Coronary microvascular dysfunction in diabetes mellitus

Journal of International Medical Research

Volumn 45, Issue 6, 2017, Pages 1901-1929

  Kibel, Aleksandar ^a,b   Selthofer Relatic, Kristina ^a,b   Drenjancevic, Ines ^b   Bacun, Tatjana ^a,b   Bosnjak, Ivica ^a   Kibel, Dijana ^a,b   Gros, Mario ^a,b  

^a UNIVERSITY HOSPITAL OSIJEK   (Croatia)

^b JOSIP JURAJ STROSSMAYER UNIVERSITY OF OSIJEK   (Croatia)

Author keywords

arachidonic acid metabolites; artery; cardiomyopathy; coronary microvascular dysfunction; Diabetes mellitus; endothelial dysfunction; microcirculation; nitric oxide

Indexed keywords

ACETYLSALICYLIC ACID; ADENOSINE RECEPTOR BLOCKING AGENT; ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTIANGINA PECTORIS AGENT; ARACHIDONIC ACID; ATORVASTATIN; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CALCIUM CHANNEL BLOCKING AGENT; CARVEDILOL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIN A RECEPTOR ANTAGONIST; EPLERENONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INSULIN; IVABRADINE; LOOP DIURETIC AGENT; METFORMIN; MIBEFRADIL; NEBIVOLOL; NICORANDIL; NITRIC ACID DERIVATIVE; NITRIC OXIDE; QUINAPRIL; RANOLAZINE; REACTIVE OXYGEN METABOLITE; RHO KINASE INHIBITOR; TRIMETAZIDINE; UNINDEXED DRUG; VANILLOID RECEPTOR 1;

ARTICLE; CARDIOVASCULAR DISEASE; CORONARY ARTERY DISEASE; CORONARY MICROVASCULAR DYSFUNCTION; DIABETES MELLITUS; DIABETIC CARDIOMYOPATHY; DIABETIC MICROANGIOPATHY; DIAGNOSTIC TEST; DISEASE ASSOCIATION; ENDOTHELIAL DYSFUNCTION; GLUCOSE BLOOD LEVEL; HUMAN; HYPERGLYCEMIA; INVASIVE PROCEDURE; NON INVASIVE PROCEDURE; NONHUMAN; PROGNOSIS; VASCULAR DISEASE; ALGORITHM; BLOOD; CORONARY BLOOD VESSEL; MICROCIRCULATION; MICROVASCULATURE; PATHOPHYSIOLOGY; VASCULAR ENDOTHELIUM;

ALGORITHMS; CORONARY VESSELS; DIABETES MELLITUS; ENDOTHELIUM, VASCULAR; HUMANS; MICROCIRCULATION; MICROVESSELS;

EID: 85038580381     PISSN: 03000605     EISSN: 14732300     Source Type: Journal    
DOI: 10.1177/0300060516675504     Document Type: Article

References (164)

1. Leon BM, Maddox TM. Diabetes and cardiovascular disease: Epidemiology, biological mechanisms, treatment recommendations and future research. World J Diabetes 2015; 6: 1246–1258.
2. Kibel A. Could angiotensin-(1–7) be connected with improvement of microvascular function in diabetic patients? Angiotensin-(1–7) iontophoresis may provide the answer. Med Hypotheses 2016; 93: 16–20. Epub ahead of print 12 May 2016. DOI: http://dx.doi.org/10.1016/j.mehy.2016.05.010.
3. Picchi A, Capobianco S, Qiu T, Coronary microvascular dysfunction in diabetes mellitus: a review. World J Cardiol 2010; 2: 377–390.
4. Tabit CE, Chung WB, Hamburg NM, Endothelial dysfunction in diabetes mellitus: molecular mechanisms and clinical implications. Rev Endocr Metab Disord 2010; 11: 61–74.
5. Tousoulis D, Papageorgiou N, Androulakis E, Diabetes mellitus-associated vascular impairment: novel circulating biomarkers and therapeutic approaches. J Am Coll Cardiol 2013; 62: 667–676.
6. Avogaro A, Albiero M, Menegazzo L, Endothelial dysfunction in diabetes: the role of reparatory mechanisms. Diabetes Care 2011; 34(Suppl 2): S285–S290.
