Skip to main content
Log in

Diabetic cardiomyopathy—fact or fiction?

Diabetische Kardiomyopathie – Fakt oder Fiktion?

  • Main topic/CME
  • Published:
Herz Aims and scope Submit manuscript

Abstract

Epidemiologic as well as clinical studies confirm the close link between diabetes mellitus and heart failure. Diabetic cardiomyopathy (DCM) is still a poorly understood “entity”, however, with several contributing pathogenetic factors which lead in different stages of diabetes to characteristic clinical phenotypes. Hyperglycemia with a shift from glucose metabolism to increased beta-oxidation and consecutive free fatty acid damage (lipotoxicity) to the myocardium, insulin resistance, renin-angiotensin-aldosterone system (RAAS) activation, altered calcium homeostasis and structural changes from the natural collagen network to a stiffer matrix due to advanced glycation endproduct (AGE) formation, hypertrophy and fibrosis contribute to the respective clinical phenotypes of DCM.

We propose the following classification of cardiomyopathy in diabetic patients:

  1. a)

    Diastolic heart failure with normal ejection fraction (HFNEF) in diabetic patients often associated with hypertrophy without relevant hypertension. Relevant coronary artery disease (CAD), valvular disease and uncontrolled hypertension are not present. This is referred to as stage 1 DCM.

  2. b)

    Systolic and diastolic heart failure with dilatation and reduced ejection (HFREF) in diabetic patients excluding relevant CAD, valvular disease and uncontrolled hypertension as stage 2 DCM.

  3. c)

    Systolic and/or diastolic heart failure in diabetic patients with small vessel disease (microvascular disease) and/or microbial infection and/or inflammation and/or hypertension but without CAD as stage 3 DCM.

  4. d)

    If heart failure may also be attributed to infarction or ischemia and remodeling in addition to stage 3 DCM the term should be heart failure in diabetes or stage 4 DCM.

These clinical phenotypes of diabetic cardiomyopathy can be separated by biomarkers, non-invasive (echocardiography, cardiac magnetic resonance imaging) and invasive imaging methods (levocardiography, coronary angiography) and further analysed by endomyocardial biopsy for concomitant viral infection. The role of specific diabetic drivers to the clinical phenotypes, to macro- and microangiopathy as well as accompanying risk factors or confounders, e.g. hypertension, autoimmune factors or inflammation with or without viral persistence, need to be identified in each individual patient separately. Thus hyperglycemia, hyperinsulinemia and insulin resistance as well as lipotoxicity by free fatty acids (FFAs) are the factors responsible for diabetic cardiomyopathy. In stage 1 and 2 DCM diabetic cardiomyopathy is clearly a fact. However, precise determination of to what degree the various underlying pathogenetic processes are responsible for the overall heart failure phenotype remains a fiction.

Zusammenfassung

Diabetes mellitus und Herzinsuffizienz treten häufig gemeinsam auf. Aus der Koinzidenz wird mit dem Begriff diabetische Kardiomyopathie (DCM) ein Zusammenhang beschrieben, der hinsichtlich Ätiologie, Pathogenese und klinischem Phänotyp bislang nur unzureichend präzisiert ist. Hyperglykämie bei gleichzeitiger Insulinresistenz führt zu einer Hochregulation der β-Oxidation. Freie Fettsäuren (FFA) decken bis zu 90% des myokardialen Energiebedarfs, anders als beim Gesunden, bei dem der Anteil der FFA nur 50% ausmacht. Die intramyokardiale FFA-Akkumulation führt zu Lipotoxizität und zu einer gestörten Kalziumhomöostase, die Bindung der FFAs an interstitielles und perivaskulären Kollagen zu „advanced glycation endproducts“ (AGE) und damit zu vermehrter Steifigkeit, Hypertrophie und additiver Fibrose. Der Diabetes mellitus umfasst als weitere Folge mikrovaskuläre Veränderungen („small vessel disease“) sowie eine Prädisposition für Infektionen und autoimmune, inflammatorische Prozesse, die den Phänotyp einer DCM ebenso prägen können wie eine begleitende arterielle Hypertonie oder eine koronare Herzerkrankung.

