The metabolic syndrome or the insulin resistance syndrome? Different names, different concepts, and different goals

Endocrinology and Metabolism Clinics of North America

Volumn 33, Issue 2, 2004, Pages 283-303

  Reaven, Gerald ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

C REACTIVE PROTEIN; CELL ADHESION MOLECULE; FIBRINOGEN; GEMFIBROZIL; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LOW DENSITY LIPOPROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; TESTOSTERONE; TRIACYLGLYCEROL; URIC ACID;

ADIPOSE TISSUE; ATHEROGENESIS; BLOOD PRESSURE; BODY MASS; BREAST CANCER; CARDIOVASCULAR DISEASE; COLORECTAL CANCER; DIAGNOSTIC APPROACH ROUTE; DIASTOLIC BLOOD PRESSURE; DYSLIPIDEMIA; ELECTROCARDIOGRAPHY MONITORING; ENDOTHELIUM CELL; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; HEALTH SERVICE; HEIGHT; HUMAN; HYPERGLYCEMIA; HYPERTENSION; HYPERTRIGLYCERIDEMIA; INSULIN RESISTANCE; LIPID METABOLISM; LIVER DISEASE; MENSTRUAL CYCLE; METABOLIC SYNDROME X; MUSCLE; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; OVARY POLYCYSTIC DISEASE; PEDAGOGICS; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; RISK FACTOR; SLEEP APNEA SYNDROME; SODIUM RETENTION; SYSTOLIC BLOOD PRESSURE; TESTOSTERONE RELEASE; URIC ACID BLOOD LEVEL; WEIGHT;

HUMANS; INSULIN RESISTANCE; METABOLIC SYNDROME X;

EID: 2542424815     PISSN: 08898529     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecl.2004.03.002     Document Type: Review

References (98)

