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(Circulation. 2001;103:1955.)
© 2001 American Heart Association, Inc.

Clinical Investigation and Reports

Elevated Levels of Oxidized Low Density Lipoprotein Show a Positive Relationship With the Severity of Acute Coronary Syndromes

Shoichi Ehara, MD; Makiko Ueda, MD; Takahiko Naruko, MD; Kazuo Haze, MD; Akira Itoh, MD; Masato Otsuka, MD; Ryushi Komatsu, MD; Toshihiko Matsuo, MD; Hiroyuki Itabe, PhD; Tatsuya Takano, PhD; Yoshiaki Tsukamoto, MD; Minoru Yoshiyama, MD; Kazuhide Takeuchi, MD; Junichi Yoshikawa, MD; Anton E. Becker, MD

From the Department of Cardiology (S.E., T.N., K.H., A.I., M.O.), Osaka City General Hospital; the Department of Pathology (M.U., R.K., T.M.) and First Department of Internal Medicine (M.Y., K.T., J.Y.), Osaka City University Medical School, Osaka; the Department of Microbiology and Molecular Pathology (H.I., T.T.), Faculty of Pharmaceutical Sciences, Teikyo University, Kanagawa, Japan; and the Department of Cardiovascular Pathology (Y.T., A.E.B.), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands.

Correspondence to Makiko Ueda, MD, Department of Pathology, Osaka City University Medical School, 1-4-3, Asahi-machi, Abeno-ku, Osaka, 545-8585, Japan. E-mail maki{at}med.osaka-cu.ac.jp

Background—There is accumulating data that acute coronary syndromes relate to recent onset activation of inflammation affecting atherosclerotic plaques. Increased blood levels of oxidized low density lipoprotein (ox-LDL) could play a role in these circumstances.

Methods and Results—Ox-LDL levels were measured in 135 patients with acute myocardial infarction (AMI; n=45), unstable angina pectoris (UAP; n=45), and stable angina pectoris (SAP; n=45) and in 46 control subjects using a sandwich ELISA method. In addition, 33 atherectomy specimens obtained from a different cohort of patients with SAP (n=10) and UAP (n=23) were studied immunohistochemically for ox-LDL. In AMI patients, ox-LDL levels were significantly higher than in patients with UAP (P<0.0005) or SAP (P<0.0001) or in controls (P<0.0001) (AMI, 1.95±1.42 ng/5 µg LDL protein; UAP, 1.19±0.74 ng/5 µg LDL protein; SAP, 0.89±0.48 ng/5 µg LDL protein; control, 0.58±0.23 ng/5 µg LDL protein). Serum levels of total, HDL, and LDL cholesterol did not differ among these patient groups. In the atherectomy specimens, the surface area containing ox-LDL–positive macrophages was significantly higher in patients with UAP than in those with SAP (P<0.0001).

Conclusions—This study demonstrates that ox-LDL levels show a significant positive correlation with the severity of acute coronary syndromes and that the more severe lesions also contain a significantly higher percentage of ox-LDL–positive macrophages. These observations suggest that increased levels of ox-LDL relate to plaque instability in human coronary atherosclerotic lesions.

Key Words: atherosclerosis • coronary disease • myocardial infarction • angina

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				J. L. Mehta, B. Hu, J. Chen, and D. Li Pioglitazone Inhibits LOX-1 Expression in Human Coronary Artery Endothelial Cells by Reducing Intracellular Superoxide Radical Generation Arterioscler Thromb Vasc Biol, December 1, 2003; 23(12): 2203 - 2208. [Abstract] [Full Text] [PDF]

				F. M. Sacks and H. Campos Low-Density Lipoprotein Size and Cardiovascular Disease: A Reappraisal J. Clin. Endocrinol. Metab., October 1, 2003; 88(10): 4525 - 4532. [Full Text] [PDF]

				H. Itabe, M. Mori, Y. Fujimoto, Y. Higashi, and T. Takano Minimally Modified LDL Is an Oxidized LDL Enriched with Oxidized Phosphatidylcholines J. Biochem., September 1, 2003; 134(3): 459 - 465. [Abstract] [Full Text] [PDF]

				A. Wakatsuki, Y. Okatani, N. Ikenoue, K. Shinohara, K. Watanabe, and T. Fukaya Effect of Lower Dose of Oral Conjugated Equine Estrogen on Size and Oxidative Susceptibility of Low-Density Lipoprotein Particles in Postmenopausal Women Circulation, August 19, 2003; 108(7): 808 - 813. [Abstract] [Full Text] [PDF]