Wir schlagen eine Klassifikation vor, die der Pathogenese, der zeitlichen Entwicklung und dem klinischen wie hämodynamischen Phänotyp Rechnung trägt:

DCM-Stufe 1: Diastolische Herzinsuffizienz bei Diabetespatienten mit normaler Ejektionsfraktion („heart failure with normal ejection fraction“, HFNEF). Hier überwiegt häufig eine Hypertrophie ohne Hochdruck.

DCM-Stufe 2: Systolische und diastolische Herzinsuffizienz mit optionaler linksventrikulärer Dilatation, aber reduzierter Ejektionsfraktion (<50%) als HFREF („heart failure with reduced ejection fraction“).

DCM-Stufe 3: Systolische und diastolische Herzinsuffizienz (wie Stufe 2), aber mit mehreren additiven, nur indirekt diabetesvermittelten Begleiterkrankungen, wie Mikrovaskulopathie, myokardialer Infektion/Inflammation oder arterieller Hypertonie.

DCM-Stufe 4: Herzinsuffizienz bei Patienten mit Diabetes mellitus, d. h. DCM-Stufe 3, zusätzlich eine koronare Herzerkrankung mit Infarkt und Remodelling.

Die Charakterisierung der vier DCM-Formen erfolgt mit den serologischen Biomarkern der Herzinsuffizienz (BNP, NTproBNP), der Nekrose (Troponine) und der Fibrose (MMPs und TIMPs), mit nichtinvasiver Bildgebung (Echokardiographie, Doppler/TDI, Kardio-MRT) und invasiver Katheterdiagnostik einschließlich Koronarangiographie und Endomyokardbiopsie. Die DCM ist für die Formen 1 und 2 etablierter Fakt. Doch den jeweiligen Anteil pathogenetischer Faktoren aller 4 DCM-Stufen an der Herzinsuffizienz/Kardiomyopathie des jeweiligen Patienten mit diesen Methoden quantitativ bestimmen zu können, bleibt eine Fiktion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Abe T, Ohga Y, Tabayashi N et al (2002) Left ventricular diastolic dysfunction in type 2 diabetes mellitus model rats. Am J Physiol Heart Circ Physiol 282:H138–H148

    PubMed  CAS  Google Scholar 

  2. Achenbach S, Ropers D, Regenfus M et al (2001) Noninvasive coronary angiography by magnetic resonance imaging, electron-beam computed tomography, and multislice computed tomography. Am J Cardiol 88(2A):70E–73E

    Article  PubMed  CAS  Google Scholar 

  3. Alter P, Grimm W, Vollrath A et al (2006) Heart rate variability in patients with cardiac hypertrophy – relation to left ventricular mass and etiology. Am Heart J 151(4):829–836

    Article  PubMed  Google Scholar 

  4. Alter P, Rupp H, Rominger MB et al (2010) Late gadolinium enhancement is associated with increased left ventricular wall stress and mass in patients with non-ischemic cardiomyopathy. Eur Heart J 31(Supp 1):282

    Google Scholar 

  5. Alter P, Rupp H, Rominger MB et al (2008) B-type natriuretic peptide and wall stress in dilated human heart. Mol Cell Biochem 314(1–2):179–191

    Google Scholar 

  6. Alter P, Rupp H, Rominger MB et al (2008) A new methodological approach to assess cardiac work by pressure-volume and stress-length relations in patients with aortic valve stenosis and dilated cardiomyopathy. Pfluegers Arch 455(4):627–636

    CAS  Google Scholar 

  7. Alter P, Rupp H, Rominger MB et al (2007) Relation of B-type natriuretic peptide to left ventricular wall stress as assessed by cardiac magnetic resonance imaging in patients with dilated cardiomyopathy. Can J Physiol Pharmacol 85(8):790–799

    Article  PubMed  CAS  Google Scholar 

  8. Alter P, Rupp H, Maisch B (2008) Assessment and relevance of ventricular wall stress in heart failure. Eur Heart J 29(18):2316