7. Haffner SJ, Cassells H. Hyperglycemia as a cardiovascular risk factor. Am J Med 2003; 115(Suppl 8A): 6S–11S.
8. Haffner SM, Lehto S, Rönnemaa T, Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 1998; 339: 229–234.
9. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham study. JAMA 1979; 241: 2035–2038.
10. Gan D. Diabetes atlas. 2nd ed. Brussels: International Diabetes Federation, 2003
11. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414: 813–820.
12. Ceriello A. Coagulation activation in diabetes mellitus: the role of hyperglycaemia and therapeutic prospects. Diabetologia 1993; 3: 1119–1125.
13. Wild S, Roglic G, Green A, Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 2004; 27: 1047–1053.
14. Howard BV, Rodriguez BL, Bennett PH, Diabetes and cardiovascular disease. Circulation 2002; 105: 132–7.
15. Gonzalez MA, Selwyn AP. Endothelial function, inflammation, and prognosis in cardiovascular disease. Am J Med 2003; 115: 99–106.
16. Baumgartner-Parzer SM, Waldhäusl WK. The endothelium as a metabolic and endocrine organ: its relation with insulin resistance. Exp Clin Endocrinol Diabetes 2001; 109(Suppl 2): S166–S179.
17. Sena CM, Pereira AM, Seiça R. Endothelial dysfunction - a major mediator of diabetic vascular disease. Biochim Biophys Acta 2013; 1832: 2216–2231.
18. Schram MT, Stehouwer CD. Endothelial dysfunction, cellular adhesion molecules and the metabolic syndrome. Horm Metab Res 2005; 37(Suppl 1): 49–55.
19. Blankenberg S, Barbaux S, Tiret L. Adhesion molecules and atherosclerosis. Atherosclerosis 2003; 170: 191–203.
20. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med 1999; 340: 115–126.
21. Rask-Madsen C, King GL. Mechanisms of Disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007; 3: 46–56.
22. Matsumoto K, Sera Y, Ueki Y, Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabet Med 2002; 19: 822–826.
23. Price D, Loscalzo J. Cellular adhesion molecules and atherogenesis. Am J Med 1999; 107: 85–97.
24. Kado S, Nagata N. Circulating intercellular adhesion molecule-1, vascular cell adhesion molecule-1, and E-selectin in patients with type 2 diabetes mellitus. Diabetes Res Clin Pract 1999; 46: 143–148.
25. Cooke CL, Davidge ST. Peroxynitrite increases iNOS through NF-kappaB and decreases prostacyclin synthase in endothelial cells. Am J Physiol Cell Physiol 2002; 282: C395–C402.
26. Endemann DH, Schiffrin EL. Endothelial dysfunction. J Am Soc Nephrol 2004; 15: 1983–1992.
27. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 2000; 87: 840–844.
28. De Caterina R. Endothelial dysfunctions: common denominators in vascular disease. Curr Opin Clin Nutr Metab Care 2000; 3: 453–467.
29. Jafar N, Edriss H, Nugent K. The effect of short-term hyperglycemia on the innate immune system. Am J Med Sci 2016; 351: 201–211.
30. Ceriello A. Postprandial hyperglycemia and diabetes complications: is it time to treat? Diabetes 2005; 54: 1–7.
31. Shanik MH, Xu Y, Skrha J, Insulin resistance and hyperinsulinemia: is hyperinsulinemia the cart or the horse? Diabetes Care 2008; 31(Suppl 2): S262–S268.
32. Roberts AC, Porter KE. Cellular and molecular mechanisms of endothelial dysfunction in diabetes. Diab Vasc Dis Res 2013; 10: 472–482.
33. Hadden DR. The diabetes control and complications trial (DCCT): what every endocrinologist needs to know. Clin Endocrinol (Oxf) 1994; 40: 293–294.
34. Intensive blood glucose control with sulfonylureas or insulin compared with conventional treatment and risk for complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998; 352: 837–853.
35. Shichiri M, Kishikawa H, Ohkubo Y, Long-term results of the Kumamoto Study on optimal diabetes control in type 2 diabetic patients. Diabetes Care 2000; 23(Suppl 2): B21–B29.
