Cardiovascular Risk Factors in Confirmed Prediabetic Individuals: Does the Clock for Coronary Heart Disease Start Ticking Before the Onset of Clinical Diabetes?

Haffner, Steven M.

doi:10.1001/jama.1990.03440210043030

Cited by 674Diabetes, Cardiovascular Risks, and LipoproteinsDiabetes Management and ResearchCardiovascular Function and Risk Factors

Cardiovascular Risk Factors in Confirmed Prediabetic Individuals: Does the Clock for Coronary Heart Disease Start Ticking Before the Onset of Clinical Diabetes?

Haffner, Steven M.·1990·JAMA

DOI 10.1001/jama.1990.03440210043030

Open this paper in CoChat — free account

Abstract

Although type II diabetes is associated with both microvascular and macrovascular complications, duration of diabetes and severity of glycemia are strongly associated only with the former. Since prediabetic individuals are hyperinsulinemic, and since hyperinsulinemia may be a cardiovascular risk factor, we hypothesized that prediabetic individuals might have an atherogenic pattern of risk factors even before the onset of clinical diabetes, thereby explaining the relative lack of an association of macrovascular complications with either glycemic severity or disease duration. We documented the cardiovascular risk factor status of 614 initially nondiabetic Mexican Americans who later participated in an 8-year follow-up of the San Antonio Heart Study, a population-based study of diabetes and cardiovascular disease. Individuals who were nondiabetic at the time of baseline examination, but who subsequently developed type II diabetes (ie, confirmed prediabetic subjects, n = 43), had higher levels of total and lowdensity lipoprotein cholesterol, triglyceride, fasting glucose and insulin, 2-hour glucose, body mass index, and blood pressure, and lower levels of high-density lipoprotein cholesterol than subjects who remained nondiabetic (n = 571). Most of these differences persisted after adjustment for obesity and/or level of glycemia, but were abolished after adjustment for fasting insulin concentration. When subjects with impaired glucose tolerance at baseline (n = 106) were eliminated, the more atherogenic pattern of cardiovascular risk factors was still evident (and statistically significant) among initially normoglycemic prediabetic subjects. These results indicate that prediabetic subjects have an atherogenic pattern of risk factors (possibly caused by obesity, hyperglycemia, and especially hyperinsulinemia), which may be present for many years and may contribute to the risk of macrovascular disease as much as the duration of clinical diabetes itself. (JAMA. 1990;263:2893-2898)

Integrity signals

Registry

Crossref · 10.1001/jama.1990.03440210043030

Cites

0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

The risk of progressing from prediabetes to overt type 2 diabetes is greatest for people with a history of gestational diabetes, a strong family history of type 2 diabetes, progressive increments in glycemia within the prediabetes range, and who meet criteria for a combination of impaired fasting glucose, impaired glucose tolerance, or metabolic syndrome (any 2 out of 3).
“The risk of progressing from prediabetes to overt T2D are greatest for those persons with a history of GDM, strong family history of T2D, progressive increments in glycemia within the prediabetes range, and who meet criteria for a combination of IFG, IGT, or metabolic syndrome (any 2 out of 3).9,805,806”
From American Association of Clinical Endocrinology Clinical Practice Guideline: Developing a Diabetes Mellitus Comprehensive Care Plan-2022 Update. (2022) · cites this paper as [805]
Elevated TG and insulin resistance may both impair HDL function and predate the development of diabetes.
“In this regard, elevated TG and insulin resistance may both impair HDL function37-39 and predate the development of diabetes.40”
From Is Isolated Low High-Density Lipoprotein Cholesterol a Cardiovascular Disease Risk Factor?: New Insights From the Framingham Offspring Study (2016) · cites this paper as [40]
High triglyceride levels that accompany either normal or impaired fasting glucose predict the development of T2DM.
“High triglyceride levels that accompany either normal or impaired fasting glucose predict the development of T2DM, 166,167 and therefore, hypertriglyceridemic states should prompt surveillance to rule out T2DM.”
From Triglycerides and Cardiovascular Disease: A Scientific Statement From the American Heart Association (2011) · cites this paper as [166]

The publisher hasn’t deposited this paper’s reference list.

