High-Dose Atorvastatin Reduces Total Plasma Levels of Oxidized Phospholipids and Immune Complexes Present on Apolipoprotein B-100 in Patients With Acute Coronary Syndromes in the MIRACL Trial

Tsimikas, Sotirios; Witztum, Joseph L.; Miller, Elizabeth R.; Sasiela, William J.; Szarek, Michael; Olsson, Anders G.; Schwartz, Gregory G.

doi:10.1161/01.cir.0000141728.23033.b5

Cited by 225Lipoproteins and Cardiovascular HealthAtherosclerosis and Cardiovascular DiseasesCholesterol and Lipid Metabolism

High-Dose Atorvastatin Reduces Total Plasma Levels of Oxidized Phospholipids and Immune Complexes Present on Apolipoprotein B-100 in Patients With Acute Coronary Syndromes in the MIRACL Trial

Tsimikas, Sotirios, Witztum, Joseph L., Miller, Elizabeth R., Sasiela, William J., Szarek, Michael, Olsson, Anders G., Schwartz, Gregory G.·2004·Circulation

DOI 10.1161/01.cir.0000141728.23033.b5

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Abstract

Background— Oxidized phospholipids (OxPL) are present within atherosclerotic plaques and bound by lipoprotein (a) [Lp(a)] in plasma. This study evaluated the impact of atorvastatin on oxidized LDL (OxLDL) in patients with acute coronary syndromes (ACS). Methods and Results— OxLDL-E06 (OxPL content on apolipoprotein B-100 [apoB] detected by antibody E06), apoB-100 immune complexes (apoB-IC), OxLDL autoantibodies, and Lp(a) levels were measured in 2341 patients at baseline and after 16 weeks of treatment with atorvastatin 80 mg/d or placebo. The OxLDL-E06 and apoB-IC data are reported per apoB-100 particle (OxPL/apoB, IC/apoB) and as total levels on all apoB-100 particles (total apoB-OxPL and total apoB-IC [eg, OxPL/apoB or IC/apoB×apoB-100 levels]). Compared with baseline values, atorvastatin reduced apoB-100 (−33%), total apoB-OxPL (−29.7%), total apoB-IC IgG (−29.5%), and IgM (−25.7%) ( P <0.0001 for all), whereas no change or an increase was observed with placebo. When normalized per apoB-100, compared with placebo, atorvastatin increased OxPL/apoB (9.5% versus −3.9%, P <0.0001) and Lp(a) (8.8% versus −0.7%, ( P <0.0001). A strong correlation was noted between OxPL/apoB and Lp(a) ( R =0.85, P <0.0001), consistent with previous data that Lp(a) binds OxPL. Conclusions— After atorvastatin treatment, total OxPL on all apoB-100 particles was decreased. However, there was enrichment of OxPL on a smaller pool of apoB-100 particles, in parallel with similar increases in Lp(a), suggesting binding by Lp(a). These data support the hypothesis that atorvastatin promotes mobilization and clearance of proinflammatory OxPL, which may contribute to a reduction in ischemic events after ACS.

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Studies reported no or only a minor increase in Lp(a) levels among patients treated with statins.
“Studies reported no or only a minor increase in lipoprotein (a) (Lp(a)) levels among patients treated with statins [33, 34].”
From Established and Emerging Lipid-Lowering Drugs for Primary and Secondary Cardiovascular Prevention (2023) · cites this paper as [33]
Beta-glucan, a viscous fibre from oats and barley, consistently lowers total cholesterol and LDL-C.
“Available evidence consistently demonstrates a TCand LDL-Clowering effect of β-glucan, a viscous fibre from oat and barley.”
From 2019 ESC/EAS guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk (2019) · cites this paper as [186]
Foods enriched with beta-glucan or related fibre supplements are well tolerated and effective for LDL-C lowering.
“Foods enriched with these fibres or supplements are well tolerated, effective, and recommended for LDL-C lowering [186].”
From 2019 ESC/EAS guidelines for the management of dyslipidaemias: lipid modification to reduce cardiovascular risk (2019) · cites this paper as [186]