36. Ferrannini E, DeFronzo RA. Impact of glucose-lowering drugs on cardiovascular disease in type 2 diabetes. Eur Heart J 2015; 36: 2288–2296.
37. Pries AR, Reglin B. Coronary microcirculatory pathophysiology: can we afford it to remain a black box? Eur Heart J 2016. pii: ehv760.
38. Deussen A, Ohanyan V, Jannasch A, Yet Mechanisms of metabolic coronary flow regulation. J Mol Cell Cardiol 2012; 52: 794–801.
39. Komaru T, Kanatsuka H, Shirato K. Coronary microcirculation: physiology and pharmacology. Pharmacol Ther 2000; 86: 217–261.
40. Spaan J, Kolyva C, van den Wijngaard J, Coronary structure and perfusion in health and disease. Philos Trans A Math Phys Eng Sci 2008; 366: 3137–3153.
41. Chilian WM. Coronary microcirculation in health and disease. Summary of an NHLBI workshop. Circulation 1997; 95: 522–528.
42. Pries AR, Badimon L, Bugiardini R, Coronary vascular regulation, remodelling, and collateralization: mechanisms and clinical implications on behalf of the working group on coronary pathophysiology and microcirculation. Eur Heart J 2015; 36: 3134–3146.
43. Yang J, Park Y, Zhang H, Feed-forward signaling of TNF-alpha and NF-kappaB via IKK-beta pathway contributes to insulin resistance and coronary arteriolar dysfunction in type 2 diabetic mice. Am J Physiol Heart Circ Physiol 2009; 296: H1850–H1858.
44. Woodman RJ, Watts GF, Playford DA, Oxidized LDL and small LDL particle size are independently predictive of a selective defect in microcirculatory endothelial function in type 2 diabetes. Diabetes Obes Metab 2005; 7: 612–617.
45. Koller A, Balasko M, Bagi Z. Endothelial regulation of coronary microcirculation in health and cardiometabolic diseases. Intern Emerg Med 2013; 8(Suppl 1): S51–S54.
46. Okon EB, Chung AW, Rauniyar P, Compromised arterial function in human type 2 diabetic patients. Diabetes 2005; 54: 2415–2423.
47. Miura H, Wachtel RE, Loberiza FR, Jr Diabetes mellitus impairs vasodilation to hypoxia in human coronary arterioles: reduced activity of ATP-sensitive potassium channels. Circ Res 2003; 92: 151–158.
48. Moien-Afshari F, Ghosh S, Elmi S, Exercise restores coronary vascular function independent of myogenic tone or hyperglycemic status in db/db mice. Am J Physiol Heart Circ Physiol 2008; 295: H1470–H1480.
49. Zhao G, Zhang X, Xu X, Depressed modulation of oxygen consumption by endogenous nitric oxide in cardiac muscle from diabetic dogs. Am J Physiol Heart Circ Physiol 2000; 279: H520–H527.
50. van den Heuvel M, Sorop O, Koopmans SJ, Coronary microvascular dysfunction in a porcine model of early atherosclerosis and diabetes. Am J Physiol Heart Circ Physiol 2012; 302: H85–H94.
51. Eid S, Abou-Kheir W, Sabra R, Involvement of renal cytochromes P450 and arachidonic acid metabolites in diabetic nephropathy. J Biol Regul Homeost Agents 2013; 27: 693–703.
52. Vanhoutte PM, Shimokawa H, Tang EH, Endothelial dysfunction and vascular disease. Acta Physiol (Oxf) 2009; 196: 193–222.
53. Gimeno AL, Sterin-Borda L, Borda ES, Arachidonate evokes constriction of coronary and mesenteric arteries isolated from diabetic dogs. Adv Prostaglandin Thromboxane Leukot Res 1983; 12: 235–240.
54. Bagi Z, Erdei N, Papp Z, Up-regulation of vascular cyclooxygenase-2 in diabetes mellitus. Pharmacol Rep 2006; 58(Suppl): 52–56.
55. Davel AP, Wenceslau CF, Akamine EH, Endothelial dysfunction in cardiovascular and endocrine-metabolic diseases: an update. Braz J Med Biol Res 2011; 44: 920–932.
56. Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002; 82: 131–185.