				E. Rother, R. Brandl, D. L. Baker, P. Goyal, H. Gebhard, G. Tigyi, and W. Siess Subtype-Selective Antagonists of Lysophosphatidic Acid Receptors Inhibit Platelet Activation Triggered by the Lipid Core of Atherosclerotic Plaques Circulation, August 12, 2003; 108(6): 741 - 747. [Abstract] [Full Text] [PDF]

				P. Holvoet, T. B. Harris, R. P. Tracy, P. Verhamme, A. B. Newman, S. M. Rubin, E. M. Simonsick, L. H. Colbert, and S. B. Kritchevsky Association of High Coronary Heart Disease Risk Status With Circulating Oxidized LDL in the Well-Functioning Elderly: Findings From the Health, Aging, and Body Composition Study Arterioscler Thromb Vasc Biol, August 1, 2003; 23(8): 1444 - 1448. [Abstract] [Full Text] [PDF]

				B. M. Singh and J. L. Mehta Interactions Between the Renin-Angiotensin System and Dyslipidemia: Relevance in the Therapy of Hypertension and Coronary Heart Disease Arch Intern Med, June 9, 2003; 163(11): 1296 - 1304. [Abstract] [Full Text] [PDF]

				Z. T. Bloomgarden Inflammation and Insulin Resistance Diabetes Care, June 1, 2003; 26(6): 1922 - 1926. [Full Text] [PDF]

				A. Onody, C. Csonka, Z. Giricz, and P. Ferdinandy Hyperlipidemia induced by a cholesterol-rich diet leads to enhanced peroxynitrite formation in rat hearts Cardiovasc Res, June 1, 2003; 58(3): 663 - 670. [Abstract] [Full Text] [PDF]

				Z. Ahmed, A. Ravandi, G. F Maguire, A. Kuksis, and P. W Connelly Formation of apolipoprotein AI-phosphatidylcholine core aldehyde Schiff base adducts promotes uptake by THP-1 macrophages Cardiovasc Res, June 1, 2003; 58(3): 712 - 720. [Abstract] [Full Text] [PDF]

				G. N. Fredrikson, I. Soderberg, M. Lindholm, P. Dimayuga, K.-Y. Chyu, P. K. Shah, and J. Nilsson Inhibition of Atherosclerosis in ApoE-Null Mice by Immunization with ApoB-100 Peptide Sequences Arterioscler Thromb Vasc Biol, May 1, 2003; 23(5): 879 - 884. [Abstract] [Full Text] [PDF]

				A. Mertens, P. Verhamme, J. K. Bielicki, M. C. Phillips, R. Quarck, W. Verreth, D. Stengel, E. Ninio, M. Navab, B. Mackness, et al. Increased Low-Density Lipoprotein Oxidation and Impaired High-Density Lipoprotein Antioxidant Defense Are Associated With Increased Macrophage Homing and Atherosclerosis in Dyslipidemic Obese Mice: LCAT Gene Transfer Decreases Atherosclerosis Circulation, April 1, 2003; 107(12): 1640 - 1646. [Abstract] [Full Text] [PDF]

				D. Li, V. Williams, L. Liu, H. Chen, T. Sawamura, F. Romeo, and J. L. Mehta Expression of lectin-like oxidized low-density lipoprotein receptors during ischemia-reperfusion and its role in determination of apoptosis and left ventricular dysfunction J. Am. Coll. Cardiol., March 19, 2003; 41(6): 1048 - 1055. [Abstract] [Full Text] [PDF]

				M Uno, K T Kitazato, K Nishi, H Itabe, and S Nagahiro Raised plasma oxidised LDL in acute cerebral infarction J. Neurol. Neurosurg. Psychiatry, March 1, 2003; 74(3): 312 - 316. [Abstract] [Full Text] [PDF]

				S. Tsimikas, C. Bergmark, R. W. Beyer, R. Patel, J. Pattison, E. Miller, J. Juliano, and J. L. Witztum Temporal increases in plasma markers of oxidized low-density lipoprotein strongly reflect the presence of acute coronary syndromes J. Am. Coll. Cardiol., February 5, 2003; 41(3): 360 - 370. [Abstract] [Full Text] [PDF]

				D. Li, L. Liu, H. Chen, T. Sawamura, S. Ranganathan, and J. L. Mehta LOX-1 Mediates Oxidized Low-Density Lipoprotein-Induced Expression of Matrix Metalloproteinases in Human Coronary Artery Endothelial Cells Circulation, February 4, 2003; 107(4): 612 - 617. [Abstract] [Full Text] [PDF]

