherlands).19 All IVUS and QCA analyses were performed by experienced technicians supervised by an expert physician in matched projections from baseline and follow-up examinations.

The primary efficacy end-point in this trial was the percentage change in atheroma volume on IVUS (follow-up to baseline/baseline times 100), and the primary analysis focused on the percentage change in the active groups. Secondary efficacy measures included the absolute change in plaque volume, the change in plaque characterization indices on IVUS, and coronary score on QCA (defined as the per-patient mean of the minimal lumen diameter for all lesions measured).

An evaluable baseline and follow-up IVUS assessment was carried out on 145 patients (47 received placebo, 89 received 40mg/kg rHDL, and nine received 80mg/kg rHDL). Following the enrollment of approximately 30 patients in the trial, the independent safety review committee recommended that dosing with 80mg/kg be discontinued due to elevations in alanine aminotransferase (ALT)/aspartate aminotransferase (AST) levels. Therefore, additional patients were randomized into the 40mg rHDL and placebo groups until the target number of patients in placebo and active treatment was reached.

Results from this study demonstrated that plaque volume was similar between the 40mg/kg rHDL treatment group and the placebo group at baseline (158.3mm3 for placebo and 151.0mm3 for rHDL 40mg/kg). The interval between baseline and follow-up IVUS examinations was approximately 43 days. The difference in percentage change in atheroma volume between the treatment groups was not statistically significant. The percentage change in atheroma volume in the 40mg/kg group was −3.41 (interquartile range (IQR) −6.55–1.88) with p<0.001 compared with baseline. The corresponding change in the placebo group was −1.62 (IQR −5.95–1.94) with p=0.07. The difference in absolute change in plaque volume was not statistically significant between groups (p=0.39). The absolute change in plaque volume was −5.43mm3 (IQR −9.11–2.25) in the 40mg/kg treatment group (p<0.001 versus baseline) and −2.33mm3 for placebo (IQR −9.41–3.31) (p=0.04 versus baseline).

The evolution of both plaque characterization indices (arc and inner perimeter) on IVUS was significantly different between study groups (p=0.01 for both between rHDL and placebo). On QCA evaluation, there was also evidence of significant differences between rHDL and placebo on the coronary score (p=0.03). For illustrative purposes, at a coronary score of 2.265mm at baseline, the least square mean (standard error, SE) change in coronary score was -0.0390mm (0.009mm) in the 40mg/kg group and -0.0713mm (0.013mm) with placebo (p=0.03).

Following the pre-planned safety interim analysis, the 80mg/kg treatment group was discontinued at the recommendation of the independent safety committee. Out of a total of 12 patients randomized to receive 80mg/kg, seven (58.3%) and four (33.3%) experienced elevations in ALT >30 times and >10 times upper level of normal (ULN), respectively, with some patients experiencing elevations >100 times ULN.

Transaminase levels peaked the day following study drug administration, consistently declined on subsequent days, and were reversible in all patients. No patient experienced major clinical adverse events as a result of these elevations. The administration of 40mg/kg rHDL was generally well-tolerated. Clinical events were generally mild or moderate, and there was no difference in overall frequency between the 40mg/kg treatment and placebo groups.

The results of this study showed differences in coronary atheroma volume after four weekly infusions that were not statistically significant between groups. However, the results suggest that rHDL may potentially induce some favorable vascular effects, as demonstrated by the significant reduction in atheroma volume with active infusions comparing follow-up minus baseline values. Additionally, both the plaque characterization indices on IVUS and coronary score on QCA revealed statistically significant differences between rHDL and placebo groups that support a biological effect of rHDL. The benefit of rHDL compared with placebo in terms of coronary score is similar to that observed in previously reported clinical trials after two years of statin treatment.20,21 Given the known longer-term prognostic value of changes on QCA,22 the results from this study support larger, longer, and more definitive clinical studies of rHDL therapy. The results obtained in this study are comparable to those of a similar study conducted with reconstituted HDL containing apolipoprotein A-I Milano.7

Although the mechanism by which high plasma HDL levels decrease the risk of coronary artery disease is not fully understood, cholesterol efflux and reverse cholesterol transport are considered important targets for new anti-atherosclerotic therapy strategies. HDL may also protect low-density lipoprotein (LDL) cholesterol from oxidation and decrease the expression of adhesion molecules and inflammatory constituents that contribute to the formation of atherosclerotic plaques. The increased risk of cardiovascular death recently reported with torcetrapib, in spite of significant increases in HDL,23 highlights the importance of evaluating the full spectrum of potential drug-induced effects in clinical trials. While 40mg/kg rHDL was well-tolerated in this trial, further assessments of the risk/benefit profile of this agent are warranted.

In summary, short-term infusions of rHDL 40mg/kg administered on a background of optimal available therapy resulted in a statistically significant decrease from baseline in plaque burden as assessed by percentage change in plaque volume. Patients receiving placebo on a background of optimal available therapy in this trial experienced smaller decreases in percentage change in plaque volume that were not statistically significant. While the difference in percentage change in plaque volume between the two treatment groups is not statistically significant, changes from baseline in patients receiving rHDL and changes between the two treatment groups on other IVUS and QCA measures taken together strongly suggest the biological activity of rHDL therapy. The clinical significance of these findings is not yet known, and further evaluations are warranted.

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