57. Li X, Zhao G, Ma B, 20-Hydroxyeicosatetraenoic acid impairs endothelial insulin signaling by inducing phosphorylation of the insulin receptor substrate-1 at Ser616. PLoS One 2014; 9: e95841–e95841.
58. Issan Y, Hochhauser E, Guo A, Elevated level of pro-inflammatory eicosanoids and EPC dysfunction in diabetic patients with cardiac ischemia. Prostaglandins Other Lipid Mediat 2013; 100–101: 15–21.
59. Pivackova L, Mensikova L, Gajdacova B, 6D.05: Endothelial dysfunction in animal models of glucose intolerance and diabetes is accompanied by different expression of key enzymes of epoxyeicosatrienoic acids pathway. J Hypertens 2015; 33(Suppl 1): e83–e84.
60. Kibel A, Novak S, Cosic A, Hyperbaric oxygenation modulates vascular reactivity to angiotensin-(1–7) in diabetic rats: potential role of epoxyeicosatrienoic acids. Diab Vasc Dis Res 2015; 12: 33–45.
61. Kibel A, Cavka A, Cosic A, Effects of hyperbaric oxygenation on vascular reactivity to angiotensin II and angiotensin-(1–7) in rats. Undersea Hyperb Med 2012; 39: 1053–1066.
62. Liu Y, Gutterman DD. The coronary circulation in diabetes: influence of reactive oxygen species on K+ channel-mediated vasodilation. Vascul Pharmacol 2002; 38: 43–49.
63. Gupte SA, Arshad M, Viola S, Pentose phosphate pathway coordinates multiple redox-controlled relaxing mechanisms in bovine coronary arteries. Am J Physiol Heart Circ Physiol 2003; 285: H2316–H2326.
64. Ammar RF, Jr Gutterman DD, Brooks LA, Free radicals mediate endothelial dysfunction of coronary arterioles in diabetes. Cardiovasc Res 2000; 47: 595–601.
65. Grainger J, Boachie-Ansah G. Anandamide-induced relaxation of sheep coronary arteries: the role of the vascular endothelium, arachidonic acid metabolites and potassium channels. Br J Pharmacol 2001; 134: 1003–1012.
66. Korovkina VP, England SK. Detection and implications of potassium channel alterations. Vascul Pharmacol 2002; 38: 3–12.
67. Hiett SC, Owen MK, Li W, Mechanisms underlying capsaicin effects in canine coronary artery: implications for coronary spasm. Cardiovasc Res 2014; 103: 607–618.
68. Bratz IN, Dick GM, Tune JD, Impaired capsaicin-induced relaxation of coronary arteries in a porcine model of the metabolic syndrome. Am J Physiol Heart Circ Physiol 2008; 294: H2489–H2496.
69. Guarini G, Ohanyan VA, Kmetz JG, Disruption of TRPV1-mediated coupling of coronary blood flow to cardiac metabolism in diabetic mice: role of nitric oxide and BK channels. Am J Physiol Heart Circ Physiol 2012; 303: H216–H223.
70. DelloStritto DJ, Connell PJ, Dick GM, Differential regulation of TRPV1 channels by H2O2: implications for diabetic microvascular dysfunction. Basic Res Cardiol 2016; 111: 21–21.
71. Hayat SA, Patel B, Khattar RS. Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci (London) 2004; 107: 539–557.
72. Picchi A, Capobianco S, Qiu T, Coronary microvascular dysfunction in diabetes mellitus: A review. World J Cardiol 2010; 2: 377–390.
73. Kannel WB, Hjortland M, Castelli WP. Role of diabetes in congestive heart failure: the Framingham study. Am J Cardiol 1974; 34: 29–34.
74. Boudina S, Abel ED. Basic science for clinicians. Diabetic cardiomyopathy revisited. Circ 2007; 115: 3213–3223.
75. Boudina S, Abel ED. Diabetic cardiomyopathy, causes and effects. Rev Endocr Metab Disord 2010; 11: 31–39.
76. Nacci C, Tarquinio M, Montagnani M. Molecular and clinical aspects of endothelial dysfunction in diabetes. Intern Emerg Med 2009; 4: 107–116.
