Association of Small Low-Density Lipoprotein Particles With the Incidence of Coronary Artery Disease in Men and Women

Gardner, Christopher D.

doi:10.1001/jama.1996.03540110029028

Cited by 847Lipoproteins and Cardiovascular HealthDiabetes, Cardiovascular Risks, and LipoproteinsCholesterol and Lipid Metabolism

Association of Small Low-Density Lipoprotein Particles With the Incidence of Coronary Artery Disease in Men and Women

Gardner, Christopher D.·1996·JAMA: The Journal of the American Medical Association

DOI 10.1001/jama.1996.03540110029028

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Abstract

OBJECTIVE: To investigate the prospective association of low-density lipoprotein (LDL) particle diameter with the incidence of fatal and nonfatal coronary artery disease (CAD). DESIGN: A nested case-control study. SETTING: Cases and controls were identified from a population-based sample of men and women combining all of the 5 cross-sectional surveys conducted from 1979 to 1990 of the Stanford Five-City Project (FCP). PARTICIPANTS: Incident CAD cases were identified through FCP surveillance between 1979 and 1992. Controls were matched by sex, 5-year age groups, survey time point, ethnicity, and FCP treatment condition. The sample included 124 matched pairs: 90 pairs of men and 34 pairs of women. MAIN OUTCOME MEASURES: LDL peak particle diameter (LDL size) was determined by gradient gel electrophoresis on plasma samples collected during the cross-sectional surveys (stored at 70 degrees C for 5-15 years). Established CAD risk-factor data were available from FCP baseline measurements. RESULTS: LDL size was smaller among CAD cases than controls (mean +/- SD) (26.17 +/- 1.00 nm vs 26.68 +/- 0.90 nm; P<.001). The association was graded across control quintiles of LDL size. The significant case-control difference in LDL size was independent of levels of high-density lipoprotein cholesterol (HDL-C), non-HDL cholesterol (non-HDL-C), triglyceride, smoking, systolic blood pressure, and body mass index, but was not significant after adjusting for the ratio of total cholesterol (TC) to HDL-C (TC:HDL-C). Among all the physiological risk factors, LDL size was the best differentiator of CAD status in conditional logistic regression. However, when added to the physiological parameters above, the TC:HDL-C ratio was found to be a stronger independent predictor of CAD status. CONCLUSION: LDL size was significantly smaller in CAD cases than in controls in a prospective, population-based study. These findings support other evidence of a role for small, dense LDL particles in the etiology of atherosclerosis.

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Legro, R. S. (2003) · Endocrine Reviews · doi:10.1210/er.2003-0004 · Cited by 466 · see citing works
“LDL subclasses are important predictors of CVD (94).”
Background
Apo B versus cholesterol in estimating cardiovascular risk and in guiding therapy: report of the thirty‐person/ten‐country panel
Barter, P. J., Ballantyne, C. M., Carmena, R., Cabezas, M. C., Chapman, M. J., Couture, P., Graaf, J. D., Durrington, P. N., Færgeman, O., Frohlich, J., et al. (2006) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2006.01616.x · Cited by 463 · see citing works
Hepatic insulin resistance, metabolic syndrome and cardiovascular disease
Meshkani, R., & Adeli, K. (2009) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2009.05.018 · Cited by 458 · see citing works
“The data from the Stanford Five-City Project showed that the incident coronary artery disease cases had significantly smaller LDL peak particle size compared with controls matched for age, sex and ethnicity [170].”