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Oxidized Phospholipids Predict the Presence and Progression of Carotid and Femoral Atherosclerosis and Symptomatic Cardiovascular Disease
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High-density lipoprotein, but not low-density lipoprotein cholesterol levels influence short-term prognosis after acute coronary syndrome: results from the MIRACL trial
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Oxidized Phospholipids on apoB-100-Containing Lipoproteins: a Biomarker Predicting Cardiovascular Disease and Cardiovascular Events
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Statin therapy and lipoprotein(a) levels: a systematic review and meta-analysis
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AMG145, a Monoclonal Antibody Against Proprotein Convertase Subtilisin Kexin Type 9, Significantly Reduces Lipoprotein(a) in Hypercholesterolemic Patients Receiving Statin Therapy
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Monocyte tissue factor–dependent activation of coagulation in hypercholesterolemic mice and monkeys is inhibited by simvastatin
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Clinical applications of circulating oxidized low-density lipoprotein biomarkers in cardiovascular disease
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Oxidation-Specific Biomarkers, Lipoprotein(a), and Risk of Fatal and Nonfatal Coronary Events
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New Insights Into the Role of Lipoprotein(a)-Associated Lipoprotein-Associated Phospholipase A 2 in Atherosclerosis and Cardiovascular Disease
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Untitled work
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Relationship of Oxidized Phospholipids on Apolipoprotein B-100 Particles to Race/Ethnicity, Apolipoprotein(a) Isoform Size, and Cardiovascular Risk Factors
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Oxidized phospholipids in cardiovascular disease
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Intermolecular Differences of 3-Hydroxy-3-Methylglutaryl Coenzyme A Reductase Inhibitors Contribute to Distinct Pharmacologic and Pleiotropic Actions
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Treatment of patients with cardiovascular disease with L-4F, an apo-A1 mimetic, did not improve select biomarkers of HDL function
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Aged garlic extract supplemented with B vitamins, folic acid and l-arginine retards the progression of subclinical atherosclerosis: A randomized clinical trial
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Measurement of Plasma Oxidized Low-Density Lipoprotein and its Clinical Implications
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Oxidative Modification of LDL: Its Pathological Role in Atherosclerosis
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The role of oxidized phospholipids in mediating lipoprotein(a) atherogenicity
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Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study
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The Dynamics of Oxidized LDL during Atherogenesis
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Lipoprotein(a), Oxidized Phospholipids, and Coronary Artery Disease Severity and Outcomes
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The Influence of Pravastatin and Atorvastatin on Markers of Oxidative Stress in Hypercholesterolemic Humans
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Protective Role for B-1b B Cells and IgM in Obesity-Associated Inflammation, Glucose Intolerance, and Insulin Resistance
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Relationship of Oxidized Phospholipids and Biomarkers of Oxidized Low-Density Lipoprotein With Cardiovascular Risk Factors, Inflammatory Biomarkers, and Effect of Statin Therapy in Patients With Acute Coronary Syndromes
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Effect of therapeutic interventions on oxidized phospholipids on apolipoprotein B100 and lipoprotein(a)
Yeang, C., Hung, M., Byun, Y. S., Clopton, P., Yang, X., Witztum, J. L., & Tsimikas, S. (2016) · Journal of clinical lipidology · doi:10.1016/j.jacl.2016.01.005 · Cited by 110 · see citing works
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Malondialdehyde Epitopes as Targets of Immunity and the Implications for Atherosclerosis
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Oxidative Biomarkers in the Diagnosis and Prognosis of Cardiovascular Disease
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Established and Emerging Lipid-Lowering Drugs for Primary and Secondary Cardiovascular Prevention
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“Studies reported no or only a minor increase in lipoprotein (a) (Lp(a)) levels among patients treated with statins [33, 34].”
Background
The Role of Lipids and Lipoproteins in Atherosclerosis
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Inflammatory Biomarkers in Acute Coronary Syndromes
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Oxidation-Specific Biomarkers and Risk of Peripheral Artery Disease
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Relationship Between Biomarkers of Oxidized Low-Density Lipoprotein, Statin Therapy, Quantitative Coronary Angiography, and Atheroma Volume
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Tea Catechin Consumption Reduces Circulating Oxidized Low-Density Lipoprotein
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Oxidized Low-Density Lipoprotein in Children With Familial Hypercholesterolemia and Unaffected Siblings
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Oxidized phospholipid modification of lipoprotein(a): Epidemiology, biochemistry and pathophysiology
Koschinsky, M. L., & Boffa, M. B. (2022) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2022.04.001 · Cited by 94 · see citing works
Changes in lipoprotein(a), oxidized phospholipids, and LDL subclasses with a low-fat high-carbohydrate diet
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Lipoprotein(a) Mass Levels Increase Significantly According to <i>APOE</i> Genotype: An Analysis of 431 239 Patients
Moriarty, P. M., Varvel, S. A., Gordts, P. L. S. M., McConnell, J. P., & Tsimikas, S. (2017) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.116.308704 · Cited by 89 · see citing works
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Lipoprotein(a) and oxidized phospholipids in calcific aortic valve stenosis