77. Laakso M. Heart in diabetes: a microvascular disease. Diabetes Care 2011; 34(Suppl 2): S145–S149.
78. Sjögren A, Edvinsson L. Vasomotor changes in isolated coronary arteries from diabetic rats. Acta Physiol Scand 1988; 134: 429–436.
79. Factor SM, Okun EM, Minase T. Capillary microaneurysms in the human diabetic heart. N Engl J Med 1980; 302: 384–388.
80. Yoon YS, Uchida S, Masuo O, Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation 2005; 111: 2073–2085.
81. Miki T, Yuda S, Kouzu H, Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev 2013; 18: 149–166.
82. Frustaci A, Kajstura J, Chimenti C, Myocardial cell death in human diabetes. Circ Res 2000; 87: 1123–1132.
83. Joshi M, Kotha SR, Malireddy S, Conundrum of pathogenesis of diabetic cardiomyopathy: role of vascular endothelial dysfunction, reactive oxygen species, and mitochondria. Mol Cell Biochem 2014; 386: 233–249.
84. Dei Cas A, Khan SS, Butler J, Impact of diabetes on epidemiology, treatment, and outcomes of patients with heart failure. JACC Heart Fail 2015; 3: 136–145.
85. Kaski JC, Rosano GM, Collins P, Cardiac syndrome X: clinical characteristics and left ventricular function: long term follow-up study. J Am Coll Cardiol 1995; 25: 807–814.
86. Lamendola P, Lanza GA, Spinelli A, Long-term prognosis of patients with cardiac syndrome X. Int J Cardiol 2010; 140: 197–199.
87. Lanza GA, Crea F. Primary coronary microvascular dysfunction, clinical presentation, pathophysiology and management. Circulation 2010; 121: 2317–2325.
88. Yağmur J, Açuköz N, Cansel M, Assessment of the left ventricular systolic function in cardiac syndrome X using speckle tracking echocardiography. Anatol J Cardiol 2015; 16: 419–423. DOI: 10.5152/AnatolJCardiol.2015.6388.
89. Leung M, Juergens CP, Lo ST, Evaluation of coronary microvascular function by left ventricular contractile reserve with low-dose dobutamine echocardiography. EuroIntervention 2014; 9: 1202–1219.
90. Marini C, Bezante G, Gandolfo P, Optimization of flow reserve measurement using SPECT technology to evaluate the determinants of coronary microvascular dysfunction in diabetes. Eur J Nucl Med Mol Imaging 2010; 37: 357–367.
91. Panting JR, Gatehouse PD, Yang GZ, Abnormal subendocardial perfusion in cardiac syndrome X detected by cardiovascular magnetic resonance. N Eng J Med 2002; 346: 1948–1953.
92. Lanza GA, Buffon A, Sestito A, Relation between stress-induced myocardial perfusion defects on cardiovascular magnetic resonance and coronary microvascular dysfunction in patients with cardiac syndrome X. J Am Coll Cardiol 2008; 51: 466–472.
93. Bøttcher M, Botker HE, Sonne H, Endothelium-dependent and -independent perfusion reserve and the effect of L-arginine on myocardial perfusion in patients with syndrome X. Circulation 1999; 99: 1795–1801.
94. Ziadi MC, Dekemp RA, Williams KA, Impaired myocardial flow reserve on rubidium-82 positron emission tomography imaging predicts adverse outcomes in patients assessed for myocardial ischemia. J Am Coll Cardiol 2011; 58: 740–748.
95. Schelbert HR. Positron emission tomography measurements of myocardial blood flow: assessing coronary circulatory function and clinical implications. Heart 2012; 98: 592–600.
96. von Scholten BJ, Hasbak P, Christensen TE, Cardiac (82)Rb PET/CT for fast and non-invasive assessment of microvascular function and structure in asymptomatic patients with type 2 diabetes. Diabetologia 2016; 59: 371–378.
97. Slomka P, Berman DS, Alexanderson E, The role of PET quantification in cardiovascular imaging. Clin Transl Imaging 2014; 2: 343–358.
98. Buchthal SD, den Hollander JA, Merz CN, Abnormal myocardial phosphorus-31 nuclear magnetic resonance spectroscopy in women with chest pain but normal coronary angiograms. N Engl J Med 2000; 342: 829–835.
