Diabetes-related heart failure: Does diabetic cardiomyopathy exist?

Circulation Journal

Volumn 78, Issue 3, 2014, Pages 576-583

  Bando, Yasuko K ^a   Murohara, Toyoaki ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Diabetes mellitus; Heart failure; Pathology; Remodeling

Indexed keywords

BRAIN NATRIURETIC PEPTIDE; DIPEPTIDYL PEPTIDASE IV; HEMOGLOBIN A1C; METFORMIN;

AUTONOMIC NEUROPATHY; CARDIOVASCULAR RISK; CORONARY ARTERY DISEASE; CORONARY ARTERY OBSTRUCTION; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; GLUCOSE BLOOD LEVEL; HEART FAILURE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; HEMODYNAMIC PARAMETERS; HYPERTENSION; MICROVASCULOPATHY; OBESITY; REVIEW; THROMBOSIS; VASCULAR DISEASE; CORONARY STENOSIS; DIABETIC CARDIOMYOPATHIES; HEART STROKE VOLUME; HUMAN; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY;

CORONARY STENOSIS; DIABETIC CARDIOMYOPATHIES; HEART FAILURE; HUMANS; HYPERTENSION; STROKE VOLUME;

EID: 84894437604     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-13-1564     Document Type: Review

References (96)