Method
New insights into the pathophysiology of dyslipidemia in type 2 diabetes
Taskinen, M.-R., & Borén, J. (2015) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2015.01.039 · Cited by 440 · see citing works
Low-Density Lipoprotein Subfractions and the Long-Term Risk of Ischemic Heart Disease in Men: 13-Year Follow-Up Data From the Québec Cardiovascular Study
St-Pierre, A. C., Cantin, B., Dagenais, G. R., Mauriège, P., Bernard, P.-M., Després, J.-P., & Lamarche, B. (2005) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000154144.73236.f4 · Cited by 422 · see citing works
Effects of Low-Carbohydrate Diets Versus Low-Fat Diets on Metabolic Risk Factors: A Meta-Analysis of Randomized Controlled Clinical Trials
Hu, T., Mills, K. T., Yao, L., Demanelis, K., Eloustaz, M., Yancy, W. S., Kelly, T. N., He, J., & Bazzano, L. A. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kws264 · Cited by 417 · see citing works
Fasting Insulin and Apolipoprotein B Levels and Low-Density Lipoprotein Particle Size as Risk Factors for Ischemic Heart Disease
Lamarche, B. (1998) · JAMA · doi:10.1001/jama.279.24.1955 · Cited by 417 · see citing works
Oxidized LDL and HDL: antagonists in atherothrombosis
Mertens, A. C., & Holvoet, P. (2001) · The FASEB Journal · doi:10.1096/fj.01-0273rev · Cited by 410 · see citing works
Low-Density Lipoprotein Particle Concentration and Size as Determined by Nuclear Magnetic Resonance Spectroscopy as Predictors of Cardiovascular Disease in Women
Blake, G. J., Otvos, J. D., Rifai, N., & Ridker, P. M. (2002) · Circulation · doi:10.1161/01.cir.0000033222.75187.b9 · Cited by 409 · see citing works
Infection and Inflammation‐Induced Proatherogenic Changes of Lipoproteins
Khovidhunkit, W., Memon, R. A., Feingold, K. R., & Grünfeld, C. (2000) · The Journal of Infectious Diseases · doi:10.1086/315611 · Cited by 403 · see citing works
“Whether ceruloplasmin is prooxidant or antioxidant in vivo is uncertain, but plasma ceruloplasmin level is a risk factor for CAD [96].”
BackgroundInfluential
Assessment of cardiovascular risk by use of multiple-risk-factor assessment equations
Grundy, S. M., Pasternak, R. C., Greenland, P., Smith, S. C., & Fuster, V. (1999) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(99)00387-3 · Cited by 401 · see citing works
Effect of ritonavir on lipids and post-heparin lipase activities in normal subjects
Purnell, J. Q., Zambon, A., Knopp, R. H., Pizzuti, D. J., Achari, R., Leonard, J. M., Locke, C. S., & Brunzell, J. D. (2000) · AIDS · doi:10.1097/00002030-200001070-00006 · Cited by 384 · see citing works
LDL particle subclasses, LDL particle size, and carotid atherosclerosis in the Multi-Ethnic Study of Atherosclerosis (MESA)
Mora, S., Szklo, M., Otvos, J. D., Greenland, P., Psaty, B. M., Goff, D. C., O’Leary, D. H., Saad, M. F., Tsai, M. Y., & Sharrett, A. R. (2007) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2006.05.007 · Cited by 380 · see citing works
Association of Cholesteryl Ester Transfer Protein– Taq IB Polymorphism With Variations in Lipoprotein Subclasses and Coronary Heart Disease Risk
Ordovás, J. M., Cupples, L. A., Corella, D., Otvos, J. D., Osgood, D. P., Martinez, A. A., Lahoz, C., Coltell, Ó., Wilson, P. W. F., & Schaefer, E. J. (2000) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.20.5.1323 · Cited by 379 · see citing works
An International Atherosclerosis Society Position Paper: Global recommendations for the management of dyslipidemia
Grundy, S. M. (2013) · Journal of clinical lipidology · doi:10.1016/j.jacl.2013.10.001 · Cited by 349 · see citing works
Relation of Lipoprotein Subclasses as Measured by Proton Nuclear Magnetic Resonance Spectroscopy to Coronary Artery Disease
Freedman, D. S., Otvos, J. D., Jeyarajah, E. J., Barboriak, J. J., Anderson, A. J., & Walker, J. A. (1998) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.18.7.1046 · Cited by 345 · see citing works
Beyond Low-Density Lipoprotein Cholesterol
Arsenault, B. J., Rana, J. S., Stroes, E. S. G., Després, J.-P., Shah, P. K., Kastelein, J. J. P., Wareham, N. J., Boekholdt, S. M., & Khaw, K.-T. (2009) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2009.07.057 · Cited by 342 · see citing works
Effects of Low-Carbohydrate and Low-Fat Diets: A Randomized Trial
Bazzano, L. A., Hu, T., Reynolds, K., Yao, L., Bunol, C., Liu, Y., Chen, C.-S., Klag, M. J., Whelton, P. K., & He, J. (2014) · Annals of Internal Medicine · doi:10.7326/m14-0180 · Cited by 346 · see citing works
“10-Year Framingham CHD Risk Score Participants in the low-carbohydrate group had significant decreases in estimated 10-year risk for CHD at 6 and 12 months, whereas those in the low-fat group did not (Table 3 and Appendix Figure).”
