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Circulation. 1996;93:1809-1817

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(Circulation. 1996;93:1809-1817.)
© 1996 American Heart Association, Inc.

Articles

Insulin Sensitivity and Atherosclerosis

George Howard, DrPH; Daniel H. O'Leary, MD; Daniel Zaccaro, MS; Steve Haffner, MD; Marian Rewers, MD, PhD; Richard Hamman, MD, DrPH; Joe V. Selby, MD, MPH; Mohammed F. Saad, MD; Peter Savage, MD; Richard Bergman, PhD; for the IRAS Investigators

From the Department of Public Health Sciences, Bowman Gray School of Medicine of Wake Forest University (G.H., D.Z.), Winston-Salem, NC; Department of Radiology, Tufts-New England Medical Center (D.H.O.), Boston, Mass; Division of Clinical Epidemiology, University of Texas at San Antonio (S.H.); Department of Preventive Medicine and Biometrics, University of Colorado Health Sciences Center (M.R., R.H.), Denver; Division of Research, Kaiser Permanente (J.V.S.), Oakland, Calif; Division of Diabetes, Hypertension, and Nutrition, Department of Medicine, University of Southern California Medical Center (M.F.S.), Los Angeles; Division of Epidemiology and Clinical Applications, National Heart, Lung, and Blood Institute (P.S.), Bethesda, Md; and Department of Physiology and Biophysics, University of Southern California School of Medicine (R.B.), Los Angeles.

Correspondence to George Howard, DrPH, Department of Public Health Sciences, Bowman Gray School of Medicine of Wake Forest University, Medical Center Blvd, Winston Salem, NC 27157-1063. E-mail howard@phs.bgsm.wfu.edu.

Background Reduced insulin sensitivity has been proposed as an important risk factor in the development of atherosclerosis. However, insulin sensitivity is related to many other cardiovascular risk factors, including plasma insulin levels, and it is unclear whether an independent role of insulin sensitivity exists. Large epidemiological studies that measure insulin sensitivity directly have not been conducted.

Methods and Results The Insulin Resistance Atherosclerosis Study (IRAS) evaluated insulin sensitivity (SI) by the frequently sampled intravenous glucose tolerance test with analysis by the minimal model of Bergman. IRAS measured intimal-medial thickness (IMT) of the carotid artery as an index of atherosclerosis by use of noninvasive B-mode ultrasonography. These measures, as well as factors that may potentially confound or mediate the relationship between insulin sensitivity and atherosclerosis, were available in relation to 398 black, 457 Hispanic, and 542 non-Hispanic white IRAS participants. There was a significant negative association between SI and the IMT of the carotid artery both in Hispanics and in non-Hispanic whites. This effect was reduced but not totally explained by adjustment for traditional cardiovascular disease risk factors, glucose tolerance, measures of adiposity, and fasting insulin levels. There was no association between SI and the IMT of the carotid artery in blacks. The association between SI and the IMT was stronger for the internal carotid artery than for the common carotid artery in all ethnic groups.

Conclusions Higher levels of insulin sensitivity are associated with less atherosclerosis in Hispanics and non-Hispanic whites but not in blacks. This effect is partially mediated by traditional cardiovascular risk factors.


Key Words: atherosclerosis • diabetes mellitus • insulin • carotid arteries




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E. Bonora, G. Formentini, F. Calcaterra, S. Lombardi, F. Marini, L. Zenari, F. Saggiani, M. Poli, S. Perbellini, A. Raffaelli, et al.
HOMA-Estimated Insulin Resistance Is an Independent Predictor of Cardiovascular Disease in Type 2 Diabetic Subjects: Prospective data from the Verona Diabetes Complications Study
Diabetes Care, July 1, 2002; 25(7): 1135 - 1141.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
A. J.G. Hanley, K. Williams, M. P. Stern, and S. M. Haffner
Homeostasis Model Assessment of Insulin Resistance in Relation to the Incidence of Cardiovascular Disease: The San Antonio Heart Study
Diabetes Care, July 1, 2002; 25(7): 1177 - 1184.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
K. Shinohara, T. Shoji, M. Emoto, H. Tahara, H. Koyama, E. Ishimura, T. Miki, T. Tabata, and Y. Nishizawa
Insulin Resistance as an Independent Predictor of Cardiovascular Mortality in Patients with End-Stage Renal Disease
J. Am. Soc. Nephrol., July 1, 2002; 13(7): 1894 - 1900.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
A. W. Miller, C. Tulbert, M. Puskar, and D. W. Busija
Enhanced Endothelin Activity Prevents Vasodilation to Insulin in Insulin Resistance
Hypertension, July 1, 2002; 40(1): 78 - 82.
[Abstract] [Full Text] [PDF]