1. Yeni-Komshian H., Carantoni M., Abbasi F., Reaven G.M. Relationship between several surrogate estimates of insulin resistance and quantification of insulin-mediated glucose disposal in 490 healthy, nondiabetic volunteers. Diabetes Care. 23:2000;171-175
2. Lillioja S., Mott D.M., Spraul M., et al. Insulin resistance and insulin secretory dysfunction as precursors of non-insulin dependent diabetes mellitus. N Engl J Med. 329:1993;1988-1992
3. Warram J.H., Martin B.C., Krowlewski A.S., et al. Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the off-spring of the diabetic parents. Ann Intern Med. 113:1990;909
4. Reaven G.M. Role of insulin resistance in human disease. Diabetes. 37:1988;1595-1607
5. Executive summary of the third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA. 285:2002;2846-2897
6. Skott P., Vaag A., Bruum N.E., Hother-Nielsen O., Gall M.-A., Beck-Nielsen H., et al. Effect of insulin on renal sodium handling in hyperinsulinemic type 2 (non-insulin-dependent) diabetic patients with peripheral insulin resistance. Diabetologia. 34:1991;275-281
7. Facchini F.S., Riccardo A., Stoohs A., Reaven G.M. Enhanced sympathetic nervous system activity: the linchpin between insulin resistance, hyperinsulinemia, and heart rate. Am J Hypertens. 9:1996;1013-1017
8. Reaven G.M. The kidney: an unwilling accomplice in syndrome X. Am J Kidney Dis. 30:1997;928-931
9. Shen S.-W., Reaven G.M., Farquhar J.W. Comparison of impedance to insulin mediated glucose uptake in normal and diabetic subjects. J Clin Invest. 49:1970;2151-2160
10. Ginsberg H., Kimmerling G., Olefsky J.M., Reaven G.M. Demonstration of insulin resistance in untreated adult onset diabetic subjects with fasting hyperglycemia. J Clin Invest. 55:1975;454-461
11. Reaven G.M. The fourth musketeer: from Alexander Dumas to Claude Bernard. Diabetologia. 38:1995;3-13
12. Pyorala K. Relationship of glucose tolerance and plasma insulin to the incidence of coronary heart disease: results from two population studies in Finland. Diabetes Care. 2:1979;131-141
13. Ducimetiere P., Eschwege E., Papoz L., et al. Relationship of plasma insulin levels to the incidence of myocardial infarction and coronary heart disease mortality in a middle-aged population. Diabetologia. 19:1980;205
14. Després J.-P., Lamarche B., Mauriége P., et al. Hyperinsulinemia as an independent risk factor for ischemic heart disease. N Engl J Med. 334:1996;952-957
15. Yip J., Facchini F.S., Reaven G.M. Resistance to insulin-mediated glucose disposal as a predictor of cardiovascular disease. J Clin Endocrinol Metab. 83:1998;2773-2776
16. Facchini F.S., Hua N., Abbasi F., Reaven G.M. Insulin resistance as a predictor of age-related diseases. J Clin Endocrinol Metab. 86:2001;3574-3578
17. Reaven G.M., Lerner R., Stern M., Farquhar J.W. Role of insulin in endogenous hypertriglyceridemia. J Clin Invest. 46:1967;1756-1767
18. Olefsky J.M., Farquhar J.W., Reaven G.M. Reappraisal of the role of insulin in hypertriglyceridemia. Am J Med. 57:1974;551-560
19. Abbasi F., McLaughlin T., Lamendola C., Reaven G.M. The relationship between glucose disposal in response to physiological hyperinsulinemia and basal glucose and free fatty acid concentrations in healthy volunteers. J Clin Endocrinol Metab. 85:2000;1251-1254
20. Laws A., Reaven G.M. Evidence for an independent relationship between insulin resistance and fasting plasma HDL-cholesterol, triglyceride and insulin concentrations. J Intern Med. 231:1992;25-30
21. Reaven G.M., Chen Y.-D.I., Jeppesen J., Maheux P., Krauss R.M. Insulin resistance and hyperinsulinemia in individuals with small, dense, low density lipoprotein particles. J Clin Invest. 92:1993;141-146
22. Jeppesen J., Hollenbeck C.B., Zhou M.-Y., Coulston A.M., Jones C., Chen Y.-D.I., et al. Relation between insulin resistance, hyperinsulinemia, postheparin plasma lipoprotein lipase activity, and postprandial lipemia. Arterioscler Thromb Vasc Biol. 15:1995;320-324
23. Juhan-Vague I., Thompson S.G., Jeppesen J., on behalf of the ECAT Angina Pectoris Study Group. Involvement of the hemostatic system in the insulin resistance syndrome. Arterioscler Thromb. 13:1993;1865-1873
24. Meigs J.B., Mittelmann M.A., Nathan D.M., et al. Hyperinsulinemia, hyperglycemia, and impaired hemostasis: the Framingham offspring study. JAMA. 283:2000;221-228
25. Chen N.-G., Abbasi F., Lamendola C., McLaughlin T., Cooke J.P., Tsao P.S., et al. Mononuclear cell adherence to cultured endothelium is enhanced by hypertension and insulin resistance in healthy nondiabetic volunteers. Circulation. 100:1999;940-943