Sorted by citations

Global and societal implications of the diabetes epidemic
Zimmet, P., Alberti, K. G. M. M., & Shaw, J. (2001) · Nature · doi:10.1038/414782a · Cited by 5,883 · see citing works
Follow-up report on the diagnosis of diabetes mellitus
The Expert Committee on the Diagnosis and Classification of Diabetes Mellitus* (2003) · Diabetes Care · doi:10.2337/diacare.26.11.3160 · Cited by 3,784 · see citing works
Triglycerides and Cardiovascular Disease: A Scientific Statement From the American Heart Association
Miller, M., Stone, N. J., Ballantyne, C., Bittner, V., Criqui, M. H., Ginsberg, H. N., Goldberg, A. C., Howard, W. J., Jacobson, M. S., Kris-Etherton, P. M., et al. (2011) · Circulation · doi:10.1161/cir.0b013e3182160726 · Cited by 1,871 · see citing works
Prevalence of impaired glucose tolerance among children and adolescents with marked obesity
Sinha, R., Fisch, G., Teague, B., Tamborlane, W. V., Banyas, B., Allen, K., Savoye, M., Rieger, V., Taksali, S., Barbetta, G., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa012578 · Cited by 1,709 · see citing works
Acarbose Treatment and the Risk of Cardiovascular Disease and Hypertension in Patients With Impaired Glucose Tolerance: The STOP-NIDDM Trial
Chiasson, J.-L., Josse, R. G., Gomis, R., Hanefeld, M., Karasik, A., Laakso, M., & for The STOP-NIDDM Trial Research Group (2003) · JAMA · doi:10.1001/jama.290.4.486 · Cited by 1,624 · see citing works
Diabetes and Cardiovascular Disease: A Statement for Healthcare Professionals From the American Heart Association
Grundy, S. M., Benjamin, I. J., Burke, G. L., Chait, A., Eckel, R. H., Howard, B. V., Mitch, W., Smith, S. C., & Sowers, J. R. (1999) · Circulation · doi:10.1161/01.cir.100.10.1134 · Cited by 2,698 · see citing works
Is Oxidative Stress the Pathogenic Mechanism Underlying Insulin Resistance, Diabetes, and Cardiovascular Disease? The Common Soil Hypothesis Revisited
Ceriello, A., & Motz, E. (2004) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/01.atv.0000122852.22604.78 · Cited by 1,378 · see citing works
Adipokines: molecular links between obesity and atheroslcerosis
Lau, D., Dhillon, B., Yan, H., Szmitko, P. E., & Verma, S. (2005) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01058.2004 · Cited by 930 · see citing works
Pravastatin and the Development of Diabetes Mellitus: Evidence for a Protective Treatment Effect in the West of Scotland Coronary Prevention Study
Freeman, D. J., Norrie, J., Sattar, N., Neely, R. D. G., Cobbe, S. M., Ford, I., Isles, C., Lorimer, A. R., Macfarlane, P. W., McKillop, J. H., et al. (2001) · Circulation · doi:10.1161/01.cir.103.3.357 · Cited by 844 · see citing works
Metabolic Syndrome: Connecting and Reconciling Cardiovascular and Diabetes Worlds
Grundy, S. M. (2006) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2005.11.046 · Cited by 679 · see citing works
Non–Insulin-Dependent Diabetes Mellitus and Fasting Glucose and Insulin Concentrations Are Associated With Arterial Stiffness Indexes
Salomaa, V. V., Riley, W. A., Kark, J. D., Nardo, C. J., & Folsom, A. R. (1995) · Circulation · doi:10.1161/01.cir.91.5.1432 · Cited by 580 · see citing works
Insulin Resistance and Atherosclerosis: Implications for Insulin-Sensitizing Agents
Di Pino, A., & DeFronzo, R. A. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00141 · Cited by 535 · see citing works
Arterial stiffness in diabetes and the metabolic syndrome: a pathway to cardiovascular disease
Stehouwer, C. D. A., Henry, R. M. A., & Ferreira, I. (2008) · Diabetologia · doi:10.1007/s00125-007-0918-3 · Cited by 560 · see citing works
Prospective study of risk factors for development of non-insulin dependent diabetes in middle aged British men
Perry, I. J., Wannamethee, S. G., Walker, M. K., Thomson, A. G., Whincup, P. H., & Shaper, A. G. (1995) · BMJ · doi:10.1136/bmj.310.6979.560 · Cited by 532 · see citing works
The metabolic syndrome: is this diagnosis necessary?
Reaven, G. (2006) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.6.1237 · Cited by 546 · see citing works
Adipose Tissue Macrophages Promote Myelopoiesis and Monocytosis in Obesity
Nagareddy, P. R., Kraakman, M. J., Masters, S. L., Stirzaker, R. A., Gorman, D. J., Grant, R. W., Dragoljevic, D., Hong, E. S., Abdel‐Latif, A., Smyth, S. S., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.03.029 · Cited by 510 · see citing works
American Association of Clinical Endocrinology Clinical Practice Guideline: Developing a Diabetes Mellitus Comprehensive Care Plan-2022 Update.
Blonde, L., Umpierrez, G. E., Reddy, S. S., McGill, J. B., Berga, S. L., Bush, M., Chandrasekaran, S., DeFronzo, R. A., Einhorn, D., Galindo, R. J., et al. (2022) · Endocrine Practice · doi:10.1016/j.eprac.2022.08.002 · Cited by 507 · see citing works
Insulin-Resistant Prediabetic Subjects Have More Atherogenic Risk Factors Than Insulin-Sensitive Prediabetic Subjects
Haffner, S. M., Mykkänen, L. M., Festa, A., Burke, J. P., & D, M. P. S. M. (2000) · Circulation · doi:10.1161/01.cir.101.9.975 · Cited by 454 · see citing works