				G. Pankhurst, X. L. Wang, D. E. Wilcken, G. Baernthaler, U. Panzenbock, M. Raftery, and R. Stocker Characterization of specifically oxidized apolipoproteins in mildly oxidized high density lipoprotein J. Lipid Res., February 1, 2003; 44(2): 349 - 355. [Abstract] [Full Text] [PDF]

				B. Bayes, M. C. Pastor, J. Bonal, J. Junca, J. M. Hernandez, N. Riutort, A. Foraster, and R. Romero Homocysteine, C-reactive protein, lipid peroxidation and mortality in haemodialysis patients Nephrol. Dial. Transplant., January 1, 2003; 18(1): 106 - 112. [Abstract] [Full Text] [PDF]

				Z. Ahmed, S. Babaei, G. F. Maguire, D. Draganov, A. Kuksis, B. N. La Du, and P. W. Connelly Paraoxonase-1 reduces monocyte chemotaxis and adhesion to endothelial cells due to oxidation of palmitoyl, linoleoyl glycerophosphorylcholine Cardiovasc Res, January 1, 2003; 57(1): 225 - 231. [Abstract] [Full Text] [PDF]

				J. C. Fang, S. Kinlay, D. Behrendt, H. Hikita, J. L. Witztum, A. P. Selwyn, and P. Ganz Circulating Autoantibodies to Oxidized LDL Correlate With Impaired Coronary Endothelial Function After Cardiac Transplantation Arterioscler Thromb Vasc Biol, December 1, 2002; 22(12): 2044 - 2048. [Abstract] [Full Text] [PDF]

				D. Li, V. Williams, L. Liu, H. Chen, T. Sawamura, T. Antakli, and J. L. Mehta LOX-1 inhibition in myocardial ischemia-reperfusion injury: modulation of MMP-1 and inflammation Am J Physiol Heart Circ Physiol, November 1, 2002; 283(5): H1795 - H1801. [Abstract] [Full Text] [PDF]

				H. Azumi, N. Inoue, Y. Ohashi, M. Terashima, T. Mori, H. Fujita, K. Awano, K. Kobayashi, K. Maeda, K. Hata, et al. Superoxide Generation in Directional Coronary Atherectomy Specimens of Patients With Angina Pectoris: Important Role of NAD(P)H Oxidase Arterioscler Thromb Vasc Biol, November 1, 2002; 22(11): 1838 - 1844. [Abstract] [Full Text] [PDF]

				S. Kopprasch, J. Pietzsch, E. Kuhlisch, K. Fuecker, T. Temelkova-Kurktschiev, M. Hanefeld, H. Kuhne, U. Julius, and J. Graessler In Vivo Evidence for Increased Oxidation of Circulating LDL in Impaired Glucose Tolerance Diabetes, October 1, 2002; 51(10): 3102 - 3106. [Abstract] [Full Text] [PDF]

				K. Nishi, H. Itabe, M. Uno, K. T. Kitazato, H. Horiguchi, K. Shinno, and S. Nagahiro Oxidized LDL in Carotid Plaques and Plasma Associates With Plaque Instability Arterioscler Thromb Vasc Biol, October 1, 2002; 22(10): 1649 - 1654. [Abstract] [Full Text] [PDF]

				A. Wakatsuki, Y. Okatani, N. Ikenoue, and T. Fukaya Different Effects of Oral Conjugated Equine Estrogen and Transdermal Estrogen Replacement Therapy on Size and Oxidative Susceptibility of Low-Density Lipoprotein Particles in Postmenopausal Women Circulation, October 1, 2002; 106(14): 1771 - 1776. [Abstract] [Full Text] [PDF]

				I. Loftus and M. Thompson The role of matrix metalloproteinases in vascular disease Vascular Medicine, May 1, 2002; 7(2): 117 - 133. [Abstract] [PDF]

				J. L. Mehta and D. Li Identification, regulation and function of a novel lectin-like oxidized low-density lipoprotein receptor J. Am. Coll. Cardiol., May 1, 2002; 39(9): 1429 - 1435. [Abstract] [Full Text] [PDF]

				K. Tanaga, H. Bujo, M. Inoue, K. Mikami, K. Kotani, K. Takahashi, T. Kanno, and Y. Saito Increased Circulating Malondialdehyde-Modified LDL Levels in Patients With Coronary Artery Diseases and Their Association With Peak Sizes of LDL Particles Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 662 - 666. [Abstract] [Full Text] [PDF]