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

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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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Effects of troglitazone on atherogenic lipoprotein phenotype in coronary patients with insulin resistance
Sunayama, S., Watanabe, Y., Ohmura, H., Sawano, M., Shimada, K., Mokuno, H., Daida, H., & Yamaguchi, H. (1999) · Atherosclerosis · doi:10.1016/s0021-9150(99)00138-0 · Cited by 39
Lipids and Diabetic Retinopathy
Modjtahedi, B. S., Bose, N., Papakostas, T. D., Morse, L. S., Vavvas, D. G., & Kishan, A. U. (2016) · Seminars in Ophthalmology · doi:10.3109/08820538.2015.1114869 · Cited by 41
“Small LDL is considered more atherogenic than large LDL because it crosses the endothelium and becomes oxidized more easily.(30) Similarly, large HDL is thought to be negatively associated with atherogenesis because it has associated paraoxonase activity that can aid in detoxifying lipid peroxidation products.”
Background
Polycystic ovary syndrome and the risk of cardiometabolic complications in longitudinal studies
Jacewicz‐Święcka, M., & Kowalska, I. (2018) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3054 · Cited by 39
“In women with PCOS, higher levels of very low‐density lipoprotein cholesterol and low‐density lipoprotein cholesterol (LDL‐C) were also described,(38-41) with predominantly small dense LDL‐C particles, which are considered to have special atherogenic potential.(42,43) One of the most often cited articles concerning ab…”
Background
Comparison of high-density and low-density lipoprotein cholesterol subclasses and sizes in asian indian women with caucasian women from the framingham offspring study
Bhalodkar, N. C., Blum, S., Rana, T., Kitchappa, R., Bhalodkar, A., & Enas, E. A. (2005) · Clinical Cardiology · doi:10.1002/clc.4960280510 · Cited by 38
The Atherogenic Significance of an Elevated Plasma Triglyceride Level
Ooi, T. C., & Ooi, D. S. (1998) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408369891234255 · Cited by 37
LipoSEARCH®; Analytical GP-HPLC method for lipoprotein profiling and its applications
Toshima, G., Iwama, Y., Kimura, F., Yukie, M., Mizuho, M., Junichiro, T., Yasuda, H., Nobuaki, A., Hisashi, M., Hata, K., et al. (2013) · Journal of Biological Macromolecules · doi:10.14533/jbm.13.21 · Cited by 37
Non-high-density lipoprotein cholesterol predicts nonfatal recurrent myocardial infarction in patients with ST segment elevation myocardial infarction
Gao, M., Zheng, Y., Zhang, W., Cheng, Y., Wang, L., & Qin, L. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0418-5 · Cited by 37
“However, prospective cohort studies show that nonhigh-density lipoprotein (non-HDL) cholesterol is an independent risk factor for mortality among individuals predominately free of coronary heart disease [14, 15], and recently revised National Cholesterol Education Program guidelines recommend that non-HDL and LDL be e…”
Background
Serum lipids level assessed in early pregnancy and risk of pre‐eclampsia
Demirci, O., Tuğrul, S., Dolgun, N., Sözen, H., & Eren, S. (2011) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2011.01562.x · Cited by 37
“Histological studies of placental arteries delivered from pre-eclamptic women showed fibrin and complement deposition and the involvement of foam cells in atheromatous lesions.(12)”
Background