Self-citation
High-Density Lipoprotein Modulates Glucose Metabolism in Patients With Type 2 Diabetes Mellitus
Drew, B. G., Duffy, S. J., Formosa, M. F., Natoli, A. K., Henstridge, D. C., Penfold, S. A., Thomas, W. G., Mukhamedova, N., de Courten, B., Forbes, J. M., et al. (2009) · Circulation · doi:10.1161/circulationaha.108.843219 · Cited by 443 · see citing works
Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk.
Folli, F. B., Kahn, C. R., Hansen, H. F., Bouchie, J. L., & Feener, E. P. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119752 · Cited by 424 · see citing works
Diabetes Dyslipidemia
Schofield, J. D., Liu, Y., Rao‐Balakrishna, P., Malik, R. A., & Soran, H. (2016) · Diabetes Therapy · doi:10.1007/s13300-016-0167-x · Cited by 430 · see citing works
Pathophysiology of impaired pulsatile insulin release
Bergsten, P. (2000) · Diabetes/Metabolism Research and Reviews · doi:10.1002/1520-7560(200005/06)16:3 · Cited by 69 · see citing works
Type 2 diabetes mellitus and cardiovascular disease: Genetic and epigenetic links
De Rosa, S., Arcidiacono, B., Chiefari, E., Brunetti, A., Indolfi, C., & Foti, D. P. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00002 · Cited by 369 · see citing works
Admission blood glucose level as risk indicator of death after myocardial infarction in patients with and without diabetes mellitus
Stranders, I., Diamant, M., van Gelder, R. E., Spruijt, H. J., Twisk, J. W. R., Heine, R. J., & Visser, F. C. (2004) · Archives of Internal Medicine · doi:10.1001/archinte.164.9.982 · Cited by 353 · see citing works
Coronary atherosclerosis in diabetes mellitus
Goraya, T., Leibson, C. L., Palumbo, P. J., Weston, S. A., Killian, J. M., Pfeifer, E. A., Jacobsen, S. J., Frye, R. L., & Roger, V. L. (2002) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)02065-x · Cited by 353 · see citing works
Increased blood–brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases
Hawkins, B. T., Lundeen, T. F., Norwood, K., Brooks, H. L., & Egleton, R. D. (2006) · Diabetologia · doi:10.1007/s00125-006-0485-z · Cited by 348 · see citing works
Effect of Insulin Resistance, Dyslipidemia, and Intra-abdominal Adiposity on the Development of Cardiovascular Disease and Diabetes Mellitus
Rader, D. J. (2007) · The American Journal of Medicine · doi:10.1016/j.amjmed.2007.01.003 · Cited by 345 · see citing works
Intensive Lifestyle Intervention or Metformin on Inflammation and Coagulation in Participants With Impaired Glucose Tolerance
The Diabetes Prevention Program Research Group (2005) · Diabetes · doi:10.2337/diabetes.54.5.1566 · Cited by 333 · see citing works
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
Diabetes Mellitus as a Risk Factor for Death From Stroke
Tuomilehto, J., Rastenytė, D., Jousilahti, P., Sarti, C., & Vartiainen, E. A. (1996) · Stroke · doi:10.1161/01.str.27.2.210 · Cited by 321 · see citing works
Assessment and Treatment of Cardiovascular Risk in Prediabetes: Impaired Glucose Tolerance and Impaired Fasting Glucose
DeFronzo, R. A., & Abdul‐Ghani, M. A. (2011) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2011.03.013 · Cited by 318 · see citing works
Insulin resistance is a cardiovascular risk factor in humans
Adeva‐Andany, M. M., Martínez‐Rodríguez, J., González-Lucán, M., Fernández‐Fernández, C., & Castro-Quintela, E. (2019) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2019.02.023 · Cited by 314 · see citing works
Dyslipidaemia
Durrington, P. N. (2003) · The Lancet · doi:10.1016/s0140-6736(03)14234-1 · Cited by 311 · see citing works
The emerging role of HDL in glucose metabolism
Drew, B. G., Rye, K.-A., Duffy, S. J., Barter, P., & Kingwell, B. A. (2012) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2011.235 · Cited by 307 · see citing works
Pathophysiological implications of insulin resistance on vascular endothelial function
Wheatcroft, S. B., Williams, I. L., Shah, A. M., & Kearney, M. T. (2003) · Diabetic Medicine · doi:10.1046/j.1464-5491.2003.00869.x · Cited by 307 · see citing works
Insulin resistance and risk for stroke
Kernan, W. N., Inzucchi, S. E., Viscoli, C. M., Brass, L. M., Bravata, D. M., & Horwitz, R. I. (2002) · Neurology · doi:10.1212/wnl.59.6.809 · Cited by 280 · see citing works
Genetic Risk Scores for Diabetes Diagnosis and Precision Medicine
Udler, M. S., McCarthy, M. I., Florez, J. C., & Mahajan, A. (2019) · Endocrine Reviews · doi:10.1210/er.2019-00088 · Cited by 302 · see citing works
Relation of Glycohemoglobin and Adiposity to Atherosclerosis in Youth
McGill, H. C., McMahan, C. A., Malcom, G. T., Oalmann, M. C., & Strong, J. P. (1995) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.15.4.431 · Cited by 296 · see citing works
Diabetes and atherosclerosis: is there a role for hyperglycemia?
Chait, A., & Bornfeldt, K. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800059-jlr200 · Cited by 292 · see citing works
Prediabetes and Cardiovascular Disease