26. Chen N.-G., Holmes M., Reaven G.M. Relationship between insulin resistance, soluble adhesion molecules, and mononuclear cell binding in healthy volunteers. J Clin Endocrinol Metab. 84:1999;3485-3489
27. Stuhlinger M.C., Abbasi F., Chu J.W., Lamendola C., McLaughlin T.L., Cooke J.P., et al. Relationship between insulin resistance and an endogenous nitric oxide synthase inhibitor. JAMA. 287:2002;1420-1426
28. Baron A. Vascular reactivity. Am J Cardiol. 84:1999;25J-27J
29. McLaughlin T., Abbasi F., Lamendola C., Liang L., Reaven G., Schaaf P., et al. Differentiation between obesity and insulin resistance in the association with C-reactive protein. Circulation. 106:2002;2908-2912
30. Reaven G.M. Insulin resistance/compensatory hyperinsulinemia, essential hypertension, and cardiovascular disease. J Clin Endocrinol Metab. 88:2003;2399-2403
31. Ferrannini E., Buzzigoli G., Bonadona R. Insulin resistance in essential hypertension. N Engl J Med. 317:1987;350-357
32. Shen D.-C., Shieh S.-M., Fuh M., Wu D.-A., Chen Y.-D.I., Reaven G.M. Resistance to insulin-stimulated glucose uptake in patients with hypertension. J Clin Endocrinol Metab. 66:1988;580-583
33. Swislocki A.L.M., Hoffman B.B., Reaven G.M. Insulin resistance, glucose intolerance and hyperinsulinemia in patients with hypertension. Am J Hypertens. 2:1989;419-423
34. Ferrari P., Weidmann P., Shaw S., Giachino D., Riesen W., Allemann Y., et al. Altered insulin sensitivity, hyperinsulinemia and dyslipidemia in individuals with a hypertensive parent. Am J Med. 91:1991;589-596
35. Facchini F., Chen Y.-D.I., Clinkingbeard C., Jeppesen J., Reaven G.M. Insulin resistance, hyperinsulinemia, and dyslipidemia in nonobese individuals with a family history of hypertension. Am J Hypertens. 5:1992;694-699
36. Allemann Y., Horber F.F., Colombo M., Ferrari P., Shaw S., Jaeger P., et al. Insulin sensitivity and body fat distribution in normotensive offspring of hypertensive parents. Lancet. 341:1993;327-331
37. Skarfors E.T., Lithell H.O., Selinus I. Risk factors for the development of hypertension: a 10-year longitudinal study in middle-aged men. J Hypertens. 9:1991;217-223
38. Lissner L., Bengtsson C., Lapidus L., Kristjansson K., Wedel H. Fasting insulin in relation to subsequent blood pressure changes and hypertension in women. Hypertension. 20:1992;797-801
39. Taittonen L., Uhari M., Nuutinen M., Turtinen J., Pokka T., Akerblom H.K. Insulin and blood pressure among healthy children. Am J Hypertens. 9:1996;193-199
40. Raitakari O.T., Porkka K.V.K., Rönnemaa T., Knip M., Uhari M., Akerblom H.K., et al. The role of insulin in clustering of serum lipids and blood pressure in children and adolescents. Diabetologia. 38:1995;1042-1050
41. Zavaroni I., Mazza S., Dall'Aglio E., Gasparini P., Passeri M., Reaven G.M. Prevalence of hyperinsulinaemia in patients with high blood pressure. J Intern Med. 231:1992;235-240
42. Sheuh W.H.-H., Jeng C.-Y., Shieh S.-M., Fuh M.M., Shen D.D., Chen Y.-D.I., et al. Insulin resistance and abnormal electrocardiograms in patients with high blood pressure. Am J Hypertens. 5:1992;444-448
43. Jeppesen J., Hein H.O., Suadicani P., Gynelberg F. High triglycerides and low HDL cholesterol and blood pressure and risk of ischemic heart disease. Hypertension. 36:2000;226-239
44. Facchini F.S., DoNascimento C., Reaven G.M., Yip J.W., Ni P.X., Humphreys M.H. Blood pressure, sodium intake, insulin resistance, and urinary nitrate excretion. Hypertension. 33:1999;1008-1012
45. Sharma A.M., Schorr U., Distler A. Insulin resistance in young salt-sensitive normotensive subjects. Hypertension. 21:1993;273-279
46. Zavaroni I., Coruzzi P., Bonini L., Mossini G.L., Musiari L., Gasparini P., et al. Association between salt sensitivity and insulin concentrations in patients with hypertension. Am J Hypertens. 8:1995;855-858
47. Troisi R.J., Weiss S.T., Parker D.R., Sparrow D., Young J.B., Landsberg L. Relation of obesity, insulin, and sympathetic nervous system activity. Hypertension. 17:1991;669-677
48. Facchini F.S., Riccardo A., Stoohs A., Reaven G.M. Enhanced sympathetic nervous system activity: the linchpin between insulin resistance, hyperinsulinemia, and heart rate. Am J Hypertens. 9:1996;1013-1017
49. O'Hare J.A., Minaker K.L., Meneilly G.S., Rowe J.W., Palotta J.A., Young J.B. Effect of insulin on plasma norepinephrine and 3, 4 dihydroxyphenylalanine in obese men. Metabolism. 38:1989;322-329