    Article  PubMed  Google Scholar 

  9. Alter P, Rupp H, Stoll F et al (2010) Left ventricular hypertrophy follows increased enddiastolic wall stress in patients with dilative heart failure. Clin Res Cardiol 99(Suppl 2). DOI: 10.1007/s00392-010-1200-0

  10. Aneja A, Tang WH, Bansilal S et al (2008) Diabetic cardiomyopathy: insights into pathogenesis, diagnostic challenges, and therapeutic options. Am J Med 121(9):748–757

    Article  PubMed  Google Scholar 

  11. Argirova MD, Ortwerth BJ (2003) Activation of protein-bound copper ions during early glycation: study on two proteins. Arch Biochem Biophys 420:176–184

    Article  PubMed  CAS  Google Scholar 

  12. Aronow WS, Ahn C (1999) Incidence of heart failure in 2,737 older persons with and without diabetes mellitus. Chest 115:867–868

    Article  PubMed  CAS  Google Scholar 

  13. Bell DS (2003) Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 26(8):2433–2441

    Article  PubMed  Google Scholar 

  14. Bella JN, Devereux RB, Roman MJ et al (2001) Separate and joint effects of systemic hypertension and diabetes mellitus on left ventricular structure and function in American Indians (the Strong Heart Study). Am J Cardiol 87:1260–1265

    Article  PubMed  CAS  Google Scholar 

  15. Bertoni AG, Goff DC Jr, D’Agostino RB Jr et al (2006) Diabetic cardiomyopathy and subclinical cardiovascular disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Diabetes Care 29(3):588–594

    Article  PubMed  Google Scholar 

  16. Bertoni AG, Tsai A, Kasper EK, Brancati FL (2003) Diabetes and idiopathic cardiomyopathy: a nationwide case-control study. Diabetes Care 26:2791–2795

    Article  PubMed  Google Scholar 

  17. Boudina S, Abel ED (2006) Mitochondrial uncoupling: a key contributor to reduced cardiac efficiency in diabetes. Physiology 21:250–258

    Article  PubMed  CAS  Google Scholar 

  18. Boudina S, Abel ED (2007) Diabetic cardiomyopathy revisited. Circulation 115:3213–3223

    Article  PubMed  Google Scholar 

  19. Boudina S, Abel ED (2010) Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 11:31–39

    Article  PubMed  Google Scholar 

  20. Boyer JK, Thanigaraj S, Schechtman KB et al (2004) Prevalence of ventricular diastolic dysfunction in asymptomatic, normotensive patients with diabetes mellitus. Am J Cardiol 93:870–875

    Article  PubMed  Google Scholar 

  21. Brilla CG (2000) Regression of myocardial fibrosis in hypertensive heart disease: diverse effects of various antihypertensive drugs. Cardiovasc Res 46:324–331

    Article  PubMed  CAS  Google Scholar 

  22. Brilla CG, Funck RC, Rupp H (2000) Lisinopril-mediated regression of myocardial fibrosis in patients with hypertensive heart disease. Circulation 102:1388–1393

    PubMed  CAS  Google Scholar 

  23. Cai L, Wang Y, Zhou G et al (2006) Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol 48:1688–1697

    Article  PubMed  CAS  Google Scholar 

  24. Charoenpanichkit C, Morgan TM, Hamilton CA et al (2010) Left ventricular hypertrophy influences cardiac prognosis in patients undergoing dobutamine cardiac stress testing. Circ Cardiovasc Imaging 3(4):392–397

    Article  PubMed  Google Scholar 

  25. Dhalla NS, Liu X, Panagia V, Takeda N (1998) Subcellular remodeling and heart dysfunction in chronic diabetes. Cardiovasc Res 40(2):239–247

    Article  PubMed  CAS  Google Scholar 

  26. Devereux RB, Roman MJ, Paranicas M et al (2000) Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 101(19):2271–2276

    PubMed  CAS  Google Scholar 

  27. Eckel J, Reinauer H (1990) Insulin action on glucose transport in isolated cardiac myocytes: signalling pathways and diabetes-induced alterations. Biochem Soc Trans 18:1125–1127