Brannick, B., & Dagogo-Jack, S. (2018) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2017.10.001 · Cited by 293 · see citing works
Vascular dysfunction in diabetes mellitus
Feener, E. P., & King, G. L. (1997) · The Lancet · doi:10.1016/s0140-6736(97)90022-2 · Cited by 287 · see citing works
Dietary Fat Consumption and Health
Lichtenstein, A. H., Kennedy, E., Barrier, P., Danford, D. E., Ernst, N. D., Grundy, S. M., Leveille, G. A., Horn, L. V., Williams, C. L., & Booth, S. L. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1998.tb01728.x · Cited by 289 · see citing works
Preventing Cardiovascular Disease and Diabetes
Eckel, R. H., Kahn, R., Robertson, R. M., & Rizza, R. A. (2006) · Circulation · doi:10.1161/circulationaha.106.176583 · Cited by 288 · see citing works
Prevalence of coronary artery disease in Asian Indians
Enas, E. A., Yusuf, S., & Mehta, J. L. (1992) · The American Journal of Cardiology · doi:10.1016/0002-9149(92)90744-j · Cited by 285 · see citing works
Novel Insights into the Pathogenesis and Management of the Metabolic Syndrome
Wang, H. H., Lee, D. K., Liu, M., Portincasa, P., & Wang, D. Q. ‐. (2020) · Pediatric Gastroenterology Hepatology & Nutrition · doi:10.5223/pghn.2020.23.3.189 · Cited by 294 · see citing works
Coronary heart disease in individuals with spinal cord injury: assessment of risk factors
Bauman, W. A., & Spungen, A. M. (2008) · Spinal Cord · doi:10.1038/sj.sc.3102161 · Cited by 279 · see citing works
Insulin resistance, inflammation, and the prediabetic state
Haffner, S. M. (2003) · The American Journal of Cardiology · doi:10.1016/s0002-9149(03)00612-x · Cited by 268 · see citing works
Self-citation
The epidemiology of cardiovascular disease in type 2 diabetes mellitus: how sweet it is … or is it?
Nathan, D. M., Meigs, J. B., & Singer, D. E. (1997) · The Lancet · doi:10.1016/s0140-6736(97)90021-0 · Cited by 264 · see citing works
Nuclear Magnetic Resonance Lipoprotein Abnormalities in Prediabetic Subjects in the Insulin Resistance Atherosclerosis Study
Festa, A., Williams, K., Hanley, A. J., Otvos, J. D., Goff, D. C., Wagenknecht, L. E., & Haffner, S. M. (2005) · Circulation · doi:10.1161/circulationaha.104.512079 · Cited by 259 · see citing works
Self-citation
Impact of glucose-lowering drugs on cardiovascular disease in type 2 diabetes
Ferrannini, E., & DeFronzo, R. A. (2015) · European Heart Journal · doi:10.1093/eurheartj/ehv239 · Cited by 256 · see citing works
Persistent Elevation of Plasma Insulin Levels Is Associated With Increased Cardiovascular Risk in Children and Young Adults
Bao, W., Srinivasan, S. R., & Berenson, G. S. (1996) · Circulation · doi:10.1161/01.cir.93.1.54 · Cited by 256 · see citing works
Molecular mechanisms of chromium in alleviating insulin resistance
Hua, Y., Clark, S., Ren, J. T., & Sreejayan, N. (2012) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2011.11.001 · Cited by 258 · 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
Asian Americans have greater prevalence of metabolic syndrome despite lower body mass index
Palaniappan, L. P., Wong, E. C., Shin, J., Fortmann, S. P., & Lauderdale, D. S. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.152 · Cited by 238 · see citing works
Etiology of the Metabolic Syndrome: Potential Role of Insulin Resistance, Leptin Resistance, and Other Players
Zimmet, P., Boyko, E. J., Collier, G. R., & de Courten, M. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb07783.x · Cited by 233 · see citing works
Inflammation in the Prediabetic State Is Related to Increased Insulin Resistance Rather Than Decreased Insulin Secretion
Festa, A., Hanley, A. J., Tracy, R. P., D’Agostino, R., & Haffner, S. M. (2003) · Circulation · doi:10.1161/01.cir.0000091339.70120.53 · Cited by 231 · see citing works
Self-citation
Metabolic Changes in Persons After Spinal Cord Injury
Bauman, W. A., & Spungen, A. M. (2000) · Physical Medicine and Rehabilitation Clinics of North America · doi:10.1016/s1047-9651(18)30150-5 · Cited by 229 · see citing works
Insulin Resistance Implications for Type II Diabetes Mellitus and Coronary Heart Disease
Haffner, S. M., & Miettinen, H. (1997) · The American Journal of Medicine · doi:10.1016/s0002-9343(97)00027-2 · Cited by 227 · see citing works
Self-citation
Screening Adults for Type 2 Diabetes: A Review of the Evidence for the U.S. Preventive Services Task Force
Norris, S. L., Kansagara, D. L., Bougatsos, C., & Fu, R. F. (2008) · Annals of Internal Medicine · doi:10.7326/0003-4819-148-11-200806030-00008 · Cited by 226 · see citing works
Epidemiology of Diabetes
Winer, N., & Sowers, J. R. (2004) · The Journal of Clinical Pharmacology · doi:10.1177/0091270004263017 · Cited by 224 · see citing works
Impaired glucose metabolism predicts mortality after a myocardial infarction
Bolk, J. H., van der Ploeg, T., Cornel, J. H., Arnold, A. E. R., Sepers, J. M., & Umans, V. A. W. M. (2001) · International Journal of Cardiology · doi:10.1016/s0167-5273(01)00422-3 · Cited by 215 · see citing works
Associations between plant-based dietary patterns and risks of type 2 diabetes, cardiovascular disease, cancer, and mortality – a systematic review and meta-analysis