99. Bosnjak I, Selthofer-Relatic K, Glasnovic M. Antiphospholipid syndrome- predictor of coronary heart disease. Exp Clin Cardiol 2014; 20: 931–931.
100. Atmaca Y, Ozdemir AO, Ozdol C, Angiographic evaluation of myocardial perfusion in patients with syndrome X. Am J Cardiol 2005; 96: 803–805.
101. Rodés-Cabau J, Gutiérrez M, Courtis J, Importance of diffuse atherosclerosis in the functional evaluation of coronary stenosis in the proximal-mid segment of a coronary artery by myocardial fractional flow reserve measurements. Am J Cardiol 2011; 108: 483–490.
102. Atmaca Y, Duzen V, Ozdol C, Total blush score: a new index for the assessment of microvascular perfusion in idiopathic dilated cardiomyopathy. Coron Artery Dis 2008; 19: 181–185.
103. Gibson CM, Cannon CP, Daley WL, TIMI frame count: a quantitative method of assessing coronary artery flow. Circulation 1996; 93: 879–888.
104. Sucato V, Evola S, Novo G, Stable microvascular angina: instrumental evaluation of coronary microvascular dysfunction with coronary angiography and myocardial scintigraphy. Int J Cardiol 2014; 171: e127–e128.
105. Di Carli MF, Janisse J, Grunberger G, Role of chronic hyperglycemia in the pathogenesis of coronary microvascular dysfunction in diabetes. J Am Coll Cardiol 2003; 41: 1387–1393.
106. Di Carli MF, Bianco-Batlles D, Landa ME, Effects of autonomic neuropathy on coronary blood flow in patients with diabetes mellitus. Circulation 1999; 100: 813–819.
107. Pitkänen OP, Nuutila P, Raitakari OT, Coronary flow reserve is reduced in young men with IDDM. Diabetes 1998; 47: 248–254.
108. Yokoyama I, Momomura S, Ohtake T, Reduced myocardial flow reserve in non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 1997; 30: 1472–1477.
109. Nitenberg A, Valensi P, Sachs R, Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes 1993; 42: 1017–1025.
110. Aneja A, Tang WH, Bansilal S, Diabetic cardiomyopathy: insights into pathogenesis, diagnostic challenges, and therapeutic options. Am J Med 2008; 121: 748–757.
111. Van Hooven KH, Factor SM. A comparison of the pathological spectrum of hypertensive, diabetic, and hypertensive-diabetic heart disease. Circulation 1990; 82: 848–855.
112. Devereux RB, Roman MJ, Paranicas M, Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 2000; 101: 2271–2276.
113. Wende AR, Abel ED. Lipotoxicity in the heart. Biochim Biophys Acta 2010; 1801: 311–319.
114. McGavock JM, Lingvay I, Zib I, Cardiac steatosis in diabetes mellitus: a 1H-magnetic resonance spectroscopy study. Circulation 2007; 116: 1170–1175.
115. Nahser PJ, Jr Brown RE, Oskarsson H, Maximal coronary flow reserve and metabolic coronary vasodilation in patients with diabetes mellitus. Circulation 1995; 91: 635–640.
116. Seferović PM, Paulus WJ. Clinical diabetic cardiomyopathy: a two faced disease with restrictive and dilated phenotypes. Eur Heart J 2015; 36: 1718–1727. 1727a-1727c.
117. Zile MR, Baicu CF, Gaasch WH. Diastolic heart failure: abnormalities in active relaxation and passive stiffness of the left ventricle. N Engl J Med 2004; 350: 1953–1959.
118. Muranaka A, Yuda S, Tsuchihashi K, Quantitative assessment of left ventricular and left atrial functions by strain rate imaging in diabetic patients with and without hypertension. Echocardiography 2009; 26: 262–271.
119. Tarquini R, Lazzeri C, Pala L, The diabetic cardiomyopathy. Acta Diabetol 2011; 48: 173–181.
120. Schwanell CM, Schneppenheim M, Perings S, Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology 2002; 98: 33–39.
121. Poirer P, Bogathy P, Garneau C, Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes. Diabetes Care 2001; 24: 5–10.