    PubMed  CAS  Google Scholar 

  28. Elliott P, Andersson B, Arbustini E et al (2008) Classification of the cardiomyopathies: a position statement from the European Society Of Cardiology Working Group on Myocardial and Pericardial Diseases. 29(2):270–276

  29. Fang ZY, Prins JB, Marwick TH (2004) Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 25(4):543–567

    Article  PubMed  CAS  Google Scholar 

  30. Fiordaliso F, Leri A, Cesselli D et al (2001) Hyperglycemia activates p53 and p53-regulated genes leading to myocyte cell death. Diabetes 50:2363–2375

    Article  PubMed  CAS  Google Scholar 

  31. Gebker R, Mirelis JG, Jahnke C et al (2010) Influence of left ventricular hypertrophy and geometry on diagnostic accuracy of wall motion and perfusion magnetic resonance during dobutamine stress. Circ Cardiovasc Imaging 3(5):507–514

    Article  PubMed  Google Scholar 

  32. Ha JW, Lee HC, Kang ES et al (2007) Abnormal left ventricular longitudinal functional reserve in patients with diabetes mellitus: implication for detecting subclinical myocardial dysfunction using exercise tissue Doppler echocardiography. Heart 93(12):1571–1576

    Article  PubMed  Google Scholar 

  33. Havers J, Haude M, Erbel R, Spiller P (2008) Röntgendensitometische Messung der myokardialen Perfusionsreserve bei symptomatischen Patienten ohne angiographisch detektierbare Koronarstenosen. Herz 33:223–232

    Article  PubMed  Google Scholar 

  34. Herrero P, Peterson LR, McGill JB et al (2006) Increased myocardial fatty acid metabolism in patients with type 1 diabetes mellitus. J Am Coll Cardiol 47:598–604

    Article  PubMed  CAS  Google Scholar 

  35. Hunt SA, American College of Cardiology, American Heart Association Task Force on Practice Guidelines (Writing Committee to Update the 2001 Guidelines for the Evaluation, Management of Heart Failure) (2005) ACC/AHA 2005 guideline update for the diagnosis and management of chronic heart failure in the adult: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Update the 2001 Guidelines for the Evaluation and Management of Heart Failure). JACC 46(6):e1–e82

    PubMed  Google Scholar 

  36. Iltis I, Kober F, Desrois M et al (2005) Defective myocardial blood flow and altered function of the left ventricle in type 2 diabetic rats: a noninvasive in vivo study using perfusion and cine magnetic resonance imaging. Invest Radiol 40(1):19–26

    PubMed  Google Scholar 

  37. Iribarren C, Karter AJ, Go AS et al (2001) Glycemic control and heart failure among adult patients with diabetes. Circulation 103:2668–2673

    PubMed  CAS  Google Scholar 

  38. Islam KN, Takahashi M, Higashiyama S et al (1995) Fragmentation of ceruloplasmin following nonenzymatic glycation reaction. J Biochem 118:1054–1060

    PubMed  CAS  Google Scholar 

  39. Jahnke C, Nagel E, Gebker R et al (2007) Prognostic value of cardiac magnetic resonance stress tests: adenosine stress perfusion and dobutamine stress wall motion imaging. Circulation 115(13):1769–1776

    Article  PubMed  Google Scholar 

  40. Kannel WB, McGee DL (1979) Diabetes and cardiovascular disease: the Framingham study. JAMA 241:2035–2038

    Article  PubMed  CAS  Google Scholar 

  41. Khavandi K, Khavandi A, Asghar O et al (2009) Diabetic cardiomyopathy-a distinct disease? Best Pract Res Clin Endocrinol Metab 23(3):347–360

    Article  PubMed  Google Scholar 

  42. Liang Q, Carlson EC, Donthi RV et al (2002) Overexpression of metallothionein reduces diabetic cardiomyopathy. Diabetes 51:174–181

    Article  PubMed  CAS  Google Scholar 

  43. Liedtke AJ, DeMaison L, Eggleston AM et al (1988) Changes in substrate metabolism and effects of excess fatty acids in reperfused myocardium. Circ Res 62:535–542