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 JAMAHome page
M. J. Davies, D. J. Baer, J. T. Judd, E. D. Brown, W. S. Campbell, and P. R. Taylor
Effects of Moderate Alcohol Intake on Fasting Insulin and Glucose Concentrations and Insulin Sensitivity in Postmenopausal Women: A Randomized Controlled Trial
JAMA, May 15, 2002; 287(19): 2559 - 2562.
[Abstract] [Full Text] [PDF]

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 Diabetes CareHome page
R. S. Surwit, R. B. Williams, I. C. Siegler, J. D. Lane, M. Helms, K. L. Applegate, N. Zucker, M. N. Feinglos, C. M. McCaskill, and J. C. Barefoot
Hostility, Race, and Glucose Metabolism in Nondiabetic Individuals
Diabetes Care, May 1, 2002; 25(5): 835 - 839.
[Abstract] [Full Text] [PDF]

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 Am J EpidemiolHome page
S. H. Golden, A. Maguire, J. Ding, J. R. Crouse, J. A. Cauley, H. Zacur, and M. Szklo
Endogenous Postmenopausal Hormones and Carotid Atherosclerosis: A Case-Control Study of the Atherosclerosis Risk in Communities Cohort
Am. J. Epidemiol., March 1, 2002; 155(5): 437 - 445.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
E. D. Motley, S. M. Kabir, C. D. Gardner, K. Eguchi, G. D. Frank, T. Kuroki, M. Ohba, T. Yamakawa, and S. Eguchi
Lysophosphatidylcholine Inhibits Insulin-Induced Akt Activation Through Protein Kinase C-{alpha} in Vascular Smooth Muscle Cells
Hypertension, February 1, 2002; 39(2): 508 - 512.
[Abstract] [Full Text] [PDF]

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 Br Med BullHome page
A. D Timmis
Diabetes: Relationship to ischaemic heart disease
Br. Med. Bull., October 1, 2001; 59(1): 159 - 172.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
G. Perseghin, A. Caumo, M. Caloni, G. Testolin, and L. Luzi
Incorporation of the Fasting Plasma FFA Concentration into QUICKI Improves Its Association with Insulin Sensitivity in Nonobese Individuals
J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4776 - 4781.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
A. W. Miller, C. Dimitropoulou, G. Han, R. E. White, D. W. Busija, and G. O. Carrier
Epoxyeicosatrienoic acid-induced relaxation is impaired in insulin resistance
Am J Physiol Heart Circ Physiol, October 1, 2001; 281(4): H1524 - H1531.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
F. S. Facchini, N. Hua, F. Abbasi, and G. M. Reaven
Insulin Resistance as a Predictor of Age-Related Diseases
J. Clin. Endocrinol. Metab., August 1, 2001; 86(8): 3574 - 3578.
[Abstract] [Full Text] [PDF]

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 Am J EpidemiolHome page
N. M. Wedick, E. J. Mayer-Davis, D. L. Wingard, C. L. Addy, and E. Barrett-Connor
Insulin Resistance Precedes Weight Loss in Adults without Diabetes : The Rancho Bernardo Study
Am. J. Epidemiol., June 15, 2001; 153(12): 1199 - 1205.
[Abstract] [Full Text] [PDF]

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 Am J EpidemiolHome page
U. Lindblad, R. D. Langer, D. L. Wingard, R. G. Thomas, and E. L. Barrett-Connor
Metabolic Syndrome and Ischemic Heart Disease in Elderly Men and Women
Am. J. Epidemiol., March 1, 2001; 153(5): 481 - 489.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
P. V. G. Katakam, J. S. Pollock, D. M. Pollock, M. R. Ujhelyi, and A. W. Miller
Enhanced endothelin-1 response and receptor expression in small mesenteric arteries of insulin-resistant rats
Am J Physiol Heart Circ Physiol, February 1, 2001; 280(2): H522 - H527.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
W. T. Cefalu
Insulin Resistance: Cellular and Clinical Concepts
Experimental Biology and Medicine, January 1, 2001; 226(1): 13 - 26.
[Abstract] [Full Text]