122. Flores-Ramirez R, Azpiri-López JR, González-González JG, Global longitudinal strain as a biomarker in diabetic cardiomypopathy. A comparative study with Gal-3 in patients with preserved ejection fraction. Arch Cardiol Mex 2016. pii: S1405–9940(16)30046–5. doi: 10.1016/j.acmx.2016.06.002.
123. Murthy VL, Naya M, Foster CR, Association between coronary vascular dysfunction and cardiac mortality in patients with and without diabetes mellitus. Circulation 2012; 126: 1858–1868.
124. Cortigiani L, Rigo F, Gherardi S, Prognostic meaning of coronary microvascular disease in type 2 diabetes mellitus: a transthoracic Doppler echocardiographic study. J Am Soc Echocardiogr 2014; 27: 742–748.
125. Ishikawa K. Poor prognosis of patients with acute myocardial infarction complicated by diabetes mellitus; possible role of impaired microvascular function. Intern Med 2003; 42: 543–544.
126. Kurisu S, Inoue I, Kawagoe T, Diabetes mellitus is associated with insufficient microvascular reperfusion following revascularization for anterior acute myocardial infarction. Intern Med 2003; 42: 554–559.
127. Kawata T, Daimon M, Miyazaki S, Coronary microvascular function is independently associated with left ventricular filling pressure in patients with type 2 diabetes mellitus. Cardiovasc Diabetol 2015; 14: 98–98.
128. Aneja A, Tang WH, Bansilal S, Diabetic Cardiomyopathy: insights into pathogenesis, diagnostic challenges, and therapeutic options. Am J Med 2008; 121: 748–757.
129. Pauly DF, Johnson BD, Anderson RD, In women with symptoms of cardiac ischemia, nonobstructive coronary arteries, and microvascular dysfunction, angiotensin-converting enzyme inhibition is associated with improved microvascular function: A double-blind randomized study from the National Heart, Lung and Blood Institute Women’s Ischemia Syndrome Evaluation (WISE). Am Heart J 2011; 162: 678–684.
130. Kaski JC, Rosano G, Gavrielides S, Effects of angiotensin-converting enzyme inhibition on exercise-induced angina and ST segment depression in patients with microvascular angina. J Am Coll Cardiol 1994; 23: 652–657.
131. Motz W, Strauer BE. Improvement of coronary flow reserve after long-term therapy with enalapril. Hypertension 1996; 27: 1031–1308.
132. Bavry AA, Handberg EM, Huo T, Aldosterone inhibition and coronary endothelial function in women without obstructive coronary artery disease: an ancillary study of the national heart, lung, and blood institute-sponsored women’s ischemia syndrome evaluation. Am Heart J 2014; 167: 826–832.
133. Bender SB, Jia G, Sowers JR. Mineralocorticoid receptors: an appealing target to treat coronary microvascular dysfunction in diabetes. Diabetes 2015; 64: 3–5.
134. Garg R, Rao AD, Baimas-George M, Mineralocorticoid receptor blockade improves coronary microvascular function in individuals with type 2 diabetes. Diabetes 2015; 64: 236−242–236−242.
135. McIvor ME, Undemir C, Lawson J, Clinical effects and utility of intracoronary diltiazem. Cathet Cardiovasc Diagn 1995; 35: 287–291.
136. Cannon RO, 3rd Watson RM, Rosing DR, Efficacy of calcium channel blocker therapy for angina pectoris resulting from small-vessel coronary artery disease and abnormal vasodilator reserve. Am J Cardiol 1985; 56: 242–246.
137. Cannon RO, 3rd Brush JE, Jr Schenke WH, Beneficial and detrimental effects of lidoflazine in microvascular angina. Am J Cardiol 1990; 66: 37–41.
138. Sütsch G, Oechslin E, Mayer I, Effect of diltiazem on coronary flow reserve in patients with microvascular angina. Int J Cardiol 1995; 52: 135–143.
139. Zhang X, Li Q, Zhao J, Effects of combination of statin and calcium channel blocker in patients with cardiac syndrome X. Coron Artery Dis 2014; 25: 40–44.
140. Eshtehardi P, McDaniel MC, Dhawan SS, Effect of intensive atorvastatin therapy on coronary atherosclerosis progression, composition, arterial remodeling, and microvascular function. J Invasive Cardiol 2012; 24: 522–529.