    PubMed  CAS  Google Scholar 

  44. Liu GX, Hanley PJ, Ray J, Daut J (2001) Long-chain acylcoenzyme A esters and fatty acids directly link metabolism to K (ATP) channels in the heart. Circ Res 88(9):918–924

    Article  PubMed  CAS  Google Scholar 

  45. Lundbaek K (1954) Diabetic angiopathy: a specific vascular disease. Lancet 266:377–379

    Article  PubMed  CAS  Google Scholar 

  46. Ma H, Li AY, Xu P et al (2009) Advanced glycation endproduct (AGE) accumulation and AGE receptor (RAGE) upregulation contribute to the onset of diabetic cardiomyopathy. J Cell Mol Med 13(8B):1751–1764

    Article  PubMed  Google Scholar 

  47. Maisch B (2006) Obesity, diabetes mellitus and metabolic syndrome: the implications for heart and the vascular system. Herz 31(3):185–188

    Article  PubMed  Google Scholar 

  48. Maisch B, Hufnagel G, Kölsch S et al (2004) Treatment of inflammatory dilated cardiomyopathy and myocarditis with immunosuppression and i.v. immunoglobulins. Herz 29:624–636

    Article  PubMed  Google Scholar 

  49. Maisch B, Pankuweit S, Karatolios K, Ristić AD (2006) Invasive techniques – from diagnosis to treatment. Rheumatology (Oxford) 45(Suppl 4):iv32–iv38

    Google Scholar 

  50. Maisch B, Richter A, Koelsch S et al (2006) Management of patients with suspected (peri-)myocarditis and inflammatory dilated cardiomyopathy. Herz 31(9):881–890

    Article  PubMed  Google Scholar 

  51. Maisch B, Rupp H (2006) Myocardial fibrosis: a cardiopathophysiologic Janus head. Herz 31(3):260–268

    Article  PubMed  Google Scholar 

  52. Maisch B, Seferovic PM, Ristic AD et al (2004) The Task Force on the Diagnosis and Management of Pericardial Diseases of the European Society of Cardiology. Guidelines on the diagnosis and management of pericardial diseases executive summary; The Task force on the diagnosis and management of pericardial diseases of the European Society of Cardiology Eur Heart J 25(7):587–610

  53. Maksimović R, Dill T, Seferović PM et al (2006) Magnetic resonance imaging in pericardial diseases. Indications and diagnostic value. Herz 31(7):708–714

    Article  PubMed  Google Scholar 

  54. Malhotra A, Sanghi V (1997) Regulation of contractile proteins in diabetic heart. Cardiovasc Res 34:34–40

    Article  PubMed  CAS  Google Scholar 

  55. Matsushima S, Kinugawa S, Ide T et al (2006) Overexpression of glutathione peroxidase attenuates myocardial remodeling and preserves diastolic function in diabetic heart. Am J Physiol Heart Circ Physiol 291:H2237–H2245

    Article  PubMed  CAS  Google Scholar 

  56. Maya L, Villarreal FJ (2010) Diagnostic approaches for diabetic cardiomyopathy and myocardial fibrosis. J Mol Cell Cardiol 48:524–529

    Article  PubMed  CAS  Google Scholar 

  57. McGavock JM, Lingvay I, Zib I et al (2007) Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 116:1170–1175

    Article  PubMed  Google Scholar 

  58. Murray AG, Anderson RE, Watson GC et al (2004) Uncoupling proteins in human heart. Lancet 364:1786–1788

    Article  PubMed  CAS  Google Scholar 

  59. Nagel E, Lorenz C, Baer F et al (2001) Stress cardiovascular magnetic resonance: consensus panel report. J Cardiovasc Magn Reson 3(3):267–281

    Article  PubMed  CAS  Google Scholar 

  60. Neubauer S, Krahe T, Schindler R et al (1992) 31P magnetic resonance spectroscopy in dilated cardiomyopathy and coronary artery disease. Altered cardiac high-energy phosphate metabolism in heart failure. Circulation 86(6):1810–1818