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 Eur Heart JHome page
Y Otsuka, S Miyazaki, H Okumura, S Yasuda, S Daikoku, I Morii, Y Sutani, Y Goto, and H Nonogi
Abnormal glucose tolerance, not small vessel diameter, is a determinant of long-term prognosis in patients treated with balloon coronary angioplasty
Eur. Heart J., November 1, 2000; 21(21): 1790 - 1796.
[Abstract] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
A. Caumo, R. N. Bergman, and C. Cobelli
Insulin Sensitivity from Meal Tolerance Tests in Normal Subjects: A Minimal Model Index
J. Clin. Endocrinol. Metab., November 1, 2000; 85(11): 4396 - 4402.
[Abstract] [Full Text]

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 CirculationHome page
K. Takeda, T. Ichiki, T. Tokunou, Y. Funakoshi, N. Iino, K. Hirano, H. Kanaide, and A. Takeshita
Peroxisome Proliferator-Activated Receptor {gamma} Activators Downregulate Angiotensin II Type 1 Receptor in Vascular Smooth Muscle Cells
Circulation, October 10, 2000; 102(15): 1834 - 1839.
[Abstract] [Full Text] [PDF]

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 ANGIOLOGYHome page
T. J. Tegos, E. Kalodiki, S.-S. Daskalopoulou, and A. N. Nicolaides
Stroke: Epidemiology, Clinical Picture, and Risk Factors: Part I of III
Angiology, October 1, 2000; 51(10): 793 - 808.
[Abstract] [PDF]

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 J Am Coll CardiolHome page
T. Takagi, K. Yoshida, T. Akasaka, S. Kaji, T. Kawamoto, Y. Honda, A. Yamamuro, T. Hozumi, and S. Morioka
Hyperinsulinemia during oral glucose tolerance test is associated with increased neointimal tissue proliferation after coronary stent implantation in nondiabetic patients: A serial intravascular ultrasound study
J. Am. Coll. Cardiol., September 1, 2000; 36(3): 731 - 738.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
N. Hirai, H. Kawano, O. Hirashima, T. Motoyama, Y. Moriyama, T. Sakamoto, K. Kugiyama, H. Ogawa, K. Nakao, and H. Yasue
Insulin resistance and endothelial dysfunction in smokers: effects of vitamin C
Am J Physiol Heart Circ Physiol, September 1, 2000; 279(3): H1172 - H1178.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
T. Hammoud, J.-F. Tanguay, and M. G. Bourassa
Management of coronary artery disease: therapeutic options in patients with diabetes
J. Am. Coll. Cardiol., August 1, 2000; 36(2): 355 - 365.
[Abstract] [Full Text] [PDF]

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 Vasc MedHome page
M. Meier and G. L King
Protein kinase C activation and its pharmacological inhibition in vascular disease
Vascular Medicine, August 1, 2000; 5(3): 173 - 185.
[Abstract] [PDF]

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 Eur Heart JHome page
T Inoue, R Matsunaga, Y Sakai, I Yaguchi, K Takayanagi, and S Morooka
Insulin resistance affects endothelium-dependent acetylcholine-induced coronary artery response
Eur. Heart J., June 1, 2000; 21(11): 895 - 900.
[Abstract] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
M. Pyorala, H. Miettinen, P. Halonen, M. Laakso, and K. Pyorala
Insulin Resistance Syndrome Predicts the Risk of Coronary Heart Disease and Stroke in Healthy Middle-Aged Men : The 22-Year Follow-Up Results of the Helsinki Policemen Study
Arterioscler. Thromb. Vasc. Biol., February 1, 2000; 20(2): 538 - 544.
[Abstract] [Full Text] [PDF]

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 ChestHome page
P. Dylewicz, S. Bienkowska, L. Szczesniak, T. Rychlewski, I. Przywarska, M. Wilk, and A. Jastrzebski
Beneficial Effect of Short-term Endurance Training on Glucose Metabolism During Rehabilitation After Coronary Bypass Surgery*
Chest, January 1, 2000; 117(1): 47 - 51.
[Abstract] [Full Text] [PDF]