1. Aguilar D, Bozkurt B, Ramasubbu K, Deswal A. Relationship of hemoglobin A1C and mortality in heart failure patients with diabetes. J Am Coll Cardiol 2009; 54: 422-428.
2. Ryden L, Grant PJ, Anker SD, Berne C, Cosentino F, Danchin N, et al. ESC Guidelines on diabetes, pre-diabetes, and cardiovascular diseases developed in collaboration with the EASD: The Task Force on diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and developed in collaboration with the European Association for the Study of Diabetes (EASD). Eur Heart J 2013; 34: 3035-3087.
3. Roger VL. Epidemiology of heart failure. Circ Res 2013; 113: 646-659.
4. Sakata Y, Shimokawa H. Epidemiology of heart failure in Asia. Circ J 2013; 77: 2209-2217.
5. Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, et al. 2013 ACCF/AHA guideline for the management of heart failure: A report of the American College of Cardiology Foundation/ American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2013; 62: e147-e239, doi:10.1016/j.jacc.2013.05.019.
6. Underwood PC, Adler GK. The renin angiotensin aldosterone system and insulin resistance in humans. Curr Hypertens Rep 2013; 15: 59-70.
7. Ogihara T, Asano T, Ando K, Chiba Y, Sakoda H, Anai M, et al. Angiotensin II-induced insulin resistance is associated with enhanced insulin signaling. Hypertension 2002; 40: 872-879.
8. Mori J, Zhang L, Oudit GY, Lopaschuk GD. Impact of the reninangiotensin system on cardiac energy metabolism in heart failure. J Mol Cell Cardiol 2013; 63: 98-106.
9. McMurray JJ, Holman RR, Haffner SM, Bethel MA, Holzhauer B, Hua TA, et al. Effect of valsartan on the incidence of diabetes and cardiovascular events. N Engl J Med 2010; 362: 1477-1490.
10. Yusuf S, Ostergren JB, Gerstein HC, Pfeffer MA, Swedberg K, Granger CB, et al. Effects of candesartan on the development of a new diagnosis of diabetes mellitus in patients with heart failure. Circulation 2005; 112: 48-53.
11. Braunwald E, Domanski MJ, Fowler SE, Geller NL, Gersh BJ, Hsia J, et al. Angiotensin-converting-enzyme inhibition in stable coronary artery disease. N Engl J Med 2004; 351: 2058-2068.
12. Kiencke S, Handschin R, von Dahlen R, Muser J, Brunner-Larocca HP, Schumann J, et al. Pre-clinical diabetic cardiomyopathy: Prevalence, screening, and outcome. Eur J Heart Fail 2010; 12: 951-957.
13. Davis TM, Coleman RL, Holman RR. Prognostic significance of silent myocardial infarction in newly diagnosed type 2 diabetes mellitus: United Kingdom Prospective Diabetes Study (UKPDS) 79. Circulation 2013; 127: 980-987.
14. Rubin J, Matsushita K, Ballantyne CM, Hoogeveen R, Coresh J, Selvin E. Chronic hyperglycemia and subclinical myocardial injury. J Am Coll Cardiol 2012; 59: 484-489.
15. Paulus WJ, Tschope C. A novel paradigm for heart failure with preserved ejection fraction: Comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation. J Am Coll Cardiol 2013; 62: 263-271.
16. Brooks BA, Franjic B, Ban CR, Swaraj K, Yue DK, Celermajer DS, et al. Diastolic dysfunction and abnormalities of the microcirculation in type 2 diabetes. Diabetes Obes Metab 2008; 10: 739-746.
17. Lam CS, Donal E, Kraigher-Krainer E, Vasan RS. Epidemiology and clinical course of heart failure with preserved ejection fraction. Eur J Heart Fail 2011; 13: 18-28.
18. Leyden E. Asthma and diabetes mellitus. Zeutschr Klin Med 1881; 3: 358-364.
19. Asghar O, Al-Sunni A, Khavandi K, Khavandi A, Withers S, Greenstein A, et al. Diabetic cardiomyopathy. Clin Sci (Lond) 2009; 116: 741-760.
20. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972; 30: 595-602.
21. Factor SM, Okun EM, Minase T. Capillary microaneurysms in the human diabetic heart. N Engl J Med 1980; 302: 384-388.
22. Fein FS, Sonnenblick EH. Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985; 27: 255-270.
23. Hamby RI, Zoneraich S, Sherman L. Diabetic cardiomyopathy. JAMA 1974; 229: 1749-1754.
24. Neely JR, Rovetto MJ, Oram JF. Myocardial utilization of carbohydrate and lipids. Prog Cardiovasc Dis 1972; 15: 289-329.
25. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 2007; 115: 3213-3223.
26. Ho JE, Lyass A, Lee DS, Vasan RS, Kannel WB, Larson MG, et al. Predictors of new-onset heart failure: Differences in preserved versus reduced ejection fraction. Circ Heart Fail 2013; 6: 279-286.
27. Lavie CJ, Milani RV, Ventura HO. Obesity and cardiovascular disease: Risk factor, paradox, and impact of weight loss. J Am Coll Cardiol 2009; 53: 1925-1932.