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Oxidized low-density lipoprotein biomarkers in atherosclerosis
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Granulocyte Macrophage Colony-Stimulating Factor Regulates Dendritic Cell Content of Atherosclerotic Lesions
Shaposhnik, Z., Wang, X., Weinstein, M. M., Bennett, B. J., & Lusis, A. J. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000254673.55431.e6 · Cited by 87 · see citing works
Increased plasma levels of oxysterols, in vivo markers of oxidative stress, in patients with familial combined hyperlipidemia: Reduction during atorvastatin and fenofibrate therapy
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Active Metabolite of Atorvastatin Inhibits Membrane Cholesterol Domain Formation by an Antioxidant Mechanism
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Is Plasma Oxidized Low-Density Lipoprotein, Measured With the Widely Used Antibody 4E6, an Independent Predictor of Coronary Heart Disease Among U.S. Men and Women?
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Oxidized Low-Density Lipoprotein Autoantibodies, Chronic Infections, and Carotid Atherosclerosis in a Population-Based Study
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Oxidized low-density lipoprotein associates with cardiovascular disease by a vicious cycle of atherosclerosis and inflammation: A systematic review and meta-analysis
Hong, C. G., Florida, E. M., Li, H., Parel, P. M., Mehta, N. N., & Sorokin, A. V. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.1023651 · Cited by 82 · see citing works
Increased Plasma Oxidized Phospholipid:Apolipoprotein B-100 Ratio With Concomitant Depletion of Oxidized Phospholipids From Atherosclerotic Lesions After Dietary Lipid-Lowering
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Transient Increase in Plasma Oxidized LDL During the Progression of Atherosclerosis in Apolipoprotein E Knockout Mice
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Reduction of oxidative stress and modulation of autoantibodies against modified low‐density lipoprotein after rosuvastatin therapy
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Comparison Effect of Atorvastatin (10 versus 80 mg) on Biomarkers of Inflammation and Oxidative Stress in Subjects With Metabolic Syndrome
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Lipoprotein(a) in Familial Hypercholesterolemia With Proprotein Convertase Subtilisin/Kexin Type 9 (PCSK9) Gain-of-Function Mutations
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Eicosapentaenoic acid inhibits glucose-induced membrane cholesterol crystalline domain formation through a potent antioxidant mechanism
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Clinical significance of the humoral immune response to modified LDL
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Hyperlipidemia, tissue factor, coagulation, and simvastatin
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Reduced In Vivo Aortic Uptake of Radiolabeled Oxidation-Specific Antibodies Reflects Changes in Plaque Composition Consistent With Plaque Stabilization
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Relationship of Oxidized Phospholipids on Apolipoprotein B-100 to Cardiovascular Outcomes in Patients Treated With Intensive Versus Moderate Atorvastatin Therapy
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The impact of age on 6-month survival in patients with cardiovascular risk factors undergoing elective non-cardiac surgery
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Lipoprotein(a), platelet function and cardiovascular disease
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Lipoprotein(a) and Its Potential Association with Thrombosis and Inflammation in COVID-19: a Testable Hypothesis
Moriarty, P. M., Gorby, L. K., Stroes, E. S. G., Kastelein, J. J. P., Davidson, M. H., & Tsimikas, S. (2020) · Current Atherosclerosis Reports · doi:10.1007/s11883-020-00867-3 · Cited by 72 · see citing works
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Diacylglycerols and Lysophosphatidic Acid, Enriched on Lipoprotein(a), Contribute to Monocyte Inflammation
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Eicosapentaenoic acid inhibits oxidation of ApoB-containing lipoprotein particles of different size in vitro when administered alone or in combination with Atorvastatin active metabolite compared with other triglyceride-lowering agents
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In Vivo Markers of Oxidative Stress and Therapeutic Interventions
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Biomarkers of Inflammation and Oxidative Stress in Atherosclerosis
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Beyond Lipid Lowering: What Have We Learned About the Benefits of Statins from the Acute Coronary Syndromes Trials?
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Small dense LDL is more susceptible to glycation than more buoyant LDL in Type 2 diabetes
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Lipoprotein(a)
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Emerging therapeutic agents to lower lipoprotein (a) levels
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New and Emerging Risk Factors for Coronary Heart Disease
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Lipoprotein a: where are we now?
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Unique Antibody Responses to Malondialdehyde-Acetaldehyde (MAA)-Protein Adducts Predict Coronary Artery Disease
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Statin treatment increases lipoprotein(a) levels in subjects with low molecular weight apolipoprotein(a) phenotype
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Letter Regarding Article by Tsimikas et al, “High-Dose Atorvastatin Reduces Total Plasma Levels of Oxidized Phospholipids and Immune Complexes Present on Apolipoprotein B-100 in Patients With Acute Coronary Syndromes in the MIRACL Trial”
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Abstract 475: Relationship Between Oxidized Phospholipid Content On Apolipoprotein B-100 Particles, Statin Therapy and Atheroma Volume: Observations From The REVERSAL Study
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Short- and long-term elevation of autoantibody titers against oxidized LDL in patients with acute coronary syndromes
Papathanasiou, A. I., Lourida, E. S., Tsironis, L. D., Goudevenos, J. A., & Tselepis, A. D. (2006) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2006.10.033 · Cited by 29 · see citing works