50. Dunaiff A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev. 18:1997;774-800
51. Nestler J.E., Jakuboficz J., Evans W.S., Pasquali R. Effects of metformin on spontaneous and clomiphene-induced ovulation in the polycystic ovary syndrome. N Engl J Med. 338:1998;1876-1880
52. Reaven G.M. Effect of metformin on various aspects of glucose, insulin and lipid metabolism in patients with non-insulin-dependent diabetes mellitus with varying degrees of hyperglycemia. Diabetes Metab Rev. 11:1995;S97-S108
53. Dunaif A., Segal K.R., Futterweit W., Dobrjansky A. Profound peripheral insulin resistance, independent of obesity, in the polycystic ovary syndrome. Diabetes. 38:1989;1165-1174
54. Sanyal A.J., Campbell-Sargent C., Mirashi F., Rizzo W.B., Contos M.J., Sterling R.K., et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 120:2001;1183-1192
55. Dixon J.B., Bhathal P.S., O'Brien P.E. Nonalcoholic fatty liver disease: predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 121:2001;91-100
56. Seppala-Lindros A., Vehkavaara S., Hakinen A.M., Gotto T., Westerbacka J., Soviharvi A., et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum fatty acids independent of obesity in normal men. J Clin Endocrinol Metab. 87:2002;3023-3028
57. Argiles J.M., Lopez-Soriano F.J. Insulin and cancer. Int J Oncol. 18:2001;683-687
58. Bruning P.F., Bonfret J.M.G., Van Nooyrd P.A.H., Hart A.A., De Jong-Bakker M., Noojen W.J. Insulin resistance and breast cancer risk. Int J Cancer. 52:1992;511-516
59. DelGiudice M.E., Fantus I.G., Ezzat S., McKeown-Eyssen G., Page D., et al. Insulin and related factors in premenopausal breast cancer risk. Breast Cancer Res Treat. 47:1998;111-120
60. Goodwin P.J., Ennis M., Pritchard K.I., Trudeau M.E., Koo J., Madamas Y., et al. Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol. 20:2001;42-51
61. Goodwin P.J., Boyd N.F., Hanna W., Hartwick W., Murray D., Qizilbash A., et al. Elevated levels of plasma triglycerides are associated with premenopausal breast cancer risk. Nutr Cancer. 27:1997;284-292
62. Glicksman A.S., Myers W.P.L., Rawson R.W. Diabetes mellitus and carbohydrate metabolism inpatients with cancer. Med Clin N Am. 40:1956;887-900
63. Goodwin P.J., Boyd N.F. Body size and breast cancer prognosis: a critical review. Breast Cancer Res Treat. 16:1990;205-214
64. La Vecchia C., Negri E., Decarli A., Frabceschi S. Diabetes mellitus and colorectal cancer risk. Cancer Epidemol Biomarkers Prev. 6:1997;1007-1010
65. Will J.C., Galuska D.A., Vinicor F., Calle E.E. Colorectal cancer: another complication of diabetes mellitus? Am J Epidemiol. 147:1998;816-825
66. Hu F.B., Manson J.E., Hunter D., Colditz G.A., Michaels K.B., Speizer F.E., et al. Prospective study of diabetes mellitus (type 2) and risk of colorectal cancer in women. J Natl Cancer Inst. 91:1999;542-547
67. Andersson S.O., Wolk A., Bergstrom R., Adami H.O., Engholm G., Englund A., et al. Body size and prostate cancer: a 20-year follow-up study among 135, 006 Swedish construction workers. J Natl Cancer Inst. 89:1997;386-389
68. Rodriguez C., Patel A.V., Calle E.E., Jacobs E.J., Chao A., Thun M.J. Body mass index, height, and prostate cancer mortality in two large cohorts of adult men in the United States. Cancer Epidemiol Biomarkers Prev. 10:2001;345-353
69. Moyad M.A. Is obesity a risk factor for prostate cancer, and does it even matter? A hypothesis and different perspective. Urology. 59:(Suppl 4A):2002;41-50
70. Copeland G.P., Leinster S.J., Davis J.C., Hipkin L.J. Insulin resistance in patients with colorectal cancer. Br J Surg. 74:1987;1031-1035
71. Kaaks R., Toniolo P., Akhmedkhanov A., Lukanova A., Biessy C., Dechaud H., et al. Serum C-peptide, insulin-like growth factor (IGF)-I binding proteins, and colorectal cancer risk in women. J Natl Cancer Inst. 92:2000;1592-1600
72. Hsing A.W., Chua S. Jr., Gao Y.T., Gentzcheim E., Chang L., Deng J., et al. Prostate cancer risk and serum levels of insulin and leptin: a population-based study. J Natl Cancer Inst. 93:2001;783-789
73. Lehrer S., Diamond E.J., Stagger S., Stone N.N., Stock R.G. Serum insulin level, disease stage, prostate specific antigen (PSA) and Gleason score in prostate cancer. Br J Cancer. 23:2002;726-728
74. Balkau B., Kahn H.S., Courbon D., Eschwege E., Ducimetiere P. Hyperinsulinemia predicts fatal liver cancer but is inversely associated with fatal cancer as some other sites: the Paris prospective study. Diabetes Care. 24:2001;843-849