28. Wannamethee SG, Shaper AG, Whincup PH, Lennon L, Papacosta O, Sattar N. The obesity paradox in men with coronary heart disease and heart failure: The role of muscle mass and leptin. Int J Cardiol 2014; 171: 49-55.
29. Oreopoulos A, Padwal R, Kalantar-Zadeh K, Fonarow GC, Norris CM, McAlister FA. Body mass index and mortality in heart failure: A meta-analysis. Am Heart J 2008; 156: 13-22.
30. Komukai K, Minai K, Arase S, Ogawa T, Nakane T, Nagoshi T, et al. Impact of body mass index on clinical outcome in patients hospitalized with congestive heart failure. Circ J 2012; 76: 145-151.
31. Stratton IM, Adler AI, Neil HA, Matthews DR, Manley SE, Cull CA, et al. Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): Prospective observational study. BMJ 2000; 321: 405-412.
32. Kwon DH, Smedira NG, Rodriguez ER, Tan C, Setser R, Thamilarasan M, et al. Cardiac magnetic resonance detection of myocardial scarring in hypertrophic cardiomyopathy: Correlation with histopathology and prevalence of ventricular tachycardia. J Am Coll Cardiol 2009; 54: 242-249.
33. Higashimoto Y, Matsui T, Nishino Y, Taira J, Inoue H, Takeuchi M, et al. Blockade by phosphorothioate aptamers of advanced glycation endproducts-induced damage in cultured pericytes and endothelial cells. Microvasc Res 2013; 90: 64-70.
34. Cheung N, Wong TY. Diabetic retinopathy and systemic vascular complications. Prog Retin Eye Res 2008; 27: 161-176.
35. Fukami K, Yamagishi SI, Okuda S. Role of AGEs-RAGE system in cardiovascular disease. Curr Pharm Des 2013 June 20, doi:10.2174 /13816128113199990475.
36. Tahara N, Yamagishi S, Takeuchi M, Tahara A, Kaifu K, Ueda S, et al. Serum levels of advanced glycation end products (AGEs) are independently correlated with circulating levels of dipeptidyl peptidase-4 (DPP-4) in humans. Clin Biochem 2013; 46: 300-303.
37. Hatano R, Ohnuma K, Yamamoto J, Dang NH, Morimoto C. CD26-mediated co-stimulation in human CD8(+) T cells provokes effector function via pro-inflammatory cytokine production. Immunology 2013; 138: 165-172.
38. Zhong J, Rao X, Rajagopalan S. An emerging role of dipeptidyl peptidase 4 (DPP4) beyond glucose control: Potential implications in cardiovascular disease. Atherosclerosis 2013; 226: 305-314.
39. Murohara T. Dipeptidyl peptidase-4 inhibitor: Another player for cardiovascular protection. J Am Coll Cardiol 2012; 59: 277-279.
40. Matheeussen V, Jungraithmayr W, De Meester I. Dipeptidyl peptidase 4 as a therapeutic target in ischemia/reperfusion injury. Pharmacol Ther 2012; 136: 267-282.
41. Shigeta T, Aoyama M, Bando YK, Monji A, Mitsui T, Takatsu M, et al. Dipeptidyl peptidase-4 modulates left ventricular dysfunction in chronic heart failure via angiogenesis-dependent and-independent actions. Circulation 2012; 126: 1838-1851.
42. Lee SA, Kim YR, Yang EJ, Kwon EJ, Kim SH, Kang SH, et al. CD26/ DPP4 levels in peripheral blood and T cells in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 2013; 98: 2553-2561.
43. Matsubara J, Sugiyama S, Akiyama E, Iwashita S, Kurokawa H, Ohba K, et al. Dipeptidyl peptidase-4 inhibitor, sitagliptin, improves endothelial dysfunction in association with its anti-inflammatory effects in patients with coronary artery disease and uncontrolled diabetes. Circ J 2013; 77: 1337-1344.
44. Makdissi A, Ghanim H, Vora M, Green K, Abuaysheh S, Chaudhuri A, et al. Sitagliptin exerts an antinflammatory action. J Clin Endocrinol Metab 2012; 97: 3333-3341.
45. Cheung N, Wang JJ, Rogers SL, Brancati F, Klein R, Sharrett AR, et al. Diabetic retinopathy and risk of heart failure. J Am Coll Cardiol 2008; 51: 1573-1578.
46. Kurioka S, Ose H, Fukuma K, Yoshimoto K. Severity of diabetic retinopathy is associated with left ventricular diastolic dysfunction in patients with type 2 diabetes. Diabetes Res Clin Pract 2013; 99: 287-291.
47. Takeda Y, Sakata Y, Mano T, Ohtani T, Tamaki S, Omori Y, et al. Diabetic retinopathy is associated with impaired left ventricular relaxation. J Card Fail 2011; 17: 556-560.
48. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006; 20: 3347-3365.
49. Hudlicka O, Brown M, Egginton S. Angiogenesis in skeletal and cardiac muscle. Physiol Rev 1992; 72: 369-417.
50. Di Bello V, Giorgi D, Pedrinelli R, Talini E, Palagi C, Nardi C, et al. Coronary microcirculation into different models of left ventricular hypertrophy-hypertensive and athlete's heart: A contrast echocardiographic study. J Hum Hypertens 2003; 17: 253-263.
51. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: The search for a unifying hypothesis. Circ Res 2006; 98: 596-605.