Authors: Tsimikas, S., Witztum, J. L., Miller, E. R., Sasiela, W. J., Szarek, M., Olsson, A. G., & Schwartz, G. G.
Affiliations: Linköping University (SE)
Corresponding author: Tsimikas, Sotirios
ORCID: Tsimikas, Sotirios
Witztum, Joseph L.
Miller, Elizabeth R.
Sasiela, William J.
Szarek, Michael
Olsson, Anders G.
Schwartz, Gregory G.
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2004-09-14
Volume: 110
Issue: 11
Pages: 1406-1412
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/01.cir.0000141728.23033.b5
OpenAlex: W2109629533
Semantic Scholar: 5d8d1d7bcae3432d2e03d42643169af12f5e5419
Cited by: 225
References: 45
Citations by year: 2026: 2 · 2025: 6 · 2024: 8 · 2023: 10 · 2022: 10 · 2021: 5 · 2020: 7 · 2019: 6 · 2018: 8 · 2017: 6 · 2016: 15 · 2015: 13 · 2014: 10 · 2013: 10 · 2012: 9
FWCI: 14.84
Type: journal article
Language: en
Open access: closed
Locations: Circulation (publishedVersion)
PubMed (publishedVersion)
Funders: Donald W. Reynolds Foundation
Pfizer
National Heart, Lung, and Blood Institute (P50HL056989, HL-56989)
Topics: Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Keywords: atorvastatin, oxidized phospholipids, oxidized LDL, apolipoprotein B-100, immune complexes, lipoprotein(a), acute coronary syndrome, statin therapy, atherosclerosis, atherosclerotic plaque
MeSH terms: Atorvastatin, Aged, Angina, Unstable, Antigen-Antibody Complex, Apolipoproteins B, Autoantibodies, Double-Blind Method, Female, Heptanoic Acids, Humans, Immunoglobulin G, Immunoglobulin M, Lipoproteins, LDL, Male, Middle Aged, Myocardial Infarction, Oxidation-Reduction, Phospholipids, Pyrroles, Lipoprotein(a), Hydroxymethylglutaryl-CoA Reductase Inhibitors, Apolipoprotein B-100

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High-Dose Atorvastatin Reduces Total Plasma Levels of Oxidized Phospholipids and Immune Complexes Present on Apolipoprotein B-100 in Patients With Acute Coronary Syndromes in the MIRACL Trial

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