    PubMed  CAS  Google Scholar 

  61. Neubauer S, Horn M, Cramer M et al (1997) Myocardial phosphocreatine-to-ATP ratio is a predictor of mortality in patients with dilated cardiomyopathy. Circulation 96(7):2190–2196

    PubMed  CAS  Google Scholar 

  62. Neubauer S (2007) The failing heart-an engine out of fuel. N Engl J Med 356(11):1140–1151

    Article  PubMed  Google Scholar 

  63. Ng ACT, Delgado V, Bertini M et al (2009) Findings from left ventricular strain and strain rate imaging in asymptomatic patients with type 2 diabetes mellitus. Am J Cardiol 104:1398–1401

    Article  PubMed  Google Scholar 

  64. Nichols GA, Hillier TA, Erbey JR, Brown JB (2001) Congestive heart failure in type 2 diabetes: prevalence, incidence, and risk factors. Diabetes Care 24:1614–1619

    Article  PubMed  CAS  Google Scholar 

  65. Palmieri V, Capaldo B, Russo C et al (2008) Uncomplicated type 1 diabetes and preclinical left ventricular myocardial dysfunction: insights from echocardiography and exercise cardiac performance evaluation. Diabetes Res Clin Pract 79(2):262–268

    Article  PubMed  Google Scholar 

  66. Pankuweit S, Funck R, Grimm W, Maisch B (2006) Diagnosis and treatment of inflammatory heart diseases: role of endomyocardial biopsy. Herz 31(4):361–365

    Article  PubMed  Google Scholar 

  67. Pankuweit S, Ruppert V, Maisch B (2004) Inflammation in dilated cardiomyopathy. Herz 29(8):788–793

    Article  PubMed  Google Scholar 

  68. Paulus WJ, Tschöpe C, Sanderson JE et al (2007) How to diagnose diastolic heart failure: a consensus statement on the diagnosis of heart failure with normal left ventricular ejection fraction by the Heart Failure and Echocardiography Associations of the European Society of Cardiology. Eur Heart J 28(20):2539–2550

    Article  PubMed  Google Scholar 

  69. Peterson LR, Herrero P, Schechtman KB et al (2004) Effect of obesity and insulin resistance on myocardial substrate metabolism and efficiency in young women. Circulation 109:2191–2196

    Article  PubMed  Google Scholar 

  70. Pogatsa G (2001) Metabolic energy metabolism in diabetes: therapeutic implications. Coron Artery Dis 12(Suppl 1):S29–S33

    PubMed  Google Scholar 

  71. Portig I, Maisch B (2004) Noninvasive methods in the diagnosis of macro- and microangiopathy of peripherial and carotid arteries. Herz 29(1):17–25

    Article  PubMed  Google Scholar 

  72. Regan TJ, Lyons MM, Ahmed SS et al (1977) Evidence for cardiomyopathy in familial diabetes mellitus. J Clin Invest 60(4):884–899

    Article  PubMed  CAS  Google Scholar 

  73. Richardson P, McKenna W, Bristow M et al (1996) Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies. Circulation 93(5):841–842

    PubMed  CAS  Google Scholar 

  74. Rijzewijk LJ, Meer RW van der, Lamb HJ et al (2009) Altered myocardial substrate metabolism and decreased diastolic function in nonischemic human diabetic cardiomyopathy: studies with cardiac positron emission tomography and magnetic resonance imaging. J Am Coll Cardiol 54:1524–1532

    Article  PubMed  CAS  Google Scholar 

  75. Rodrigues B, Camm MC, Mcneill GH (1998) Metabolic disturbances in diabetic cardiomyopathy. Mol Cell Biochem 180:53–57

    Article  PubMed  CAS  Google Scholar 

  76. Rubler S, Dlugash J, Yuceoglu YZ et al (1972) New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30(6):595–602

    Article  PubMed  CAS  Google Scholar 

  77. Ryden L, Standl E, Bartnik M et al (2007) Guidelines on diabetes, pre-diabetes, and cardiovascular diseases: executive summary. The Task Force on Diabetes and Cardiovascular Diseases of the European Society of Cardiology (ESC) and of the European Association for the Study of Diabetes (EASD). Eur Heart J 28(1):88–136

