Insulin Resistance And Human Disease: A Short History

Journal of Basic and Clinical Physiology and Pharmacology

Volumn 9, Issue 2-4, 1998, Pages 387-406

  Reaven, Gerald M ^a  

^a Shaman Pharmaceuticals Inc   (United States)

Author keywords

dyslipidemia; glucose intolerance; hyperinsulinemia; hypertension; insulin resistance; Syndrome X; type 2 diabetes

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN;

DISEASE ASSOCIATION; DYSLIPIDEMIA; GLUCOSE INTOLERANCE; HUMAN; HYPERTENSION; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; REVIEW; SYNDROME X;

BLOOD GLUCOSE; CORONARY DISEASE; DIABETES MELLITUS, TYPE 2; GLUCOSE INTOLERANCE; HISTORY, 20TH CENTURY; HUMANS; HYPERLIPIDEMIAS; HYPERTENSION; INSULIN RESISTANCE;

EID: 0032464031     PISSN: 07926855     EISSN: 21910286     Source Type: Journal    
DOI: 10.1515/JBCPP.1998.9.2-4.387     Document Type: Article

References (107)

1. Himsworth, HP. The mechanism of diabetes mellitus. I. Lancet 1939; II: 1–6.
2. Himsworth, HP. The mechanism of diabetes mellitus. II. The control of the blood sugar level. Lancet 1939; II: 65–68.
3. Himsworth, HP. The mechanism of diabetes mellitus. II. The control of the blood sugar level (cont). Lancet 1939; II: 118–122.
4. Himsworth, HP. The mechanism of diabetes mellitus. III. Human diabetes mellitus. Lancet 1939; II: 171–175.
5. Himsworth, HP. The syndrome of diabetes mellitus and its causes. Lancet 1949; I: 465–473.
6. Shen, S-W, Reaven, GM, Farquhar, JW. Comparison of impedance to insulin mediated glucose uptake in normal and diabetic subjects. J Clin Invest 1970; 49: 2151–2160.
7. Ginsberg, H, Olefsky, JM, Reaven, GM. Further evidence that insulin resistance exists in patients with chemical diabetes. Diabetes 1974; 23: 674–678.
8. Ginsberg, H, Kimmerling, G, Olefsky, JM, Reaven, GM. Demonstration of insulin resistance in untreated adult onset diabetic subjects with fasting hyperglycemia. J Clin Invest 1975; 55: 454–461.
9. National Diabetes Data Group: Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. Diabetes 1979; 28: 1039–1057.
10. Bornstein, J, Trewhella, P. Plasma insulin levels in diabetes mellitus in man. Aust J Exp Biol Med Sei 1950; 28: 569–572.
11. Bornstein, J, Lawrence, DD. Plasma insulin in human diabetes. Br Med J 1951; 2: 1541–1544.
12. Vallance-Owen, J, Hurlock, B, Pease, NW. Plasma insulin activity in diabetes mellitus. Lancet 1955; 2: 583–587.
13. Randle, PJ. In: Wolstenholme GEW, Cameron MP, eds. Ciba Foundation Colloquium on Endocrinology, 1957; 11: 115.
14. Yalow, RS, Berson, SA. Immunoassay of endogenous plasma insulin in man. J Clin Invest 1960; 39: 1157–1175.
15. Berson, SA, Yalow, RS. In: Wolstenholme GEW, Cameron MP, eds. Immunoassay of Hormones. Ciba Foundation Colloquium on Endocrinology, 1962; 14: 18
16. Hales, CN, Randle, PJ. Effects of low-carbohydrate diet and diabetes mellitus on plasma concentrations of glucose, non-esterified fatty acids, and insulin during oral glucose tolerance. Lancet 1963; I: 790–794.
17. Buchanan, KD, McKiddie, MT. Factors determining the plasma insulin response to oral glucose in diabetes mellitus. Diabetes 1967; 16: 466.
18. Reaven, GM, Miller, R. Study of the relationship between glucose and insulin responses to an oral glucose load in man. Diabetes 1968; 17: 560–569.
19. Chiles, R, Tzagournis, M. Excessive serum insulin response to oral glucose in obesity and mild diabetes. Diabetes 1970; 19: 458–464.
20. Seltzer, HS, Allen, WD, Herron, AL Jr, Brennan, MT. Insulin secretion in response to glycemic stimulus; relation of delayed initial release to carbohydrate intolerance in mild diabetes. J Clin Invest 1967; 46: 323–335.
21. Cerasi, E. An analogue computer model for the insulin response to glucose infusion. Acta Endocrinol 1967; 55: 163–183.
22. Perley, M, Kipnis, DM. Plasma insulin responses to glucose and tolbutamide of normal weight and obese diabetic and nondiabetic subjects. Diabetes 1966; 15: 867–874.
23. Alford, FP, Martin, FIR, Pearson, MJ. The significance and interpretation of mildly abnormal oral glucose tolerance. Diabetologia 1971; 7: 173–180.
24. Gerden, P, Roth, J. Plasma insulin: fluctuations in the “big” insulin component in man after glucose and other stimuli. J Clin Invest 1970; 48: 2225–2234.
25. Melani, F, Rubenstein, A, Steiner, D. Human serum proinsulin. J Clin Invest 1970; 49: 497–507.
26. Duckworth, WC, Kitabchi, AE. Direct measurement of plasma proinsulin in normal and diabetic subjects. Am J Med 1972; 53: 418–427.
27. Temple, RC, Carrington, CA, Luzio, SD, Owens, DR, Schneider, AE, Sobey, WJ, Hales, CN. Insulin deficiency in non-insulin-dependent diabetes. Lancet 1989; I: 293–295.
28. DeFronzo, R, Deibert, D, Hendler, R, Felig, P, Soman, V. Insulin sensitivity and insulin binding to monocytes in maturity-onset diabetes. J Clin Invest 1979; 63: 939–946.
29. Kolterman, OG, Gray, RS, Griifin, J, Brunstein, P, Insel, J. Receptor and postreceptor defects contribute to the insulin resistance in non-insulindependent diabetes mellitus. J Clin Invest 1981; 68: 957–969.
30. Reaven, GM. Insulin resistance in non-insulin-dependent diabetes mellitus. Does it exist and can it be measured? Am J Med 1983; 74: 3–17.
31. Sicree, RA, Zimmet, PZ, King, HOM, Coventry, JS. Plasma insulin response among Nauruans: prediction of deterioration in glucose tolerance over 6 yr. Diabetes 1987; 36: 179–186.
32. Saad, MF, Pettit, DJ, Mott, DM, Knowler, WC, Nelson, RG, Bennett, PH. Sequential changes in serum insulin concentration during development of non-insulin-dependent diabetes. Lancet 1989; I: 1356–1359.
33. Haffner, SM, Stern, MP, Mitchell, BD, Hazua, HP, Patterson, JK. Incidence of type II diabetes in Mexican Americans predicted by fasting insulin and glucose levels, obesity and body-fat distribution. Diabetes 1990; 39: 283–288.
34. Warram, JH, Martin, BC, Krolewski, AS, Soeldner, JS, Kahn, CR. Slow glucose removal rate and hyperinsulinemia precede the development of type II diabetes in the offspring of the diabetic parents. Ann Intern Med 1990; 113: 909–915.
35. Lillioja, S, Mott, DM, Spraul, M, Ferraro, R, Foley, JE, Ravussin, E, Knowler, WC, Bennett, PH, Bogardus, C. Insulin resistance and insulin secretory dysiunction as precursors of non-insulin-dependent diabetes mellitus. N Engl JMed 1993; 329: 1988–1992.
36. Himsworth, HP, Kerr, RB. Insulin-sensitive and insulin-insensitive types of diabetes mellitus. Clinical Science 1939; 4: 119–152.
37. Hollenbeck, C, Reaven, GM. Variations in insulin-stimulated glucose uptake in healthy individuals with normal glucose tolerance. J Clin Endocrinol Metab 1987; 64: 1169–1173.
38. Reaven, GM, Brand, RJ, Chen, Y-DI, Mathur, AK, Goldfine, I. Insulin resistance and insulin secretion are determinants of oral glucose in normal individuals. Diabetes 1993; 42: 1324–1332.
39. Reaven, GM. Role of insulin resistance in human disease. Diabetes 1988; 37: 1595–1607.
40. Reaven, GM, Olefsky, J, Farquhar, JW. Does hyperglycemia or hyperinsulinemia characterize the patient with chemical diabetes? Lancet 1972; I: 1247–1249.
41. Reaven, GM, Chen, Y-DI, Hollenbeck, CB, Sheu, WHH, Ostrega, D, Polonsky, KS. Plasma insulin, C-peptide, and proinsulin concentrations in obese and nonobese individuals with varying degrees of glucose tolerance. J Clin Endocrinol Metab 1993; 76: 44–48.
42. Zavaroni, I, Dall'Aglio, E, Bonora, E, Alpi, O, Passed, M, Reaven, GM,. Evidence that multiple risk factors for coronary artery disease exist in persons with abnormal glucose tolerance. Am J Med 1987; 83: 609–612.
43. Zavaroni, I, Bonora, E, Pagliara, M, Dall'Aglio, E, Luchetti, L, Buonanno, G, Bonati, PA, Bergonzani, M, Gnudi, L, Passeri, M, Reaven, GM,. Risk factors for coronary artery disease in healthy persons with hyperinsulinemia and normal glucose tolerance. N Engl J Med 1989; 320: 702–706.
44. Reaven, G, Calciano, A, Cody, R, Lucas, C, Miller, R. Carbohydrate intolerance and hyperlipemia in patients with myocardial infarction without known diabetes mellitus. J Clin Endocrinol Metab 1963; 23: 1013–1023.
45. Young, MH, Jeng, C-Y, Sheu, WH-H, Shieh, S-M, Fuh, MM-T, Chen, Y-DI, Reaven, GM. Insulin resistance, glucose intolerance, hyperinsulinemia and dyslipidemia in patients with angiographically demonstrated coronary arteiy disease. Am J Cardiol 1993; 72: 458–460.
46. Ahrens, EH Jr, Hirsch, J, Oette, K, Farquhar, JW, Stein, Y. Carbohydrate-induced and fat-induced lipemia. Trans Assoc Am Phvs 1961; 74: 134.
47. Reaven, GM, Hill, DB, Gross, RC, Farquhar, JW. Kinetics of triglyceride turnover of very low density lipoproteins of human plasma. J Clin Invest 1965; 44: 1826–1833.
48. Farquhar, JW, Frank, A, Gross, RC, Reaven, GM. Glucose, insulin and triglyceride responses to high and low carbohydrate diets in man. J Clin Invest 1966; 45: 1648–1656.
49. Reaven, GM, Lerner, RL, Stern, MP, Farquhar, JW. Role of insulin in endogenous hypertriglyceridemia. J Clin Invest 1967; 46: 1756–1767.
50. Olefsky, JM, Farquhar, JW, Reaven, GM. Reappraisal of the role of insulin in hypertriglyceridemia. Am J Med 1974; 57: 551–560.
51. Tobey, TA, Greenfield, MS, Kraemer, FB, Reaven, GM. Relationship between insulin resistance, insulin secretion, very low density lipoprotein kinetics and plasma triglyceride levels in normotriglyceridemia in man. Metabolism 1981; 30: 165–171.
52. Reaven, GM. Are triglycerides important as a risk factor for coronary disease? Heart Disease and Stroke 1993; 2: 44–48.
53. Reaven, GM. Hypertriglyceridemia: The central feature of Syndrome X. Cardiovasc Risk Factors 1996; 6: 29–35.
54. Miller, GJ, Miller, NE. Plasma-high-density-lipoprotein concentration and development of ischaemic heart disease. Lancet 1975; I: 16–19.
55. Castelli, WP, Garrison, RJ, Wilson, PWF, Abbott, RO, Kalonsdian, S, Kannel, WB. Incidence of coronary heart disease and lipoprotein cholesterol levels. The Framingham Study. JAMA 1986; 256: 2835–2837.
56. Laws, A, Reaven, GM. Evidence for an independent relationship between insulin resistance and fasting plasma HDL-cholesterol. triglyceride and insulin concentrations. J Intern Med 1992; 231: 25–30.
57. Swenson, TL. The role of the cholesteryl ester transfer protein in lipoprotein metabolism. Diabetes Metab Rev 1991; 7: 139–153.
58. Golay, A, Zech, L, Shi, M-Z, Chiou, Y-AM, Reaven, GM, Chen, Y-DL. High density lipoprotein (HDL) metabolism in noninsulin-dependent diabetes mellitus: measurement of HDL turnover using tritiated HDL. J Clin Endocrinol Metab 1987; 65: 512–518.
59. Brinton, EA. Eisenberg, S, Breslow, JL. Human HDL cholesterol levels are determined by apoA-1 fractional catabolic rate, which correlates inversely with estimates of HDL particle size. Effects of gender, hepatic and lipoprotein lipases, triglyceride and insulin levels, and body fat distribution. Arterioscler Thromb 1994; 14: 707–720.
60. Zilversmit, DB. Atherogenesis: a postprandial phenomenon. Circulation 1979; 60: 473–485.
61. Simmons, LA, Sweyer, T, Simons, J, et al. Chylomicrons and chylomicron remnants in coronary arteiy disease: a case-control study. Atherosclerosis 1987; 65: 181–189.
62. Simpson, HS, Williamson, CM, Olivecrona, T, et al. Postprandial lipemia, fenofibrate and coronary artery disease. Atherosclerosis 1990; 85: 193–202.
63. Groot, PHE, van Stiphout, WAHJ, Krauss, XH, et al. Postprandial lipoprotein metabolism in normolipidemic men with and without coronary artery disease. Arterioscler Thromb 1991; 11: 653–662.
64. Patsch, IR. Miesenbsck, G, Hopferwieser, T, et al. Relation of triglyceride metabolism and coronary artery disease: studies in the postprandial state. Arterioscler Thromb 1992; 12: 1336–1345.
65. Karpe, F, Bard, JM, Steiner, G, Carlson, LA, Fruchart, JC, Hamsten, A. HDLs and alimentary lipemia: studies in men with previous myocardial infarction at young age. Arterioscler Thromb 1993; 13: 11–22.
66. Nestel, PJ. Relationship between plasma triglycerides and removal of chylomicrons. J Clin Invest 1964; 43: 943–949.
67. Wilson, DE, Chan, I-F, Buchi, KN, Horton, SC. Post-challenge plasma lipoprotein retinoids: chylomicron remnants in endogenous hypertriglyceridemia. Metabolism 1985; 34: 551–558.
68. Chen, Y-DI, Swami, S, Skowronski, R, Coulston, A, Reaven, GM. Differences in postprandial lipemia between patients with normal glucose tolerance and noninsulin-dependent diabetes mellitus. J Clin Endocrinol Metab 1993; 76: 347–351.
69. Chen, Y-DI, Sheu, WH-H, Swislock, ALM, Reaven, GM. High density lipoprotein turnover in patients with hypertension. Hypertension 1991; 17: 386–393.
70. Jeppesen, J, Hollenbeck, CB, Zhou, M-Y, Coulston, AM, Jones, C, Chen, Y-DI, Reaven, GM. Relation between insulin resistance, hyperinsulinemia, postheparin plasma lipoprotein lipase activity, and postprandial lipemia. Arterioscler Thromb Vasc Biol 1995; 15: 320–324.
71. Austin, MA, Breslow, JL, Hennekens, CH, Buring, JE, Willett, WS, Krauss, RM. Low-density lipoprotein subclass patterns and risk of myocardial infarction. JAMA 1988; 260: 1917–1921
72. Austin, MA, King, M-C, Vranizan, KM, Krauss, RM. Atherogenic lipoprotein phenotype: a proposed genetic marker for coronary heart disease risk. Circulation 1990; 82: 495–506.
73. Reaven, GM, Chen, Y-DI, Jeppesen, J, Maheux, P, Krauss, RM. Insulin resistance and hyperinsulinemia in individuals with small, dense, low density lipoprotein particles. J Clin Invest 1993; 92: 141–146.
74. Welborn, TA, Breckenridge, A, Rubinstein, AH, Dolleiy, CT, Fraser, TR. Serum-insulin in essential hypertension and in peripheral vascular disease. Lancet 1966; I: 1136–1137.
75. Lucas, CP, Estigarribia, JA, Darga, LL, Reaven, GM. Insulin and blood pressure in obesity. Hypertension 1985; 7: 702–706.
76. Modan, M, Halkin, H, Almog, S, Lusky, A, Eshkil, A, Shefi, M, Shitrit, A, Fuchs, A. Hyperinsulinemia: a link between hypertension, obesity and glucose intolerance. J Clin Invest 1985; 75: 809–817.
77. Ferrannini, E, Buzzigoli, G, Bonadona, R. Insulin resistance in essential hypertension. N Engl J Med 1987; 317: 350–357.
78. Shen, D-C, Shieh, S-M, Fuh, M, Wu, D-A, Chen, Y-DI, Reaven, GM. Resistance to insulin-stimulated glucose uptake in patients with hypertension. J Clin Endocrinol Metab 1988; 66: 580–583.
79. Swislocki, ALM, Hoffman, BB, Reaven, GM. Insulin resistance, glucose intolerance and hyperinsulinemia in patients with hypertension. Am J Hypertens 1989; 2: 419–423.
80. Jarret, RJ, Keen, H, McCartney, M, Fuller, JH, Hamilton, PJS, Reid, DD, Rose, GL. Glucose tolerance and blood pressure in two population samples: their relation to diabetes mellitus and hypertension. Int J Epidemiol 1978; 7: 15–24.
81. Follare, T, Lithell, H, Berne, C. Insulin resistance is a characteristic feature of primary hypertension independent of obesity. Metabolism 1990; 39: 167–174.
82. Zavaroni, I, Mazza, S, Dall'Aglio, E, Gasparini, P, Passeri, M, Reaven, GM,. Prevalence of hyperinsulinaemia in patients with high blood pressure. J Intern Med 1992; 231: 235–240.
83. Ferrari, P, Weidmann, P, Shaw, S, Giachino, D, Riesen, W, Allemann, Y, Heynen, G. Altered insulin sensitivity, hyperinsulinemia and dyslipidemia in individuals with a hypertensive parent. Am J Med 1991; 91: 589–596.
84. Allemann, Y, Horber, FF, Colombo, M, Ferrari, P, Shaw, S, Jaeger, P, Weidman, P. Insulin sensitivity and body fat distribution in normotensive offspring of hypertensive parents. Lancet 1993; 341: 327–331.
85. Facchini, F, Chen, Y-DI. Clinkingbeard, C, Jeppesen, J. Reaven, GM. Insulin resistance, hyperinsulinemia, and dyslipidemia in nonobese individuals with a family history of hypertension. Am J Hypertens 1992; 5: 694–699.
86. Ohno, Y, Suzuki, H, Yamakawa, H. Nakamura, M, Otsuka, K. Saruta, T. Impaired insulin sensitivity in young, lean normotensive offspring of essential hypertensive: possible role of disturbed calcium metabolism. J Hypertens 1993; 11: 421–426.
87. Beatty, OL. Harper, R. Sheridan, B. Atkinson, AB, Bell, PM. Insulin resistance in offepring of hypertensive parents. BMJ 1993; 307: 92–96.
88. Manicardi, V, Camellini, L, Bellodi, G, Caselli, C, Ferrannini, E. Evidence for an association of high blood pressure and hyperinsulinemia in obese man. J Clin Endocrinol Metab 1986; 62: 1302–1304.
89. Fournier, AM. Gadia, MT, Kubrusly, DB, Skylar, JS, Sosenko, JM. Blood pressure, insulin, and glycemia in nondiabetic subjects. Am J Med 1986; 80: 861–864.
90. Denker, PS, Pollok, VE. Fasting serum insulin levels in essential hypertension. A meta analysis. Arch Intern Med 1992; 152: 1649–1651.
91. Ferrannini, E, Natali, A, Capaldo, B, Lehtovirta, M, Jacob, S, Yki-Järvinen, H, for the European Group for the Study of Insulin Resistance (EGIR). Insulin resistance, hyperinsulinemia, and blood pressure. Role of age and obesity. Hypertension 1997; 30: 1144–1149.
92. Skarfors, ET, Lithell, HO, Selinus, I. Risk factors for the development of hypertension: a 10-year longitudinal study in middle-aged men. J Hypertension 1991; 9: 217–223.
93. Lissner, L, Bengtsson, C, Lapidus, L, Kristjansson, K. Wedel, H. Fasting insulin in relation to subsequent blood pressure changes and hypertension in women. Hypertension 1992; 20: 797–801.
94. Taittonen, L. Uhari, M, Nuutinen, M. Turtinen, J, Pokka, T, Akerblom, HK. Insulin and blood pressure among healthy children. Am J Hypertens 1996; 9: 193–199.
95. Raitakari, OT, Porkka, KVK, Rönnemaa, T, Knip, M, Uhari, M, Akerblom, HK, Viikari, JSA. The role of insulin in clustering of serum lipids and blood pressure in children and adolescents. Diabetologia 1995; 38: 1042–1050.
96. Hwang, I-S, Ho, H. Hoffman, BB, Reaven, GM. Fructose-induced insulin and hypertension in rats. Hypertension 1987; 10: 512–516.
97. Reaven, GM, Ho, H, Hoffman, BB. Attenuation of fructose-induced hypertension in rats by exercise training. Hypertension 1988; 12: 129–132.
98. Reaven, GM. Ho, H, Hoffman, BB. Somatostatin inhibition of fructose-induced hypertension. Hypertension 1989; 14: 117–120.
99. Mondon, CE, Reaven, GM. Evidence of abnormalities of insulin metabolism in rats with spontaneous hypertension. Metabolism 1988; 37: 303–305.
100. Reaven, GM, Chang, H, Hoffman, BB, Azhar, S. Resistance to insulin-stimulated glucose uptake in adipocytes isolated from spontaneously hypertensive rats. Diabetes 1989; 38: 1155–1160.
101. Reaven, GM. Ho, H, Chang, H. Hypertriglyceridemia in Dahl rats: effect of sodium intake and gender. Horm Metab Res 1991; 23: 44–45.
102. Reaven, GM, Chang, H. Relationship between blood pressure, plasma insulin and triglyceride concentration, and insulin action in spontaneous hypertensive and Wistar-Kyoto rats. Am J Hypertens 1991; 4: 34–38.
103. Dall'Aglio, E, Tosini, P, Ferrari, P, Zavaroni, I, Passeri, M, Reaven, GM,. Abnormalities of insulin and lipid metabolism in Milan hypertensive rats. Am J Hypertens 1991; 4: 773–775.
104. Reaven, GM, Twersky, J, Chang, H. Abnormalities of carbohydrate and lipid metabolism in Dahl rats. Hypertension 1991; 18: 630–635.
105. Collins, R, Peto, R, MacMahon, S, Herber, P, Fiebach, NH, Eberlein, KA, Godwin, J, Qizilbash, N, Taylor, JO, Hennekens, CH. Blood pressure, stroke and coronary heart disease. Pt. 2. Short-term reductions in blood pressure: overview of randomised drug trials in their epidemiological context. Lancet 1990; 335: 827–838.
106. Reaven, GM. Pathophysiology of insulin resistance in human disease. Physiol Rev 1995; 75: 473–486.
107. Sheu, WH-H, Jeng, C-Y, Shieh, S-M, Fuh, MM, Shen, DD, Chen, Y-DI, Reaven, GM. Insulin resistance and abnormal electrocardiograms in patients with high blood pressure. Am J Hypertens 1992; 5: 444–448.