Wang, Y., Liu, B., Han, H., Hu, Y., Zhu, L., Rimm, E. B., Hu, F. B., & Sun, Q. (2023) · Nutrition Journal · doi:10.1186/s12937-023-00877-2 · Cited by 220 · see citing works
The role and function of HDL in patients with diabetes mellitus and the related cardiovascular risk
Femlak, M., Gluba-Brzózka, A., Ciałkowska-Rysz, A. D., & Rysz, J. (2017) · Lipids in Health and Disease · doi:10.1186/s12944-017-0594-3 · Cited by 222 · see citing works
Preventing Type 2 diabetes and the dysmetabolic syndrome in the real world: a realistic view
Zimmet, P., Shaw, J. E., & Alberti, K. G. M. M. (2003) · Diabetic Medicine · doi:10.1046/j.1464-5491.2003.01052.x · Cited by 207 · see citing works
Cardiovascular disease risk factors as predictors of Type 2 (non-insulin-dependent) diabetes mellitus in elderly subjects
Mykkänen, L. M., Kuusisto, J., Pyörälà, K., & Laakso, M. (1993) · Diabetologia · doi:10.1007/bf02743273 · Cited by 206 · see citing works
Metabolic risks identified by the combination of enlarged waist and elevated triacylglycerol concentration
Kahn, H. S., & Valdez, R. A. (2003) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/78.5.928 · Cited by 203 · see citing works
Obesity, metabolic syndrome, and type 2 diabetes: emerging epidemics and their cardiovascular implications
Mensah, G. A., Mokdad, A. H., Ford, E. S., Narayan, K. M. V., Giles, W. H., Vinicor, F., & DEEDWANIA, P. C. (2004) · Cardiology Clinics · doi:10.1016/j.ccl.2004.06.005 · Cited by 202 · see citing works
Validation of the Finnish diabetes risk score (FINDRISC) questionnaire for screening for undiagnosed type 2 diabetes, dysglycaemia and the metabolic syndrome in Greece
Makrilakis, K., Liatis, S., Grammatikou, S., Perrea, D., Stathi, C., Tsiligros, P., & Katsilambros, N. (2011) · Diabetes & Metabolism · doi:10.1016/j.diabet.2010.09.006 · Cited by 199 · see citing works
The Importance of Hyperglycemia in the Nonfasting State to the Development of Cardiovascular Disease
Haffner, S. M. (1998) · Endocrine Reviews · doi:10.1210/edrv.19.5.0343 · Cited by 193 · see citing works
Self-citation
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
PPARγ and Atherosclerosis
Hsueh, W. A., & Law, R. E. (2001) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/hq1201.100261 · Cited by 191 · see citing works
Type II diabetes mellitus and impaired glucose regulation in Caucasian children and adolescents with obesity living in Germany
Wabitsch, M., Hauner, H., Hertrampf, M., Muche, R., Hay, B., Mayer, H. G., Kratzer, W., Debatin, K.-M., & Heinze, E. (2004) · International Journal of Obesity · doi:10.1038/sj.ijo.0802555 · Cited by 188 · see citing works
Microalbuminuria in essential hypertension: Significance, pathophysiology, and therapeutic implications
Bianchi, S., Bigazzi, R., & Campese, V. M. (1999) · American Journal of Kidney Diseases · doi:10.1016/s0272-6386(99)70002-8 · Cited by 185 · see citing works
Insulin and Insulin-Like Growth Factor in Normal and Pathological Cardiovascular Physiology
Sowers, J. R. (1997) · Hypertension · doi:10.1161/01.hyp.29.3.691 · Cited by 184 · see citing works
Screening for Type 2 Diabetes Mellitus in Adults: U.S. Preventive Services Task Force Recommendation Statement
U.S. Preventive Services Task Force* (2008) · Annals of Internal Medicine · doi:10.7326/0003-4819-148-11-200806030-00007 · Cited by 184 · see citing works
RELATIONSHIP BETWEEN BMI, TOTAL TESTOSTERONE, SEX HORMONE-BINDING-GLOBULIN, LEPTIN, INSULIN AND INSULIN RESISTANCE IN OBESE MEN
Osuna C., J. A., Gómez-Pérez, R., Arata-Bellabarba, G., & Villaroel, V. (2006) · Archives of Andrology · doi:10.1080/01485010600692017 · Cited by 183 · see citing works
Insulin resistance, compensatory hyperinsulinaemia, and coronary heart disease
Reaven, G. M., & Laws, A. (1994) · Diabetologia · doi:10.1007/bf00400953 · Cited by 179 · see citing works
Diabetes Mellitus
Kuller, L. H., Velentgas, P., Barzilay, J. I., Beauchamp, N. J., O’Leary, D. H., & Savage, P. J. (2000) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.20.3.823 · Cited by 181 · see citing works
Prevalence of coronary heart disease and carotid arterial thickening in patients with the metabolic syndrome (The ARIC Study)
McNeill, A. M., Rosamond, W. D., Girman, C. J., Heiss, G., Golden, S. H., Duncan, B. B., East, H. E., & Ballantyne, C. (2004) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2004.07.107 · Cited by 177 · see citing works
The Look AHEAD Trial: a review and discussion of its outcomes
Pi-Sunyer, X. (2014) · Current Nutrition Reports · doi:10.1007/s13668-014-0099-x · Cited by 176 · see citing works
The epidemiology of impaired glucose tolerance and hypertension
Kannel, W. B., Wilson, P. W. F., & Zhang, T. (1991) · American Heart Journal · doi:10.1016/0002-8703(91)90432-h · Cited by 178 · see citing works
Obesity, Peroxisome Proliferator-Activated Receptor, and Atherosclerosis in Type 2 Diabetes