    Article  PubMed  CAS  Google Scholar 

  78. Schneider CA, Pfister R, Erdmann E (2010) Diabetes and heart failure. Herz 35(3):140–146

    Article  PubMed  Google Scholar 

  79. Scognamiglio R, Avogaro A, Casara D et al (1998) Myocardial dysfunction and adrenergic cardiac innervations in patients with insulin-dependent diabetes mellitus. J Am Coll Cardiol 31(2):404–412

    Article  PubMed  CAS  Google Scholar 

  80. Shen X, Zheng S, Metreveli NS, Epstein PN (2006) Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes 55:798–805

    Article  PubMed  CAS  Google Scholar 

  81. Shimazu M, Umeda K, Sugihara N et al (1993) Collagen remodelling in myocardia of diabetic patients. J Clin Path 46:32–36

    Article  Google Scholar 

  82. Soufi M, Sattler AM, Herzum M et al (2006) Molecular basis of obesity and the risk for cardiovascular disease. Herz 31(3):200–206

    Article  PubMed  Google Scholar 

  83. Stratmann B, Gawlowski T, Tschoepe D (2010) Diabetic cardiomyopathy-to take a long story serious. Herz 35(3):161–168

    Article  PubMed  Google Scholar 

  84. Stratmann B, Stork I, Tschoepe D (2008) Diabetic cardiomyopathy-a type of coronary artery disease? Internist 49(4):436–440

    Article  PubMed  CAS  Google Scholar 

  85. Stratton IM, Adler AI, Neil HA et al (2000) Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 321:405–412

    Article  PubMed  CAS  Google Scholar 

  86. Swan GW, Anker SD, Walton C et al (1997) Insulin resistance in chronic failure: relation to severity and etiology of heart failure. J Am Coll Cardiol 30:527–532

    Article  PubMed  CAS  Google Scholar 

  87. Taegtmeyer H (2004) Cardiac metabolism as a target for the treatment of heart failure. Circulation 110:894–896

    Article  PubMed  Google Scholar 

  88. Takeda N, Nakamura I, Hatanaka T et al (1988) Myocardial mechanical and myosin isoenzyme alterations in streptozotocin-diabetic rats. Jpn Heart J 29:455–463

    PubMed  CAS  Google Scholar 

  89. Tarquini R, Lazzeri C, Pala L et al (2010) The diabetic cardiomyopathy. Acta Diabetol. DOI: 10.1007/s00592-010-0180-x

  90. Von Bibra H, Sutton J St M (2010) Diastolic dysfunction in diabetes and the metabolic syndrome: promising potential for diagnosis and prognosis. Diabetologia 53:1033–1045

    Article  Google Scholar 

  91. Wachter R, Lüers C, Leta S et al (2007) Impact of diabetes on left ventricular diastolic function in patients with arterial hypertension. Eur J Heart Fail 9:469–476

    Article  PubMed  Google Scholar 

  92. Westermann D, Walther T, Savvatis K et al (2009) Gene deletion of the kinin receptor B1 attenuates cardiac inflammation and fibrosis during the development of experimental diabetic cardiomyopathy. Diabetes 58(6):1373–1381

    Article  PubMed  Google Scholar 

  93. Yim MB, Yim HS, Lee C et al (2001) Protein glycation: creation of catalytic sites for free radical generation. Ann N Y Acad Sci 928:48–53

    Article  PubMed  CAS  Google Scholar 

  94. Yu X, Tesiram YA, Towner RA et al (2007) Early myocardial dysfunction in streptozotocin-induced diabetic mice: a study using in vivo magnetic resonance imaging (MRI). Cardiovasc Diabetol 6:6

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

The corresponding author states that there are no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. Maisch.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maisch, B., Alter, P. & Pankuweit, S. Diabetic cardiomyopathy—fact or fiction?. Herz 36, 102–115 (2011). https://doi.org/10.1007/s00059-011-3429-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00059-011-3429-4

Keywords

Schlüsselwörter

Navigation