75. Vgontzas A.N., Bixler E.O., Chrousos G.P. Metabolic disturbances in obesity versus sleep apnea: the importance of visceral obesity and insulin resistance. J Intern Med. 254:2003;32-44
76. Olefsky J.M., Reaven G.M., Farquhar J.W. Effects of weight reduction on obesity: studies of carbohydrate and lipid metabolism. J Clin Invest. 53:1974;64-76
77. Bogardus C., Lillioja S., Mott D.M., Hollenbeck C., Reaven G.M. Relationship between degree of obesity and in vivo insulin action in man. Am J Physiol. 248:1985;E286-E291
78. Abbasi F., Brown B.W.B., Lamendola C., McLaughlin T., Reaven G.M. Relationship between obesity, insulin resistance, and coronary heart disease risk. J Am Coll Cardiol. 40:2002;937-943
79. McLaughlin T., Abbasi F., Lamendola C., Liang L., Reaven G., Schaaf P., et al. Differentiation between obesity and insulin resistance in the association with C-reactive protein. Circulation. 106:2002;2908-2912
80. McLaughlin T., Abbasi F., Cheal K., Chu J., Lamendola C., Reaven G. Use of metabolic markers to identify overweight individuals who are insulin resistant. Ann Intern Med. 139:2003;802-809
81. Ford E.S., Mokdad A.H., Giles W.H. Trends in waist circumference among US adults. Obes Res. 11:2003;1223-1231
82. Centers for Disease Control and Prevention. The third national health and nutrition examination survey (NHANES III 1988-1994) reference manuals and reports. Bethesda: Centers for Disease Control and Prevention; 1996.
83. Ferrannini E., Natali A., Bell P., Cavallo-Perin P., Lalic N., Mingrone G., on behalf of the European Group for the Study of Insulin Resistance. Insulin resistance and hypersecretion in obesity. J Clin Invest. 100:1997;1166-1173
84. Report of the expert committee on the diagnosis and classification of diabetes mellitus. Diabetes Care. 25:(Suppl 1):2002;S5-S20
85. Tuan C.-Y., Abbasi F., Lamendola C., McLaughlin T., Reaven G. Usefulness of plasma glucose and insulin concentrations in identifying patients with insulin resistance. Am J Cardiol. 92:2003;606-610
86. The DECODE Study Group, on behalf of the European Diabetes Epidemiology Group. Glucose tolerance and cardiovascular mortality: comparison of fasting and 2-hour diagnostic criteria. Arch Intern Med. 161:2001;397-404
87. Jeppesen J., Hein H.O., Suadicani P., Gynterberg F. Low triglycerides, high-density lipoprotein cholesterol and risk of ischemic heart disease. Arch Intern Med. 161:2001;361-366
88. Reaven G.M. The insulin resistance syndrome. Curr Atheroscler Rep. 5:2003;364-371
89. Ross R. The pathogenesis of atherosclerosis. N Engl J Med. 314:1986;488-500
90. Vallance P. Importance of asymmetrical dimethylarginine in cardiovascular risk. Lancet. 358:2002;2096-2097
91. Castelli W.P., Garrison R.J., Wilson P.W.F., Abbott R.O., Kalonsdian S., Kannel W.B. Incidence of coronary heart disease and lipoprotein cholesterol levels: the Framingham study. JAMA. 256:1986;2385-2387
92. Hulley S.H., Roseman R.H., Bawol R.D., Brand R.J. Epidemiology as a guide to clinical decisions: the association between triglyceride and coronary heart disease. N Engl J Med. 302:1980;1383-1389
93. Austin M.A., Hokanson J.E., Edwards K.I. Hypertriglyceridemia as a cardiovascular risk factor. Am J Cardiol. 81:(4A):1998;7B-12B
94. Austin M.A., Breslow J.L., Hennekens C.H., Buring J.E., Willett W.S., Krauss R.M. Low-density lipoprotein subclass patterns and risk of myocardial infarction. JAMA. 260:1988;1917-1921
95. Patsch J.R., Miesenbock T., Hopferwieser T., et al. Relation of triglyceride metabolism and coronary artery disease: studies in the postprandial state. Arterioscler Thromb. 12:1992;1336-1345
96. Manninen V., Tenkanen L., Koskinen P., Huttunen J.K., Manttari M., Heinonen O.P., et al. Joint effects of serum triglyceride and LDL and HDL cholesterol concentrations on coronary heart disease risk in the Helsinki heart study: implications for treatment. Circulation. 85:1992;37-45
97. Rubins H.B., Robins S.J., Collins D., Frye C.L., Anderson J.W., Elam W.B., et al. Gemfibrozil for the secondary prevention of coronary heart disease in men with low levels of high-density lipoprotein cholesterol: Veterans Affairs high-density lipoprotein cholesterol intervention trial (VA-HIT). N Engl J Med. 341:1999;410-418
98. Robins S.J., Rubins H.B., Fass F.H., Schaefer E.J., Elam M.B., Anderson J.W., et al. Insulin resistance and cardiovascular events with low HDL cholesterol: the Veterans Affairs HDL intervention trial (VA-Hit). Diabetes Care. 26:2003;1513-1517