Effects of fenofibrate and ezetimibe, both as monotherapy and in coadministration, on cholesterol mass within lipoprotein subfractions and low-density lipoprotein peak particle size in patients with mixed hyperlipidemia
Tribble, D. L., Farnier, M., Macdonell, G., Perevozskaya, I. T., Davies, M. J., Gumbiner, B., & Musliner, T. A. (2008) · Metabolism · doi:10.1016/j.metabol.2008.01.026 · Cited by 37
Relationship between cholesteryl ester transfer protein and LDL heterogeneity in familial hypercholesterolemia
Hogue, J., Lamarche, B., Gaudet, D., Larivière, M., Tremblay, A. J., Bergeron, J., Lemieux, I., Després, J., Gagné, C., & Couture, P. (2004) · Journal of Lipid Research · doi:10.1194/jlr.m300420-jlr200 · Cited by 37
Pioglitazone plus a sulphonylurea or metformin is associated with increased lipoprotein particle size in patients with type 2 diabetes
Pérez, A., Khan, M. A., Johnson, T., & Karunaratne, M. (2004) · Diabetes and Vascular Disease Research · doi:10.3132/dvdr.2004.006 · Cited by 37
Differences in Risk Factors for Coronary Atherosclerosis According to Sex
Kim, H. (2024) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2024.13.2.97 · Cited by 40
Rapid Development of Atherosclerosis in the World’s Smallest Microminipig Fed a High-Fat/High-Cholesterol Diet
Kawaguchi, H., Yamada, T., Miura, N., Ayaori, M., Uto‐Kondo, H., Ikegawa, M., Noguchi, M., Wang, K., Izumi, H., & Tanimoto, A. (2013) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.21246 · Cited by 36
Association between small dense LDL and early atherosclerosis in a sample of menopausal women
Gentile, M., Panico, S., Mattiello, A., Ubaldi, S., Iannuzzo, G., Michele, M. D., Iannuzzi, A., & Rubba, P. (2013) · Clinica Chimica Acta · doi:10.1016/j.cca.2013.08.010 · Cited by 36
Low-Density Lipoprotein Subfractions and Cardiovascular Risk in Hypertension
Felmeden, D. C., Spencer, C. G. C., Blann, A. D., Beevers, D. G., & Lip, G. Y. H. (2003) · Hypertension · doi:10.1161/01.hyp.0000056997.40992.41 · Cited by 36
Associations between plasma lipid parameters and APOC3 and APOA4 genotypes in a healthy population are independent of dietary cholesterol intake
Herron, K. L., Lofgren, I. E., Adiconis, X., Ordovás, J. M., & Fernández, M. L. (2005) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2005.03.023 · Cited by 37
Emerging therapeutic strategies for the management of dyslipidemia in patients with the metabolic syndrome
Davidson, M. H. (2004) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2004.02.006 · Cited by 35
Genome-wide scan for quantitative trait loci influencing LDL size and plasma triglyceride in familial hypertriglyceridemia
Austin, M. A., Edwards, K. L., Monks, S. A., Koprowicz, K. M., Brunzell, J. D., Motulsky, A. G., Mahaney, M. C., & Hixson, J. E. (2003) · Journal of Lipid Research · doi:10.1194/jlr.m300272-jlr200 · Cited by 35
Low-Density Lipoprotein Particle Size Loci in Familial Combined Hyperlipidemia
Badzioch, M. D., Igo, R. P., Gagnon, F., Brunzell, J. D., Krauss, R. M., Motulsky, A. G., Wijsman, E. M., & Jarvik, G. P. (2004) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000143499.09575.93 · Cited by 36
“The use of novel Bayesian MCMC analytic methods allows for: (1) consideration of multilocus trait models that are not prespecified, (2) multipoint linkage analyses using all chromosome markers simultaneously, and (3) comparison of these results to those of logarithm of odds (lod) score methods.”