52. 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.
53. Doenst T, Nguyen TD, Abel ED. Cardiac metabolism in heart fail ure: Implications beyond ATP production. Circ Res 2013; 113: 709-724.
54. Parra V, Verdejo HE, Iglewski M, Campo AD, Troncoso R, Jones D, et al. Insulin stimulates mitochondrial fusion and function in cardiomyocytes via the Akt-mTOR-NFkappaB-Opa-1 signaling pathway. Diabetes 2014; 63: 75-88.
55. Abel ED, O'Shea KM, Ramasamy R. Insulin resistance: Metabolic mechanisms and consequences in the heart. Arterioscler Thromb Vasc Biol 2012; 32: 2068-2076.
56. Shimizu I, Minamino T, Toko H, Okada S, Ikeda H, Yasuda N, et al. Excessive cardiac insulin signaling exacerbates systolic dysfunction induced by pressure overload in rodents. J Clin Invest 2010; 120: 1506-1514.
57. Monji A, Mitsui T, Bando YK, Aoyama M, Shigeta T, Murohara T. Glucagon-like peptide-1 receptor activation reverses cardiac remodeling via normalizing cardiac steatosis and oxidative stress in type 2 diabetes. Am J Physiol Heart Circ Physiol 2013; 305: H295-H304.
58. Ramirez E, Klett-Mingo M, Ares-Carrasco S, Picatoste B, Ferrarini A, Ruperez FJ, et al. Eplerenone attenuated cardiac steatosis, apoptosis and diastolic dysfunction in experimental type-II diabetes. Cardiovasc Diabetol 2013; 12: 172.
59. Noyan-Ashraf MH, Shikatani EA, Schuiki I, Mukovozov I, Wu J, Li RK, et al. A glucagon-like peptide-1 analog reverses the molecular pathology and cardiac dysfunction of a mouse model of obesity. Circulation 2013; 127: 74-85.
60. McGavock JM, Lingvay I, Zib I, Tillery T, Salas N, Unger R, et al. Cardiac steatosis in diabetes mellitus: A 1H-magnetic resonance spectroscopy study. Circulation 2007; 116: 1170-1175.
61. Rijzewijk LJ, van der Meer RW, Smit JW, Diamant M, Bax JJ, Hammer S, et al. Myocardial steatosis is an independent predictor of diastolic dysfunction in type 2 diabetes mellitus. J Am Coll Cardiol 2008; 52: 1793-1799.
62. Lan HY. Transforming growth factor-beta/Smad signalling in diabetic nephropathy. Clin Exp Pharmacol Physiol 2012; 39: 731-738.
63. Asbun J, Villarreal FJ. The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J Am Coll Cardiol 2006; 47: 693-700.
64. Zieman S, Kass D. Advanced glycation endproduct crosslinking: Pathophysiologic role and therapeutic target in cardiovascular disease [Review]. Congest Heart Fail 2004; 10: 144-149, quiz 150-151.
65. Cieslik KA, Trial J, Carlson S, Taffet GE, Entman ML. Aberrant differentiation of fibroblast progenitors contributes to fibrosis in the aged murine heart: Role of elevated circulating insulin levels. FASEB J 2013; 27: 1761-1771.
66. Van Linthout S, Seeland U, Riad A, Eckhardt O, Hohl M, Dhayat N, et al. Reduced MMP-2 activity contributes to cardiac fibrosis in experimental diabetic cardiomyopathy. Basic Res Cardiol 2008; 103: 319-327.
67. Grant PJ. Diabetes mellitus as a prothrombotic condition. J Intern Med 2007; 262: 157-172.
68. Davi G, Catalano I, Averna M, Notarbartolo A, Strano A, Ciabattoni G, et al. Thromboxane biosynthesis and platelet function in type II diabetes mellitus. N Engl J Med 1990; 322: 1769-1774.
69. Spectre G, Ostenson CG, Li N, Hjemdahl P. Postprandial platelet activation is related to postprandial plasma insulin rather than glucose in patients with type 2 diabetes. Diabetes 2012; 61: 2380-2384.
70. Santilli F, Formoso G, Sbraccia P, Averna M, Miccoli R, Di Fulvio P, et al. Postprandial hyperglycemia is a determinant of platelet activation in early type 2 diabetes mellitus. J Thromb Haemost 2010; 8: 828-837.
71. Cerbone AM, Macarone-Palmieri N, Saldalamacchia G, Coppola A, Di Minno G, Rivellese AA. Diabetes, vascular complications and antiplatelet therapy: Open problems. Acta Diabetol 2009; 46: 253-261.
72. Ogawa H, Nakayama M, Morimoto T, Uemura S, Kanauchi M, Doi N, et al. Low-dose aspirin for primary prevention of atherosclerotic events in patients with type 2 diabetes: A randomized controlled trial. JAMA 2008; 300: 2134-2141.
73. Granger DN, Rodrigues SF, Yildirim A, Senchenkova EY. Microvascular responses to cardiovascular risk factors. Microcirculation 2010; 17: 192-205.
74. Herrmann J, Kaski JC, Lerman A. Coronary microvascular dysfunction in the clinical setting: From mystery to reality. Eur Heart J 2012; 33: 2771-2782b.
75. Borlaug BA, Paulus WJ. Heart failure with preserved ejection fraction: Pathophysiology, diagnosis, and treatment. Eur Heart J 2011; 32: 670-679.