Blaschke, F., Takata, Y., Caglayan, E., Law, R. E., & Hsueh, W. A. (2006) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000191663.12164.77 · Cited by 176 · see citing works
Exenatide suppresses postprandial elevations in lipids and lipoproteins in individuals with impaired glucose tolerance and recent onset type 2 diabetes mellitus
Schwartz, E. A., Koska, J., Mullin, M. P., Syoufi, I., Schwenke, D. C., & Reaven, P. D. (2010) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2010.05.028 · Cited by 173 · see citing works
Diabetes and Progression of Carotid Atherosclerosis
Wagenknecht, L. E., Zaccaro, D. J., Espeland, M. A., Karter, A. J., O’Leary, D. H., & Haffner, S. M. (2003) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000072273.67342.6d · Cited by 172 · see citing works
Self-citation
The insulin resistance syndrome: physiological considerations
Kashyap, S. R., & DeFronzo, R. A. (2007) · Diabetes and Vascular Disease Research · doi:10.3132/dvdr.2007.001 · Cited by 172 · see citing works
Nontraditional Risk Factors for Cardiovascular Disease in Diabetes
Fonseca, V. A., Desouza, C. V., Asnani, S., & Jialal, I. (2004) · Endocrine Reviews · doi:10.1210/er.2002-0034 · Cited by 165 · see citing works
Relationship between Serum Lipoprotein Ratios and Insulin Resistance in Obesity
Brehm, A., Pfeiler, G., Pacini, G., Vierhapper, H., & Roden, M. (2004) · Clinical Chemistry · doi:10.1373/clinchem.2004.037556 · Cited by 169 · see citing works
Prospective Study of Small LDLs as a Risk Factor for Non–Insulin Dependent Diabetes Mellitus in Elderly Men and Women
Austin, M. A., Mykkänen, L. M., Kuusisto, J., Edwards, K. L., Nelson, C., Haffner, S. M., Pyörälà, K., & Laakso, M. (1995) · Circulation · doi:10.1161/01.cir.92.7.1770 · Cited by 164 · see citing works
Self-citation
Liver‐Fat Accumulation and Insulin Resistance in Obese Women with Previous Gestational Diabetes
Tiikkainen, M., Tamminen, M., Häkkinen, A., Bergholm, R., Vehkavaara, S., Halavaara, J. T., Teramo, K., Rissanen, A., & Yki‐Järvinen, H. (2002) · Obesity Research · doi:10.1038/oby.2002.118 · Cited by 161 · see citing works
Comparison of carotid intima-media thickness, arterial stiffness, and brachial artery flow mediated dilatation in diabetic and nondiabetic subjects (The Chennai Urban Population Study [CUPS-9])
Ravikumar, R., Deepa, R., Shanthirani, C. S., & Mohan, V. (2002) · The American Journal of Cardiology · doi:10.1016/s0002-9149(02)02593-6 · Cited by 161 · see citing works
Evolving Trends in the Epidemiology, Risk Factors, and Prevention of Type 2 Diabetes: A Review
Weisman, A., Fazli, G. S., Johns, A., & Booth, G. L. (2018) · Canadian Journal of Cardiology · doi:10.1016/j.cjca.2018.03.002 · Cited by 161 · see citing works
Impaired glucose tolerance and impaired fasting glucose — a review of diagnosis, clinical implications and management
Petersen, J. L., & McGuire, D. K. (2005) · Diabetes and Vascular Disease Research · doi:10.3132/dvdr.2005.007 · Cited by 159 · see citing works
Diabetes mellitus, race, and socioeconomic status a population-based study
Brancati, F. L., Whelton, P. K., Kuller, L. H., & Klag, M. J. (1996) · Annals of Epidemiology · doi:10.1016/1047-2797(95)00095-x · Cited by 159 · see citing works
Metabolic Syndrome and Risk of Cardiovascular Events After Myocardial Infarction
Levantesi, G., Macchia, A., Marfisi, R., Franzosi, M. G., Maggioni, A. P., Nicolosi, G. L., Schweiger, C., Tavazzi, L., Tognoni, G., Valagussa, F., et al. (2005) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2005.03.062 · Cited by 157 · see citing works
The changing face of macrovascular disease in non-insulin-dependent diabetes mellitus: an epidemic in progress
Zimmet, P., & Alberti, K. (1997) · The Lancet · doi:10.1016/s0140-6736(97)90020-9 · Cited by 156 · see citing works
The role of interleukin-18 in the metabolic syndrome
Trøseid, M., Seljeflot, I., & Arnesen, H. (2010) · Cardiovascular Diabetology · doi:10.1186/1475-2840-9-11 · Cited by 155 · see citing works
Risk for Diabetes Mellitus in Middle-Aged Caucasian Male Participants of the PROCAM Study: Implications for the Definition of Impaired Fasting Glucose by the American Diabetes Association
von Eckardstein, A., Schulte, H., & Assmann, G. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.9.6773 · Cited by 154 · see citing works
Diabetic dyslipidemia
Kreisberg, R. A. (1998) · The American Journal of Cardiology · doi:10.1016/s0002-9149(98)00848-0 · Cited by 154 · see citing works
A Major Locus for Fasting Insulin Concentrations and Insulin Resistance on Chromosome 6q with Strong Pleiotropic Effects on Obesity-Related Phenotypes in Nondiabetic Mexican Americans
Duggirala, R., Blangero, J., Almasy, L. A., Arya, R., Dyer, T. D., Williams, K. L., Leach, R. J., O'Connell, P., & D, M. P. S. M. (2001) · The American Journal of Human Genetics · doi:10.1086/320100 · Cited by 149 · see citing works
THE NATURAL HISTORY OF TYPE 2 DIABETES
Ramlo-Halsted, B. A., & Edelman, S. V. (1999) · Primary Care Clinics in Office Practice · doi:10.1016/s0095-4543(05)70130-5 · Cited by 150 · see citing works