MethodResult
LDL and HDL subclass distribution in patients with end-stage renal diseases
Alabakovska, S. B., Todorova, B., Labudović, D. D., & Trajkovska, K. T. (2002) · Clinical Biochemistry · doi:10.1016/s0009-9120(02)00300-4 · Cited by 35
Lipid-lowering therapy in diabetes mellitus
Niemeijer-Kanters, S. D. J. M. (2001) · The Netherlands Journal of Medicine · doi:10.1016/s0300-2977(01)00105-x · Cited by 35
Effect of intensive lipid-lowering strategy on low-density lipoprotein particle size in patients with type 2 diabetes mellitus
Niemeijer-Kanters, S. D. J. M., Dallinga‐Thie, G. M., de Ruijter-Heijstek, F. C., Algra, A., Erkelens, D. W., Banga, J. D., & Jansen, H. (2001) · Atherosclerosis · doi:10.1016/s0021-9150(00)00642-0 · Cited by 35
Gemfibrozil Reduces Small Low-Density Lipoprotein More in Normolipemic Subjects Classified as Low-Density Lipoprotein Pattern B Compared With Pattern A
Superko, H. R., Berneis, K. K., Williams, P. T., Rizzo, M., & Wood, P. D. (2005) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2005.06.069 · Cited by 34
Effects of Statin on Small Dense Low-Density Lipoprotein Cholesterol and Remnant-Like Particle Cholesterol in Heterozygous Familial Hypercholesterolemia
Nozue, T., Michishita, I., Ito, Y., & Hirano, T. (2008) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.e552 · Cited by 34
LDL particle size, fat distribution and insulin resistance in obese children
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Low density lipoprotein (LDL) binding affinity for the LDL receptor in hyperlipoproteinemia
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“Small, dense LDL particles are reported to be common in patients with CAD [16–20], and have been suggested to be associated with increases in the plasma triglyceride level [19–21].”
Background
Association between small dense LDL and sub-clinical atherosclerosis in patients with psoriatic arthritis
Gentile, M., Peluso, R., Minno, M. N. D. D., Costa, L., Caso, F., Simone, B. D., Iannuzzo, G., Scarpa, R., & Rubba, P. (2016) · Clinical Rheumatology · doi:10.1007/s10067-016-3344-4 · Cited by 33
LDL cholesterol estimation in patients with the metabolic syndrome
Gazi, I. F., Tsimihodimos, V., Filippatos, T. D., Saougos, V. G., Bairaktari, E. T., Tselepis, A. D., & Elisaf, M. (2006) · Lipids in Health and Disease · doi:10.1186/1476-511x-5-8 · Cited by 33
“Large clinical studies have shown a consistent association between sdLDL particles and incident atherosclerotic disease [14, 15 ].”
Treatment of Small Dense LDL
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Response of lipid, lipoprotein-cholesterol, and electrophoretic characteristics of lipoproteins following a single bout of aerobic exercise in women
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“One recently identiWed example of such a perturbation is the association between small, dense lowdensity lipoprotein (LDL) and increased CHD risk (Gardner et al. 1996; St-Pierre et al. 2001).”
Background
Triglyceride-rich lipoproteins: are links with atherosclerosis mediated by a procoagulant and proinflammatory phenotype?
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“[8] Gardner CD, Fortmann SP, Krauss RM.”
Background
Effect of Ezetimibe on LDL-C Lowering and Atherogenic Lipoprotein Profiles in Type 2 Diabetic Patients Poorly Controlled by Statins
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Effects of 12 months of treatment with disease-modifying anti-rheumatic drugs on low and high density lipoprotein subclass distribution in patients with early rheumatoid arthritis: a pilot study
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“A previous study proved that LDL-C is an important univariate predictor for CAD [6].”
Background
Localization of genes that control LDL size fractions in baboons
Rainwater, D. L., Kammerer, C. M., Mahaney, M. C., Rogers, J., Cox, L. A., Schneider, J. L., & VandeBerg, J. L. (2003) · Atherosclerosis · doi:10.1016/s0021-9150(03)00051-0 · Cited by 31
Long-term effects of fish oil on lipoprotein subfractions and low density lipoprotein size in non-insulin-dependent diabetic patients with hypertriglyceridemia
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“prospective studies [3,4,6].”
Background
Linkage analysis of candidate genes and the small, dense low-density lipoprotein phenotype
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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 › Cardiology and Cardiovascular Medicine › Lipoproteins and Cardiovascular Health
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › 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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