BackgroundInfluential
Hypertriglyceridemic HyperapoB: The Unappreciated Atherogenic Dyslipoproteinemia in Type 2 Diabetes Mellitus
Sniderman, A. D., Scantlebury, T., & Cianflone, K. (2001) · Annals of Internal Medicine · doi:10.7326/0003-4819-135-6-200109180-00014 · Cited by 329 · see citing works
Obesity and Disturbed Lipoprotein Profile in Estrogen Receptor-α-Deficient Male Mice
Ohlsson, C., Hellberg, N., Parini, P., Vidal, O., Bohlooly, M., Rudling, M., Lindberg, M. K., Warner, M., Angelin, B., & Gustafsson, J.-Å. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.3827 · Cited by 332 · see citing works
Separate effects of reduced carbohydrate intake and weight loss on atherogenic dyslipidemia
Krauss, R. M., Blanche, P. J., Rawlings, R. S., Fernstrom, H. S., & Williams, P. T. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.5.1025 · Cited by 321 · see citing works
An International Atherosclerosis Society Position Paper: Global recommendations for the management of dyslipidemia-Full report
Grundy, S. M., Arai, H., Barter, P. J., Bersot, T. P., Betteridge, D. J., Carmena, R., Cuevas, A. M., Davidson, M. H., Genest, J. J., Kesäniemi, Y. A., et al. (2013) · Journal of clinical lipidology · doi:10.1016/j.jacl.2013.12.005 · Cited by 328 · see citing works
“A high Lp-PLA2 appears to be predictive of ASCVD; but at present the test is not widely available.”
Background
Cardiometabolic Aspects of the Polycystic Ovary Syndrome
Randeva, H. S., Tan, B. K., Weickert, M. O., Lois, K. B., Nestler, J. E., Sattar, N. A., & Lehnert, H. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1003 · Cited by 323 · see citing works
Health Outcomes of Severely Obese Type 2 Diabetic Subjects 1 Year After Laparoscopic Adjustable Gastric Banding
Dixon, J. B., & O’Brien, P. E. (2002) · Diabetes Care · doi:10.2337/diacare.25.2.358 · Cited by 319 · see citing works
“The size of LDL particles is the best indicator of coronary artery disease status, with small particles being highly atherogenic (23).”
Background
HDL-cholesterol as a marker of coronary heart disease risk: the Québec cardiovascular study
Després, J., Lemieux, I., Dagenais, G. R., Cantin, B., & Lamarche, B. (2000) · Atherosclerosis · doi:10.1016/s0021-9150(00)00603-1 · Cited by 315 · see citing works
“small, dense LDL particles [31–33], hyperinsulinemia as a marker of insulin resistance in non-diabetic subjects [34,35], elevated homocysteine concentrations [36,37], renin and aldosterone in hypertensive patients [38,39], markers of an impaired fibrinolytic capacity and of susceptibility to thrombosis [26,27,40,41] a…”
Background
Nuclear Magnetic Resonance Spectroscopy of Lipoproteins and Risk of Coronary Heart Disease in the Cardiovascular Health Study
Kuller, L. H., Arnold, A. M., Tracy, R. P., Otvos, J. D., Burke, G. L., Psaty, B. M., Siscovick, D. S., Freedman, D. S., & Kronmal, R. A. (2002) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000022015.97341.3a · Cited by 310 · see citing works
Diabetic Retinopathy and Serum Lipoprotein Subclasses in the DCCT/EDIC Cohort
Lyons, T. J., Jenkins, A. J., Zheng, D., Lackland, D. T., McGee, D., Garvey, W. T., & Klein, R. L. (2004) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.02-0648 · Cited by 309 · see citing works
Sex and Age Differences in Lipoprotein Subclasses Measured by Nuclear Magnetic Resonance Spectroscopy: The Framingham Study
Freedman, D. S., Otvos, J. D., Jeyarajah, E. J., SHALAUROVA, I. Y., Cupples, L. A., Parise, H., D’Agostino, R. B., Wilson, P. W. F., & Schaefer, E. J. (2004) · Clinical Chemistry · doi:10.1373/clinchem.2004.032763 · Cited by 304 · see citing works
“Lipoprotein particle size VLDL, nm 48 ( 9 ) 44 (8) 4c 2c”
Pathophysiology and types of dyslipidemia in PCOS
Diamanti‐Kandarakis, E., Papavassiliou, A. G., Kandarakis, S., & Chrousos, G. P. (2007) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2007.07.004 · Cited by 301 · see citing works
Multivariable Analysis: A Practical Guide for Clinicians and Public Health Researchers
Katz, M. H. (2011) · Cited by 298 · see citing works
Non-HDL Cholesterol as a Predictor of Cardiovascular Disease in Type 2 Diabetes
Lu, W., Resnick, H. E., Jablonski, K. A., Jones, K. L., Jain, A. K., Howard, W. J., Robbins, D. C., & Howard, B. V. (2003) · Diabetes Care · doi:10.2337/diacare.26.1.16 · Cited by 370 · see citing works
Non-high-density lipoprotein and very-low-density lipoprotein cholesterol and their risk predictive values in coronary heart disease
Liu, J., Sempos, C. T., Donahue, R. P., Dorn, J., Trevisan, M., & Grundy, S. M. (2006) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2006.06.032 · Cited by 277 · see citing works
Lipid management in patients with chronic kidney disease
Ferro, C. J., Mark, P. B., Kanbay, M., Sarafidis, P. A., Heine, G. H., Rossignol, P., Massy, Z. A., Mallamaci, F., Valdivielso, J. M., Małyszko, J., et al. (2018) · Nature Reviews Nephrology · doi:10.1038/s41581-018-0072-9 · Cited by 275 · see citing works
Relationships Between Low-Density Lipoprotein Particle Size, Plasma Lipoproteins, and Progression of Coronary Artery Disease
Vakkilainen, J., Steiner, G. A., Ansquer, J.-C., Aubin, F., Rattier, S., Foucher, C., Hamsten, A., & Taskinen, M. (2003) · Circulation · doi:10.1161/01.cir.0000057982.50167.6e · Cited by 270 · see citing works
Lipids and lipoproteins as coronary risk factors in non-insulin-dependent diabetes mellitus
Syvänne, M., & Taskinen, M. (1997) · The Lancet · doi:10.1016/s0140-6736(97)90024-6 · Cited by 268 · see citing works
Development of a Rapid, Quantitative Method for LDL Subfractionation with Use of the Quantimetrix Lipoprint LDL System
Hoefner, D. M., Hodel, S. D., O’Brien, J. F., Branum, E. L., Sun, D. H., Meissner, I., & McConnell, J. P. (2001) · Clinical Chemistry · doi:10.1093/clinchem/47.2.266 · Cited by 266 · see citing works
“An association between phenotype B and increased risk for CAD was first postulated in retrospective studies (2–5) and was later supported by prospective studies (6, 7).”