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 J Am Coll CardiolHome page
K. Saku, B. Zhang, K. Shirai, S. Jimi, K. Yoshinaga, and K. Arakawa
Hyperinsulinemic hypoalphalipoproteinemia as a new indicator for coronary heart disease
J. Am. Coll. Cardiol., November 1, 1999; 34(5): 1443 - 1451.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
E. J. G. Sijbrands, M. J. V. Hoffer, A. E. Meinders, L. M. Havekes, R. R. Frants, A. H. M. Smelt, and P. De Knijff
Severe Hyperlipidemia in Apolipoprotein E2 Homozygotes Due to a Combined Effect of Hyperinsulinemia and an SstI Polymorphism
Arterioscler. Thromb. Vasc. Biol., November 1, 1999; 19(11): 2722 - 2729.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
S. M. Haffner, R. D'Agostino Jr, D. Goff, B. Howard, A. Festa, M. F. Saad, and L. Mykkanen
LDL Size in African Americans, Hispanics, and Non-Hispanic Whites : The Insulin Resistance Atherosclerosis Study
Arterioscler. Thromb. Vasc. Biol., September 1, 1999; 19(9): 2234 - 2240.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
A. Festa, R. D'Agostino Jr, P. Rautaharju, D. H. O'Leary, M. Rewers, L. Mykkanen, and S. M. Haffner
Is QT Interval a Marker of Subclinical Atherosclerosis in Nondiabetic Subjects? : The Insulin Resistance Atherosclerosis Study (IRAS)
Stroke, August 1, 1999; 30(8): 1566 - 1571.
[Abstract] [Full Text] [PDF]

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 CirculationHome page
P. Lempiainen, L. Mykkanen, K. Pyorala, M. Laakso, and J. Kuusisto
Insulin Resistance Syndrome Predicts Coronary Heart Disease Events in Elderly Nondiabetic Men
Circulation, July 13, 1999; 100(2): 123 - 128.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
E. Bonora, G. Targher, M. Alberiche, R. C. Bonadonna, F. Saggiani, M. B. Zenere, S. Uleri, and M. Muggeo
Effect of Chronic Treatment with Lacidipine or Lisinopril on Intracellular Partitioning of Glucose Metabolism in Type 2 Diabetes Mellitus
J. Clin. Endocrinol. Metab., May 1, 1999; 84(5): 1544 - 1550.
[Abstract] [Full Text]

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 Arterioscler. Thromb. Vasc. Bio.Home page
A. Festa, R. D'Agostino Jr, L. Mykkanen, R. P. Tracy, D. J. Zaccaro, C. N. Hales, and S. M. Haffner
Relative Contribution of Insulin and Its Precursors to Fibrinogen and PAI-1 in a Large Population With Different States of Glucose Tolerance : The Insulin Resistance Atherosclerosis Study (IRAS)
Arterioscler. Thromb. Vasc. Biol., March 1, 1999; 19(3): 562 - 568.
[Abstract] [Full Text] [PDF]

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 StrokeHome page
S. Soderberg, B. Ahren, B. Stegmayr, O. Johnson, P.-G. Wiklund, L. Weinehall, G. Hallmans, and T. Olsson
Leptin Is a Risk Marker for First-Ever Hemorrhagic Stroke in a Population-Based Cohort
Stroke, February 1, 1999; 30(2): 328 - 337.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
Y. Hong, T. Rice, J. Gagnon, J.-P. Després, A. Nadeau, L. Pérusse, C. Bouchard, A. S. Leon, J. S. Skinner, J. H. Wilmore, et al.
Familial Clustering of Insulin and Abdominal Visceral Fat: The HERITAGE Family Study
J. Clin. Endocrinol. Metab., December 1, 1998; 83(12): 4239 - 4245.
[Abstract] [Full Text]

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 J. Clin. Endocrinol. Metab.Home page
R. A. Phillips, L. R. Krakoff, A. Dunaif, D. T. Finegood, R. Gorlin, and S. Shimabukuro
Relation among Left Ventricular Mass, Insulin Resistance, and Blood Pressure in Nonobese Subjects
J. Clin. Endocrinol. Metab., December 1, 1998; 83(12): 4284 - 4288.
[Abstract] [Full Text]

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 Arterioscler. Thromb. Vasc. Bio.Home page
L. Karjalainen, J. Pihlajamaki, P. Karhapaa, and M. Laakso
Impaired Insulin-Stimulated Glucose Oxidation and Free Fatty Acid Suppression in Patients with Familial Combined Hyperlipidemia : A Precursor Defect for Dyslipidemia?
Arterioscler. Thromb. Vasc. Biol., October 1, 1998; 18(10): 1548 - 1553.
[Abstract] [Full Text] [PDF]


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