Cardiovascular risk factors in confirmed prediabetic individuals. Haffner S M, Stern M P, Hazuda H P, et al. JAMA, 1990; 263: 2893–8
Shaw, K. M. (1990) · Practical Diabetes · doi:10.1002/pdi.1960070612
Cardiovascular Risk Factors in Patients With Prediabetes and its Relationship With Metabolic Syndrome
Topaloğlu, U. S. (2020) · Koşuyolu Heart Journal · doi:10.51645/khj.20075
The prediabetic problem: Development of non-insulin-dependent diabetes mellitus and related abnormalities
Haffner, S. M. (1997) · Journal of Diabetes and its Complications · doi:10.1016/s1056-8727(96)00099-2 · Cited by 31 · see citing works
Self-citation
Parental history of diabetes is associated with increased cardiovascular risk factors.
Haffner, S. M., Stern, M. P., Hazuda, H. P., Mitchell, B. D., Patterson, J. K., & Ferrannini, E. (1989) · Arteriosclerosis An Official Journal of the American Heart Association Inc · doi:10.1161/01.atv.9.6.928 · Cited by 88 · see citing works
Self-citation
Insulin resistance: The linchpin between prediabetes and cardiovascular disease
Salazar, M. R., Carbajal, H. A., Espeche, W. G., Aizpurúa, M., Sisnieguez, C. E. L., Sisnieguez, B. C. L., Stavile, R. N., March, C. E., & Reaven, G. M. (2016) · Diabetes and Vascular Disease Research · doi:10.1177/1479164115610057 · Cited by 27 · see citing works