Background
Evidence for a New Pathophysiological Mechanism for Coronary Artery Disease Regression: Hepatic Lipase–Mediated Changes in LDL Density
Zambon, A., Hokanson, J. E., Brown, B. G., & Brunzell, J. D. (1999) · Circulation · doi:10.1161/01.cir.99.15.1959 · Cited by 263 · see citing works
Cardiovascular disease mortality in familial forms of hypertriglyceridemia: a 20-year prospective study.
Austin, M. A., McKnight, B., Edwards, K. L., Bradley, C. M., McNeely, M. J., Psaty, B. M., Brunzell, J. D., & Motulsky, A. G. (2000) · Circulation · doi:10.1161/01.cir.101.24.2777 · Cited by 255 · see citing works
Low-density lipoprotein size and cardiovascular risk assessment
Rizzo, M., & Berneis, K. K. (2005) · QJM · doi:10.1093/qjmed/hci154 · Cited by 257 · see citing works
Comparison of Various Electrophoretic Characteristics of LDL Particles and Their Relationship to the Risk of Ischemic Heart Disease
St-Pierre, A., Ruel, I. L., Cantin, B., Dagenais, G. R., Bernard, P., Després, J., & Lamarche, B. (2001) · Circulation · doi:10.1161/hc4401.098490 · Cited by 259 · see citing works
Implications of plasma concentrations of adiponectin in patients with coronary artery disease
Nakamura, Y., Shimada, K., Fukuda, D., Shimada, Y., Ehara, S., Hirose, M., Kataoka, T., Kamimori, K., Shimodozono, S., 小林, 芳., et al. (2004) · Heart · doi:10.1136/hrt.2003.011114 · Cited by 256 · see citing works
Obesity and Insulin Resistance
Després, J., & Marette, A. (1999) · Humana Press eBooks · doi:10.1007/978-1-59259-716-1_4 · Cited by 254 · see citing works
A major health hazard: The metabolic syndrome
Isomaa, B. (2003) · Life Sciences · doi:10.1016/s0024-3205(03)00646-5 · Cited by 245 · see citing works
Low-Density Lipoprotein Size and Cardiovascular Disease: A Reappraisal
Sacks, F. M., & Campos, H. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030636 · Cited by 241 · see citing works
Value of Low-Density Lipoprotein Particle Number and Size as Predictors of Coronary Artery Disease in Apparently Healthy Men and Women
El Harchaoui, K., van der Steeg, W. A., Stroes, E. S. G., Kuivenhoven, J. A., Otvos, J. D., Wareham, N. J., Hutten, B. A., Kastelein, J. J. P., Khaw, K.-T., & Boekholdt, S. M. (2007) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2006.09.043 · Cited by 239 · see citing works
Effects of Recombinant Apolipoprotein A-I Milano on Aortic Atherosclerosis in Apolipoprotein E–Deficient Mice
Shah, P. K., Nilsson, J. Å., Kaul, S., Fishbein, M. C., Ageland, H., Hamsten, A., Johansson, J., Karpe, F., & Cercek, B. (1998) · Circulation · doi:10.1161/01.cir.97.8.780 · Cited by 238 · see citing works
RVX-208
Bailey, D., Jahagirdar, R., Gordon, A., Hafiane, A., Campbell, S., Chatur, S., Wagner, G. S., Hansen, H. C., Chiacchia, F. S., Johansson, J., et al. (2010) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2010.02.035 · Cited by 233 · see citing works
Soy isoflavones improve plasma lipids in normocholesterolemic, premenopausal women
Merz-Demlow, B. E., Duncan, A. M., Wangen, K. E., Xu, X., Carr, T. P., Phipps, W. R., & Kurzer, M. S. (2000) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.6.1462 · Cited by 231 · see citing works
Identification of Unique Lipoprotein Subclasses for Visceral Obesity by Component Analysis of Cholesterol Profile in High-Performance Liquid Chromatography
Okazaki, M., Usui, S., Ishigami, M., Sakai, N., Nakamura, T., Matsuzawa, Y., & Yamashita, S. (2005) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000155017.60171.88 · Cited by 229 · see citing works
Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women
Wangen, K. E., Duncan, A. M., Xu, X., & Kurzer, M. S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.225 · Cited by 220 · see citing works
Recipes for Creating Animal Models of Diabetic Cardiovascular Disease
Hsueh, W. A., Abel, E. D., Breslow, J. L., Maeda, N., Davis, R. C., Fisher, E. A. A., Dansky, H. M., McClain, D. A., McIndoe, R., Wassef, M. K., et al. (2007) · Circulation Research · doi:10.1161/01.res.0000266449.37396.1f · Cited by 219 · see citing works
Clinical relevance of the biochemical, metabolic, and genetic factors that influence low-density lipoprotein heterogeneity
Kwiterovich, P. O. (2002) · The American Journal of Cardiology · doi:10.1016/s0002-9149(02)02749-2 · Cited by 207 · see citing works
Plasma Lipidomic Profiling and Risk of Type 2 Diabetes in the PREDIMED Trial
Razquín, C., Toledo, E., Clish, C. B., Ruiz‐Canela, M., Dennis, C., Corella, D., Papandreou, C., Ros, E., Estruch, R., Guasch‐Ferré, M., et al. (2018) · Diabetes Care · doi:10.2337/dc18-0840 · Cited by 208 · see citing works
Low-density lipoprotein particle number and risk for cardiovascular disease
Cromwell, W. C., & Otvos, J. D. (2004) · Current Atherosclerosis Reports · doi:10.1007/s11883-004-0050-5 · Cited by 198 · see citing works
Effect of long-chain n-3 polyunsaturated fatty acids on fasting and postprandial triacylglycerol metabolism.
Roche, H. M., & Gibney, M. J. (2000) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/71.1.232s · Cited by 195 · see citing works
Lipoprotein Subfraction Changes in Normal Pregnancy: Threshold Effect of Plasma Triglyceride on Appearance of Small, Dense Low Density Lipoprotein1
Sattar, N. A., Greer, I. A., Louden, J., Lindsay, G., McConnell, M., Shepherd, J., & Packard, C. J. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.8.4126 · Cited by 193 · see citing works
“Furthermore, recently reported prospective studies have demonstrated that the presence of small, dense LDL particles precedes CHD (15, 16 ) and predicts the development of noninsulin dependent diabetes mellitus (17).”
Background
Diagnosis, prevention, and intervention for the metabolic syndrome.
Scott, C. (2003) · American Journal of Cardiology · doi:10.1016/s0002-9149(03)00507-1 · Cited by 214 · see citing works
Enhanced oxidative susceptibility and reduced antioxidant content of metabolic precursors of small, dense low-density lipoproteins
Tribble, D. L., Rizzo, M., Chait, A., Lewis, D. M., Blanche, P. J., & Krauss, R. M. (2001) · The American Journal of Medicine · doi:10.1016/s0002-9343(00)00700-2 · Cited by 185 · see citing works
Strawberries decrease atherosclerotic markers in subjects with metabolic syndrome
Basu, A., Fu, D. X., Wilkinson, M., Simmons, B. N., Wu, M., Betts, N. M., Du, M., & Lyons, T. J. (2010) · Nutrition Research · doi:10.1016/j.nutres.2010.06.016 · Cited by 184 · see citing works
“Distribution of lipoprotein sub-class profiles, such as variations in concentrations of small, medium and large particles, not reflected in conventional lipid analyses, has been inversely associated with vascular complications in diabetes and atherosclerosis [22,23].”
Lipoprotein atherogenicity: an overview of current mechanisms
Griffin, B. A. (1999) · Proceedings of The Nutrition Society · doi:10.1079/pns19990022 · Cited by 182 · see citing works
“There is now prospective evidence to show that small dense LDL is as predictive of CHD as many of the more traditional risk factors such as smoking and blood pressure (Gardner et al. 1996; Stampfer et al. 1996).”
Background
Development of a Homogeneous Assay for Measurement of Small Dense LDL Cholesterol
Ito, Y., Fujimura, M., Ohta, M., & Hirano, T. (2010) · Clinical Chemistry · doi:10.1373/clinchem.2010.149559 · Cited by 181 · see citing works
Dietary Fats and Health: Dietary Recommendations in the Context of Scientific Evidence
Lawrence, G. D. (2013) · Advances in Nutrition · doi:10.3945/an.113.003657 · Cited by 174 · see citing works
“It was later found that LDL particle size was also significantly smaller in men with CAD than in case-matched controls (27), although another study showed the ratio of total serum cholesterol to HDL-C was a better predictor of CAD risk than LDL particle size (28).”
Result
Long-term efficacy and tolerability of add-on pioglitazone therapy to failing monotherapy compared with addition of gliclazide or metformin in patients with type 2 diabetes
Charbonnel, B., Schernthaner, G., Brunetti, P., Matthews, D. R., Urquhart, R., Tan, M. H., & Hanefeld, M. (2005) · Diabetologia · doi:10.1007/s00125-005-1751-1 · Cited by 170 · see citing works
“Compositional alterations in LDL particles can be potentially atherogenic [31–34].”
Non–High-Density Lipoprotein Cholesterol Levels Predict Five-Year Outcome in the Bypass Angioplasty Revascularization Investigation (BARI)
Bittner, V., Hardison, R., Kelsey, S. F., Weiner, B. H., Jacobs, A. K., & Sopko, G. (2002) · Circulation · doi:10.1161/01.cir.0000038496.57570.06 · Cited by 168 · see citing works
Lipids and Glucose in Type 2 Diabetes
Boden, G. H., & Laakso, M. (2004) · Diabetes Care · doi:10.2337/diacare.27.9.2253 · Cited by 168 · see citing works
“Some (3,4) but not all (5) studies have demonstrated that increased levels of small, dense LDL are associated with an elevated risk of cardiovascular disease.”
Background
The effect of isoflavones extracted from red clover (Rimostil) on lipid and bone metabolism
Clifton-Bligh, P. B., Baber, R., Fulcher, G., Nery, M.-L., & Moreton, T. (2001) · Menopause The Journal of The North American Menopause Society · doi:10.1097/00042192-200107000-00007 · Cited by 167 · see citing works
Swine Models of Type 2 Diabetes Mellitus: Insulin Resistance, Glucose Tolerance, and Cardiovascular Complications
Bellinger, D. A., Merricks, E. P., & Nichols, T. C. (2006) · ILAR Journal · doi:10.1093/ilar.47.3.243 · Cited by 166 · see citing works
“The human IR phenotype is characterized by accumulation of small dense LDL particles as opposed to large LDL particles (Carr et al. 1999; Gardner et al. 1996; Kohen-Avramoglu et al. 2003) and by suppression of large HDL particles (Brown et al. 1990; Deeb et al. 2003; Garvey et al. 2003; Goff et al.…”
Background
High-fiber oat cereal compared with wheat cereal consumption favorably alters LDL-cholesterol subclass and particle numbers in middle-aged and older men.
Davy, B. M., Davy, K. P., Ho, R. C., Beske, S. D., Davrath, L. R., & Melby, C. L. (2002) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/76.2.351 · Cited by 161 · see citing works
“An elevated LDL particle number, often indicated by high apolipoprotein B concentrations, has also been linked to an increased CAD risk (8, 13).”
BackgroundInfluential
Systematic review: association of low-density lipoprotein subfractions with cardiovascular outcomes.
Ip, S., Lichtenstein, A. H., Chung, M., Lau, J., & Balk, E. M. (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-150-7-200904070-00007 · Cited by 163 · see citing works
“…case–control 68 70 100 17 63 (ever smoked) LDL-c: 142 mg/dL Mykkänen et al, 1999 (27) GE Nested case–control 69 100 50 33 20 (current) TC–HDL-c ratio: 6.09 Gardner et al, 1996 (26) GE Nested case–control 59 33 73 No data 42 (not defined) Non–HDL-c: 176 mg/dL CAD coronary artery disease; CHD…”
Influential
Lipoprotein-Associated Phospholipase A2 Activity Is a Marker of Small, Dense LDL Particles in Human Plasma
Gazi, I. F., Lourida, E. S., Filippatos, T. D., Tsimihodimos, V., Elisaf, M., & Tselepis, A. D. (2005) · Clinical Chemistry · doi:10.1373/clinchem.2005.058404 · Cited by 162 · see citing works
Guinea pigs: A suitable animal model to study lipoprotein metabolism, atherosclerosis and inflammation
Fernández, M. L., & Volek, J. S. (2006) · Nutrition & Metabolism · doi:10.1186/1743-7075-3-17 · Cited by 162 · see citing works
“Small dense LDL particles classified as pattern B are associated with a much higher risk for cardiovascular disease [ 51 ], thus this important feature of carbohydrate restriction in increasing the size of LDL is quite beneficial, specifically for patients with the metabolic syndrome and type II diabetes, which have a…”
Background
Novel Risk Factors for Atherosclerosis
Kullo, I. J., Gau, G. T., & Tajik, A. J. (2000) · Mayo Clinic Proceedings · doi:10.4065/75.4.369 · Cited by 160 · see citing works
Statin-fibrate combination therapy for hyperlipidaemia: a review
Wierzbicki, A. S., Mikhailidis, D. P., Wray, R., Schachter, M., Cramb, R., Simpson, W. G., & Byrne, C. D. (2003) · Current Medical Research and Opinion · doi:10.1185/030079903125001668 · Cited by 156 · see citing works
Unfavorable lipid profile in women with endometriosis
Melo, A. S., Rosa-e-Silva, J. C., Rosa-e-Silva, A. C. J. D. S., Poli-Neto, O. B., Ferriani, R. A., & Vieira, C. S. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.08.043 · Cited by 143 · see citing works
Low-Density Lipoprotein Triglycerides Associated With Low-Grade Systemic Inflammation, Adhesion Molecules, and Angiographic Coronary Artery Disease
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Low density lipoprotein particle size and coronary artery disease. Arterioscler. Thromb
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Authors: Gardner, C. D.
Affiliations: Stanford Medicine (US)
Corresponding author: Gardner, Christopher D.
ORCID: Gardner, Christopher D.
Venue: JAMA: The Journal of the American Medical Association
Publisher: American Medical Association (AMA)
Published: 1996-09-18
Volume: 276
Issue: 11
Pages: 875
ISSN: 0002-9955 (ISSN-L)
0098-7484
DOI: 10.1001/jama.1996.03540110029028
OpenAlex: W2050758709
Cited by: 843
References: 53
Citations by year: 2026: 3 · 2025: 4 · 2024: 5 · 2023: 10 · 2022: 10 · 2021: 16 · 2020: 23 · 2019: 14 · 2018: 7 · 2017: 16 · 2016: 10 · 2015: 23 · 2014: 14 · 2013: 33 · 2012: 22
FWCI: 37.88
Type: journal article
Language: en
Open access: closed
Locations: JAMA (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5p01hl018574-26, 5r01hl021906-19)
National Heart, Lung, and Blood Institute (T32HL007034, HL21906, HL-18574, 5 T32 HL07034)
Topics: Health Sciences › Medicine › Surgery › Lipoproteins and Cardiovascular Health
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Health Sciences › Medicine › Surgery › Cholesterol and Lipid Metabolism
Keywords: small dense LDL, LDL particle size, coronary artery disease, atherosclerosis, cardiovascular risk factors, TC/HDL-C ratio, HDL cholesterol, non-HDL cholesterol, triglycerides, sex differences
MeSH terms: Adult, Aged, Coronary Disease, Cross-Sectional Studies, Electrophoresis, Polyacrylamide Gel, Female, Humans, Lipids, Lipoproteins, LDL, Male, Middle Aged, Prospective Studies, Risk Factors, Body Mass Index, Incidence, Linear Models, Logistic Models, Case-Control Studies

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Association of Small Low-Density Lipoprotein Particles With the Incidence of Coronary Artery Disease in Men and Women

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