76. Lane DJ, Huang ML, Ting S, Sivagurunathan S, Richardson DR. Biochemistry of cardiomyopathy in the mitochondrial disease Friedreich's ataxia. Biochem J 2013; 453: 321-336.
77. Faden G, Faganello G, De Feo S, Berlinghieri N, Tarantini L, Di Lenarda A, et al. The increasing detection of asymptomatic left ventricular dysfunction in patients with type 2 diabetes mellitus without overt cardiac disease: Data from the SHORTWAVE study. Diabetes Res Clin Pract 2013; 101: 309-316.
78. Ernande L, Rietzschel ER, Bergerot C, De Buyzere ML, Schnell F, Groisne L, et al. Impaired myocardial radial function in asymptomatic patients with type 2 diabetes mellitus: A speckle-tracking imaging study. J Am Soc Echocardiogr 2010; 23: 1266-1272.
79. Miki T, Yuda S, Kouzu H, Miura T. Diabetic cardiomyopathy: Pathophysiology and clinical features. Heart Fail Rev 2013; 18: 149-166.
80. Roumie CL, Hung AM, Greevy RA, Grijalva CG, Liu X, Murff HJ, et al. Comparative effectiveness of sulfonylurea and metformin monotherapy on cardiovascular events in type 2 diabetes mellitus: A cohort study. Ann Intern Med 2012; 157: 601-610.
81. Matsushita K, Blecker S, Pazin-Filho A, Bertoni A, Chang PP, Coresh J, et al. The association of hemoglobin A1c with incident heart failure among people without diabetes: The atherosclerosis risk in communities study. Diabetes 2010; 59: 2020-2026.
82. Banerjee D, Biggs ML, Mercer L, Mukamal K, Kaplan R, Barzilay J, et al. Insulin resistance and risk of incident heart failure: Cardiovascular Health Study. Circ Heart Fail 2013; 6: 364-370.
83. Witteles RM, Fowler MB. Insulin-resistant cardiomyopathy clinical evidence, mechanisms, and treatment options. J Am Coll Cardiol 2008; 51: 93-102.
84. Balkau B, Hu G, Qiao Q, Tuomilehto J, Borch-Johnsen K, Pyorala K. Prediction of the risk of cardiovascular mortality using a score that includes glucose as a risk factor. The DECODE Study. Diabetologia 2004; 47: 2118-2128.
85. Tominaga M, Eguchi H, Manaka H, Igarashi K, Kato T, Sekikawa A. Impaired glucose tolerance is a risk factor for cardiovascular disease, but not impaired fasting glucose: The Funagata Diabetes Study. Diabetes Care 1999; 22: 920-924.
86. Shimabukuro M, Higa N, Asahi T, Yamakawa K, Oshiro Y, Higa M, et al. Impaired glucose tolerance, but not impaired fasting glucose, underlies left ventricular diastolic dysfunction. Diabetes Care 2011; 34: 686-690. ure: Implications beyond ATP production. Circ Res 2013; 113: 709-724.
87. Stahrenberg R, Edelmann F, Mende M, Kockskamper A, Dungen HD, Scherer M, et al. Association of glucose metabolism with diastolic function along the diabetic continuum. Diabetologia 2010; 53: 1331-1340.
88. Wang TJ, Larson MG, Keyes MJ, Levy D, Benjamin EJ, Vasan RS. Association of plasma natriuretic peptide levels with metabolic risk factors in ambulatory individuals. Circulation 2007; 115: 1345-1353.
89. Miyashita K, Itoh H, Tsujimoto H, Tamura N, Fukunaga Y, Sone M, et al. Natriuretic peptides/cGMP/cGMP-dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes 2009; 58: 2880-2892.
90. Proost P, Struyf S, Schols D, Opdenakker G, Sozzani S, Allavena P, et al. Truncation of macrophage-derived chemokine by CD26/dipeptidyl- peptidase IV beyond its predicted cleavage site affects chemotactic activity and CC chemokine receptor 4 interaction. J Biol Chem 1999; 274: 3988-3993.
91. Ohnuma K, Dang NH, Morimoto C. Revisiting an old acquaintance: CD26 and its molecular mechanisms in T cell function. Trends Immunol 2008; 29: 295-301.
92. dos Santos L, Salles TA, Arruda-Junior DF, Campos LC, Pereira AC, Barreto AL, et al. Circulating dipeptidyl peptidase IV activity correlates with cardiac dysfunction in human and experimental heart failure. Circ Heart Fail 2013; 6: 1029-1038.
93. Ravassa S, Barba J, Coma-Canella I, Huerta A, Lopez B, Gonzalez A, et al. The activity of circulating dipeptidyl peptidase-4 is associated with subclinical left ventricular dysfunction in patients with type 2 diabetes mellitus. Cardiovasc Diabetol 2013; 12: 143.
94. Vinik AI, Ziegler D. Diabetic cardiovascular autonomic neuropathy. Circulation 2007; 115: 387-397.
95. Sacre JW, Franjic B, Jellis CL, Jenkins C, Coombes JS, Marwick TH. Association of cardiac autonomic neuropathy with subclinical myocardial dysfunction in type 2 diabetes. JACC Cardiovasc Imaging 2010; 3: 1207-1215.
96. Ma RC, Chan JC. Type 2 diabetes in East Asians: Similarities and differences with populations in Europe and the United States. Ann N Y Acad Sci 2013; 1281: 64-91.