Authors: Haffner, S. M.
Corresponding author: Haffner, Steven M.
Venue: JAMA
Publisher: American Medical Association (AMA)
Published: 1990-06-06
Volume: 263
Issue: 21
Pages: 2893
ISSN: 0002-9955 (ISSN-L)
0098-7484
DOI: 10.1001/jama.1990.03440210043030
OpenAlex: W4297681290
Cited by: 668
References: 0
Citations by year: 2026: 3 · 2025: 9 · 2024: 14 · 2023: 9 · 2022: 18 · 2021: 12 · 2020: 23 · 2019: 15 · 2018: 16 · 2017: 14 · 2016: 17 · 2015: 25 · 2014: 21 · 2013: 16 · 2012: 22
FWCI: 6.93
Type: journal article
Language: en
Open access: closed
Locations: JAMA (publishedVersion)
Topics: Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Function and Risk Factors
Keywords: prediabetes, type 2 diabetes, cardiovascular risk factors, hyperinsulinemia, atherogenic lipid profile, impaired glucose tolerance, macrovascular complications, Mexican Americans, San Antonio Heart Study, fasting insulin, obesity, disease duration

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Cardiovascular Risk Factors in Confirmed Prediabetic Individuals: Does the Clock for Coronary Heart Disease Start Ticking Before the Onset of Clinical Diabetes?

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks