Diabetic cardiomyopathy: The search for a unifying hypothesis

Circulation Research

Volumn 98, Issue 5, 2006, Pages 596-605

  Poornima, Indu G ^b   Parikh, Pratik ^b   Shannon, Richard P ^a  

^a ALLEGHENY GENERAL HOSPITAL   (United States)

^b NONE

Author keywords

Cardiac hypertrophy; Diabetic cardiomyopathy; Diastolic function; Insulin resistance

Indexed keywords

FATTY ACID; AKT1 PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

CARDIOMYOPATHY; CORONARY ARTERY ATHEROSCLEROSIS; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIASTOLE; GLUCOSE HOMEOSTASIS; HEART FUNCTION; HEART LEFT VENTRICLE FAILURE; HEART LEFT VENTRICLE HYPERTROPHY; HUMAN; HYPERGLYCEMIA; HYPERINSULINEMIA; INSULIN DEPENDENT DIABETES MELLITUS; ISCHEMIC HEART DISEASE; METABOLIC DISORDER; MICROCIRCULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; OBESITY; PRIORITY JOURNAL; REVIEW; SYSTOLE; ANIMAL; BLOOD; CORONARY ARTERY BLOOD FLOW; HEART LEFT VENTRICLE FUNCTION; HYPERINSULINISM; INSULIN RESISTANCE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CARDIOMYOPATHIES; CORONARY CIRCULATION; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FATTY ACIDS, NONESTERIFIED; HUMANS; HYPERGLYCEMIA; HYPERINSULINISM; HYPERTROPHY, LEFT VENTRICULAR; INSULIN RESISTANCE; PROTO-ONCOGENE PROTEINS C-AKT; VENTRICULAR DYSFUNCTION, LEFT;

EID: 33645280925     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000207406.94146.c2     Document Type: Review

References (98)

1. Francis GS. Diabetic cardiomyopathy: fact or fiction? Heart. 2001;85:247-248.
2. Picano E. Diabetic cardiomyopathy. The importance of being earliest. J Am Coll Cardiol. 2003;42:454-457.
3. Avogaro A, Vigili dKS, Negut C, Tiengo A, Scognamiglio R. Diabetic cardiomyopathy: a metabolic perspective. Am J Cardiol. 2004;93:13A-16A.
4. Adeghate E. Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol Cell Biochem. 2004;261:187-191.
5. Ho KK, Pinsky JL, Kannel WB, Levy D. The epidemiology of heart failure: the Framingham Study. J Am Coll Cardiol. 1993;22:6A-13A.
6. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol. 1974;34:29-34.
7. Kitzman DW, Gardin JM, Gottdiener JS, Arnold A, Boineau R, Aurigemma G, Marino EK, Lyles M, Cushman M, Enright PL; Cardiovascular Health Study Research Group. Importance of heart failure with preserved systolic function in patients > or = 65 years of age. CHS Research Group. Cardiovascular Health Study. Am J Cardiol. 2001;87:413-419.
8. McMurray JJ, Stewart S. Epidemiology, aetiology, and prognosis of heart failure. Heart. 2000;83:596-602.
9. Bertoni AG, Tsai A, Kasper EK, Brancati FL. Diabetes and idiopathic cardiomyopathy: a nationwide case-control study. Diabetes Care. 2003;26:2791-2795.
10. Shulman GI. Cellular mechanisms of insulin resistance. J Clin Invest. 2000;106:171-176.
11. Birnbaum MJ. Turning down insulin signaling. J Clin Invest. 2001;108:655-659.
12. Kim JK, Kim YJ, Fillmore JJ, Chen Y, Moore I, Lee J, Yuan M, Li ZW. Karin M, Perret P, Shoelson SE, Shulman GI. Prevention of fat-induced insulin resistance by salicylate. J Clin Invest. 2001;108:437-446.
13. Brazil DP, Hemmings BA. Ten years of protein kinase B signalling: a hard Akt to follow. Trends Biochem Sci. 2001;26:657-664.
14. Lawlor MA, Alessi DR. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci. 2001;114:2903-2910.
15. Morisco C, Zebrowski D, Condorelli G, Tsichlis P, Vatner SF, Sadoshima J. The Akt-glycogen synthase kinase 3beta pathway regulates transcription of atrial natriuretic factor induced by beta-adrenergic receptor stimulation in cardiac myocytes. J Biol Chem. 2000;275:14466-14475.
16. Schwartzbauer G, Robbins J. The tumor suppressor gene PTEN can regulate cardiac hypertrophy and survival. J Biol Chem. 2001;276:35786-35793.
17. Unger RH, Orci L. Lipotoxic diseases of nonadipose tissues in obesity. Int J Obes Relat Metab Disord. 2000;24(suppl 4):S28-S32.
18. Liu GX, Hanley PJ, Ray J, Daut J. Long-chain acyl-coenzyme A esters and fatty acids directly link metabolism to K(ATP) channels in the heart. Circ Res. 2001;88:918-924.
19. Halse R, Pearson SL, McCormack JG, Yeaman SJ, Taylor R. Effects of tumor necrosis factor-alpha on insulin action in cultured human muscle cells. Diabetes. 2001;50:1102-1109.
20. Zhang DX, Fryer RM, Hsu AK, Zou AP, Gross GJ, Campbell WB, Li PL. Production and metabolism of ceramide in normal and ischemic-reperfused myocardium of rats. Basic Res Cardiol. 2001;96:267-274.
21. Ilercil A, Devereux RB, Roman MJ, Paranicas M, O'Grady MJ, Lee ET, Welty TK, Fabsitz RR, Howard BV. Associations of insulin levels with left ventricular structure and function in Am Indians: the strong heart study. Diabetes. 2002;51:1543-1547.
22. Iacobellis G, Ribaudo MC, Zappaterreno A, Vecci E, Tiberti C, Di Mario U, Leonetti F. Relationship of insulin sensitivity and left ventricular mass in uncomplicated obesity. Obes Res. 2003;11:518-524.
23. McNulty PH. Insulin resistance and cardiac mass: the end of the beginning? Obes Res. 2003;11:507-508.
24. Ueno M, Carvalheira JB, Tambascia RC, Bezerra RM, Amaral ME, Carneiro EM, Folli F, Franchini KG, Saad MJ. Regulation of insulin signalling by hyperinsulinaemia: role of IRS-1/2 serine phosphorylation and the mTOR/p70 S6K pathway. Diabetologia. 2005;4:506-518.
25. O'Neill BT, Abel ED. Akt1 in the cardiovascular system: friend or foe? J Clin Invest. 2005;115:2059-2064.
26. Morisco C, Condorelli G, Trimarco V, Bellis A, Marrone C, Condorelli G, Sadoshima J, Trimarco B. Akt mediates the cross-talk between beta-adrenergic and insulin receptors in neonatal cardiomyocytes. Circ Res. 2005;96:180-188.
27. Khamzina L, Veilleux A, Bergeron S, Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology. 2005;146:1473-1481.
28. Manning BD. Balancing Akt with S6K: implications for both metabolic diseases and tumorigenesis. J Cell Biol. 2004;167:399-403.
29. Shah OJ, Wang Z, Hunter T. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies. Curr Biol. 2004;14:1650-1656.
30. Tremblay F, Marette A. Amino acid and insulin signaling via the mTOR/p70 S6 kinase pathway. A negative feedback mechanism leading to insulin resistance in skeletal muscle cells. J Biol Chem. 2001;276:38052-38060.
31. Kern W, Peters A, Born J, Fehm HL, Schultes B. Changes in blood pressure and plasma catecholamine levels during prolonged hyperinsulinemia. Metabolism. 2005;54:391-396.
32. Grassi G. Counteracting the sympathetic nervous system in essential hypertension. Curr Opin Nephrol Hypertens. 2004;13:513-519.
33. Yosefy C, Magen E, Kiselevich A, Priluk R, London D, Volchek L, Viskoper RJ Jr. Rosiglitazone improves, while Glibenclamide worsens blood pressure control in treated hypertensive diabetic and dyslipidemic subjects via modulation of insulin resistance and sympathetic activity. J Cardiovasc Pharmacol. 2004;44:215-222.
34. Wang CC, Goalstone ML, Draznin B. Molecular mechanisms of insulin resistance that impact cardiovascular biology. Diabetes. 2004;53:2735-2740.
35. Naito Z, Takashi E, Xu G, Ishiwata T, Teduka K, Yokoyama M, Yamada N, Sugisaki Y, Asano G. Different influences of hyperglycemic duration on phosphorylated extracellular signal-regulated kinase 1/2 in rat heart. Exp Mol Pathol. 2003;74:23-32.
36. Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, Brownlee M. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells. J Clin Invest. 2003;112:1049-1057.
37. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Dates PJ, Hammes HP, Giardino I, Brownlee M. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature. 2000;404:787-790.
38. Nishikawa T, Edelstein D, Brownlee M. The missing link: a single unifying mechanism for diabetic complications. Kidney Int Suppl. 2000;77:S26-S30.
39. Cai L, Kang YJ. Oxidative stress and diabetic cardiomyopathy: a brief review. Cardiovasc Toxicol. 2001;1:181-193.
40. Farhangkhoee H, Khan ZA, Mukherjee S, Cukiernik M, Barbin YP, Karmazyn M Chakrabarti S. Heme oxygenase in diabetes-induced oxidative stress in the heart. J Mol Cell Cardiol. 2003;35:1439-1448.
41. Bidasee KR, Nallani K, Yu Y, Cocklin RR, Zhang Y, Wang M, Dincer UD, Besch HR Jr. Chronic diabetes increases advanced glycation end products on cardiac ryanodine receptors/calcium-release channels. Diabetes. 2003;52:1825-1836.
42. Candido R, Forbes JM, Thomas MC, Thallas V, Dean RG, Burns WC, Tikellis C, Ritchie RH, Twigg SM, Cooper ME, Burrell LM. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res. 2003;92:785-792.
43. Cooper ME Importance of advanced glycation end products in diabetes-associated cardiovascular and renal disease. Am J Hypertens. 2004;17:31S-38S.
44. Herrmann KL, McCulloch AD, Omens JH. Glycated collagen cross-linking alters cardiac mechanics in volume-overload hypertrophy. Am J Physiol Heart Circ Physiol. 2003;284:H1277-H1284.
45. Clark RJ, McDonough PM, Swanson E, Trost SU, Suzuki M, Fukuda M, Dillmann WH. Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem. 2003;278:44230-44237.
46. Wu-Wong JR, Berg CE, Dayton BD. Endothelin-stimulated glucose uptake: effects of intracellular Ca (2+), cAMP and glucosamine. Clin Sci (Lond). 2002;103(suppl 48):418S-423S.
47. Galvez AS, Ulloa JA, Chiong M, Criollo A, Eisner V, Barros LF, Lavandero S. Aldose reductase induced by hyperosmotic stress mediates cardiomyocyte apoptosis: differential effects of sorbitol and mannitol. J Biol Chem. 2003;278:38484-38494.
48. Ramasamy R. Aldose reductase: a novel target for cardioprotective interventions. Curr Drug Targets. 2003;4:625-632.
49. Guo M, Wu MH, Korompai F, Yuan SY. Upregulation of PKC genes and isozymes in cardiovascular tissues during early stages of experimental diabetes. Physiol Genomics. 2003;12:139-146.
50. Koya D, King GL. Protein kinase C activation and the development of diabetic complications. Diabetes. 1998;47:859-866.
51. Wakasaki H, Koya D, Schoen FJ, Jirousek MR, Ways DK, Hoit BD, Walsh RA, King GL. Targeted overexpression of protein kinase C beta2 isoform in myocardium causes cardiomyopathy. Proc Natl Acad Sci U S A. 1997;94:9320-9325.
52. Tahiliani AG, McNeill JH. Diabetes-induced abnormalities in the myocardium. Life Sci. 1986;38:959-974.
53. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev. 2004;25:543-567.
54. Depre C, Young ME, Ying J, Ahuja HS, Han Q, Garza N, Davies PJ, Taegtmeyer H. Streptozotocin-induced changes in cardiac gene expression in the absence of severe contractile dysfunction. J Mol Cell Cardiol. 2000;32:985-996.
55. Dhalla NS, Pierce GN, Innes IR, Beamish RE. Pathogenesis of cardiac dysfunction in diabetes mellitus. Can J Cardiol. 1985;1:263-281.
56. Jackson CV, McGrath GM, Tahiliani AG, Vadlamudi RV, McNeill JH. A functional and ultrastructural analysis of experimental diabetic rat myocardium. Manifestation of a cardiomyopathy. Diabetes. 1985;34:876-883.
57. Hu P, Zhang D, Swenson L, Chakrabarti G, Abel ED, Litwin SE. Minimally invasive aortic banding in mice: effects of altered cardiomyocyte insulin signaling during pressure overload. Am J Physiol Heart Circ Physiol. 2003;285:H1261-H1269.
58. Scognamiglio R, Avogaro A, Negut C, Piccolotto R, Vigili dK, Tiengo A. Early myocardial dysfunction in the diabetic heart: current research and clinical applications. Am J Cardiol. 2004;93:17A-20A.
59. Rodrigues B, Cam MC, McNeill JH. Myocardial substrate metabolism: implications for diabetic cardiomyopathy. J Mol Cell Cardiol. 1995;27:169-179.
60. Vadlamudi RV, Rodgers RL, McNeill JH. The effect of chronic alloxan- and streptozotocin-induced diabetes on isolated rat heart performance. Can J Physiol Pharmacol. 1982;60:902-911.
61. Fein FS, Strobeck JE, Malhotra A, Scheuer J, Sonnenblick EH. Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res. 1981;49:1251-1261.
62. Malhotra A, Penpargkul S, Fein FS, Sonnenblick EH, Scheuer J. The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ Res. 1981;49:1243-1250.
63. Rajapurohitam V, Gan XT, Kirshenbaum LA, Karmazyn M. The obesity-associated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ Res. 2003;93:277-279.
64. Purdham DM, Zou MX, Rajapurohitam V, Karmazyn M. Rat heart is a site of leptin production and action. Am J Physiol Heart Circ Physiol. 2004;287:H2877-H2884.
65. Atkinson LL, Fischer MA, Lopaschuk GD. Leptin activates cardiac fatty acid oxidation independent of changes in the AMP-activated protein kinase-acetyl-CoA carboxylase-malonyl-CoA axis. J Biol Chem. 2002;277:29424-29430.
66. Tajmir P, Ceddia RB, Li RK, Coe IR, Sweeney G. Leptin increases cardiomyocyte hyperplasia via extracellular signal-regulated kinase-and phosphatidylinositol 3-kinase-dependent signaling pathways. Endocrinology. 2004;145:1550-1555.
67. Paolisso G, Tagliamonte MR, Galderisi M, Zito GA, Petrocelli A, Carella C, de Divitiis O, Varricchio M. Plasma leptin level is associated with myocardial wall thickness in hypertensive insulin-resistant men. Hypertension. 1999;34:1047-1052.
68. Mazumder PK, O'Neill BT, Roberts MW, Buchanan J, Yun UJ, Cooksey RC, Boudina S, Abel ED. Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes. 2004;53:2366-2374.
69. Barouch LA, Berkowitz DE, Harrison RW, O'Donnell CP, Hare JM. Disruption of leptin signaling contributes to cardiac hypertrophy independently of body weight in mice. Circulation. 2003;108:754-759.
70. McDonagh PF, Hokama JY. Microvascular perfusion and transport in the diabetic heart. Microcirculation. 2000;7:163-181.
71. Raev DC. Left ventricular function and specific diabetic complications in other target organs in young insulin-dependent diabetics: an echocardiographic study. Heart Vessels. 1994;9:121-128.
72. Belke DD, Larsen TS, Gibbs EM, Severson DL. Altered metabolism causes cardiac dysfunction in perfused hearts from diabetic (db/db) mice. Am J Physiol Endocrinol Metab. 2000;279:E1104-E1113.
73. Young ME, Guthrie PH, Razeghi P, Leighton B, Abbasi S, Patil S, Youker KA, Taegtmeyer H. Impaired long-chain fatty acid oxidation and contractile dysfunction in the obese Zucker rat heart. Diabetes. 2002;51:2587-2595.
74. Paradise NF, Pilati CF, Payne WR, Finkelstein JA. Left ventricular function of the isolated, genetically obese rat's heart. Am J Physiol. 1985;248:H438-H444.
75. Ren J, Sowers JR, Walsh MF, Brown RA. Reduced contractile response to insulin and IGF-I in ventricular myocytes from genetically obese Zucker rats. Am J Physiol Heart Circ Physiol. 2000;279:H1708-H1714.
76. Conti M, Renaud IM, Poirier B, Michel O, Belair MF, Mandet C, Bruneval P, Myara I, Chevalier J. High levels of myocardial antioxidant defense in aging nondiabetic normotensive Zucker obese rats. Am J Physiol Regul Integr Comp Physiol. 2004;286:R793-R800.
77. Rosen P, Herberg L, Reinauer H. Different types of postinsulin receptor defects contribute to insulin resistance in hearts of obese Zucker rats. Endocrinology. 1986;119:1285-1291.
78. Sidell RJ, Cole MA, Draper NJ, Desrois M, Buckingham RE, Clarke K. Thiazolidinedione treatment normalizes insulin resistance and ischemic injury in the zucker Fatty rat heart. Diabetes. 2002;51:1110-1117.
79. Wang P, Lloyd SG, Zeng H, Bonen A, Chatham JC. Impact of altered substrate utilization on cardiac function in isolated hearts from Zucker diabetic fatty rats. Am J Physiol Heart Circ Physiol. 2005;288:H2102-H2110.
80. Chatham JC, Seymour AM. Cardiac carbohydrate metabolism in Zucker diabetic fatty rats. Cardiovasc Res. 2002;55:104-112.
81. Huisamen B, van Zyl M, Keyser A, Lochner A. The effects of insulin and beta-adrenergic stimulation on glucose transport, glut 4 and PKB activation in the myocardium of lean and obese noninsulin dependent diabetes mellitus rats. Mol Cell Biochem. 2001;223:15-25.
82. Golfman LS, Wilson CR, Sharma S, Burgmaier M, Young ME, Guthrie PH, Van Arsdall M, Adrogue JV, Brown KK, Taegtmeyer H. Activation of PPAR (gamma) enhances myocardial glucose oxidation and improves contractile function in isolated working hearts of ZDF rats. Am J Physiol Endocrinol Metab. 2005;289:E328-E336.
83. Fredersdorf S, Thumann C, Ulucan C, Griese DP, Luchner A, Riegger GA, Kromer EP, Weil J. Myocardial hypertrophy and enhanced left ventricular contractility in Zucker diabetic fatty rats. Cardiovasc Pathol. 2004;13:11-19.
84. Yu Y, Ohmori K, Kondo I, Yao L, Noma T, Tsuji T, Mizushige K, Kohno M. Correlation of functional and structural alterations of the coronary arterioles during development of type II diabetes mellitus in rats. Cardiovasc Res. 2002;56:303-311.
85. Abe T, Ohga Y, Tabayashi N, Kobayashi S, Sakata S, Misawa H, Tsuji T, Kohzuki H, Suga H, Taniguchi S, Takaki M. Left ventricular diastolic dysfunction in type 2 diabetes mellitus model rats. Am J Physiol Heart Circ Physiol. 2002;282:H138-H148.
86. Finck BN, Lehman JJ, Leone TC, Welch MJ, Bennett MJ, Kovacs A, Han X, Gross RW, Kozak R, Lopaschuk GD, Kelly DP. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest. 2002;109:121-130.
87. Huss JM, Kelly DP. Mitochondrial energy metabolism in heart failure: a question of balance. J Clin Invest. 2005;115:547-555.
88. Chiu HC, Kovacs A, Blanton RM, Han X, Courtois M, Weinheimer CJ, Yamada KA, Brunet S, Xu H, Nerbonne JM, Welch MJ, Fettig NM, Sharp TL, Sambandam N, Olson KM, Ory DS, Schaffer JE. Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ Res. 2005;96:225-233.
89. Rutter MK, Parise H, Benjamin EJ, Levy D, Larson MG, Meigs JB, Nesto RW, Wilson PW, Vasan RS. Impact of glucose intolerance and insulin resistance on cardiac structure and function: sex-related differences in the Framingham Heart Study. Circulation. 2003;107:448-454.
90. Tenenbaum A, Fisman EZ, Schwammenthal E, Adler Y, Benderly M, Motro M, Shemesh J. Increased prevalence of left ventricular hypertrophy in hypertensive women with type 2 diabetes mellitus. Cardiovasc Diabetol. 2003;2:14.
91. Camper-Kirby D, Welch S, Walker A, Shiraishi I, Setchell KDR, Schaefer E, Kajstura J, Anversa P, Sussman MA. Myocardial Akt activation and gender. Increased nuclear activity in females versus males. Circ Res. 2001;88:1020-1027.
92. Sugden PH, Clerk A. Akt like a women. Gender differences in susceptibility to cardiovascular disease. Circ Res. 2001;88:975-977.
93. Dagres N, Saller B, Haude M, Husing J, von Birgelen C, Schmermund A, Sack S, Baumgart D, Mann K, Erbel R. Insulin sensitivity and coronary vasoreactivity: insulin sensitivity relates to adenosine-stimulated coronary flow response in human subjects. Clin Endocrinol (Oxf). 2004;61:724-731.
94. Dietz U, Tries HP, Merkle W, Jaursch-Hancke C, Lambertz H. Coronary artery flow reserve in diabetics with erectile dysfunction using sildenafil. Cardiovasc Diabetol. 2003;2:8.
95. Pop-Busui R, Kirkwood I, Schmid H, Marinescu V, Schroeder I, Larkin D, Yamada E, Raffel DM, Stevens MJ. Sympathetic dysfunction in type 1 diabetes: association with impaired myocardial blood flow reserve and diastolic dysfunction. J Am Coll Cardiol. 2004;44:2368-2374.
96. Yokoyama I, Yonekura K, Ohtake T, Yang W, Shin WS, Yamada N, Ohtomo K, Nagai R. Coronary microangiopathy in type 2 diabetic patients: relation to glycemic control, sex, and microvascular angina rather than to coronary artery disease. J Nucl Med. 2000;41:978-985.
97. Sasso FC, Carbonara O, Cozzolino D, Rambaldi P, Mansi L, Torella D, Gentile S, Turco S, Torella R, Salvatore T. Effects of insulin-glucose infusion on left ventricular function at rest and during dynamic exercise in healthy subjects and noninsulin dependent diabetic patients: a radionuclide ventriculographic study. J Am Coll Cardiol. 2000;36:219-226.
98. Huikuri HV, Airaksinen JK, Lilja M, Takkunen JT. Echocardiographic evaluation of left ventricular response to isometric exercise in young insulin-dependent diabetics. Acta Diabetol Lat. 1986;23:193-200.