141. Nemes A, Forster T, Gruber N, Coronary flow velocity reserve and indices describing aortic distensibility in patients after coronary angiography. Int J Cardiol 2004; 96: 29–33.
142. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 2008; 7: 156–167.
143. Denardo SJ, Wen X, Handberg EM, Effect of phosphodiesterase type 5 inhibition on microvascular coronary dysfunction in women: a women’s ischemia syndrome evaluation (WISE) ancillary study. Clin Cardiol 2011; 34: 483–487.
144. Egashira K, Hirooka Y, Kuga T, Effects of L-arginine supplementation on endothelium-dependent coronary vasodilation in patients with angina pectoris and normal coronary arteriograms. Circulation 1996; 94: 130–134.
145. Gellman J, Hare JM, Lowenstein CJ, L-arginine ameliorates the abnormal sympathetic response of the dysfunctional human coronary microvasculature. Angiology 2004; 55: 1–8.
146. Lerman A, Burnett JC, Jr Higano ST, Long-term L-arginine supplementation improves small-vessel coronary endothelial function in humans. Circulation 1998; 97: 2123–2128.
147. Bøtker HE, Sonne HS, Schmitz O, Effects of doxazosin on exercise-induced angina pectoris, ST-segment depression, and insulin sensitivity in patients with syndrome X. Am J Cardiol 1998; 82: 1352–1356.
148. Merz CN, Olson MB, McClure C, A randomized controlled trial of low-dose hormone therapy on myocardial ischemia in postmenopausal women with no obstructive coronary artery disease: results from the national institutes of health/national heart, lung, and blood institute-sponsored women’s ischemia syndrome evaluation (WISE). Am Heart J 2010; 159: 987.e1–e7–987.e1–e7.
149. Knuuti J, Kalliokoski R, Janatuinen T, Effect of estradiol-drospirenone hormone treatment on myocardial perfusion reserve in postmenopausal women with angina pectoris. Am J Cardiol 2007; 99: 1648–1652.
150. Jessurun GA, Hautvast RW, Tio RA, Electrical neuromodulation improves myocardial perfusion and ameliorates refractory angina pectoris in patients with syndrome X: fad or future? Eur J Pain 2003; 7: 507–512.
151. Luo C, Liu D, Wu G, Effect of enhanced external counterpulsation on coronary slow flow and its relation with endothelial function and inflammation: a mid-term follow-up study. Cardiology 2012; 122: 260–268.
152. Marinescu MA, Löffler AI, Ouellette M, Coronary microvascular dysfunction, microvascular angina, and treatment strategies. JACC Cardiovasc Imaging 2015; 8: 210–220.
153. Maurizio G. Beta-Blockers and Coronary Flow Reserve. Prof. Federico Piscione (Ed.) Angina pectoris. ISBN: 978–953-307–359-0, InTech. Available from: http://www.intechopen.com/books/anginapectoris/beta-blockers-and-coronary-flow-reserve
154. Fukomoto Y, Mohri M, Inokuchi K, Anti-ischemic effect of fasudil, specific Rho-kinase inhibitor, in patients with stabile effort angina. J Cardiovascular Pharmacol 2007; 49: 117–121.
155. Mehta PK, Goykhman P, Thomson LE, Ranolazine improves angina in women with evidence of myocardial ischemia but no obstructive coronary artery disease. JACC Cardiovasc Imaging 2011; 4: 514–522.
156. Villano A, Di Franco A, Nerla R, Effects of ivabradine and ranolazine in patients with microvascular angina pectoris. Am J Cardiol 2013; 112: 8–13.
157. Russo G, Di Franco A, Lamendola P, Lack of effect of nitrates on exercise stress test results in patients with microvascular angina. Cardiovasc Drugs Ther. 27: 229–234.
158. Bugiardini R, Borghi A, Pozzati A, The paradox of nitrates in patients with angina pectoris and angiographically normal coronary arteries. Am J Cardiol 1993; 72: 343–347. patients with microvascular angina. Cardiovasc Drugs Ther 2013; 27(3): 229–34.
159. Nerla R, Tarzia P, Sestito A, Effect of bariatric surgery on peripheral flow-mediated dilation and coronary microvascular function. Nutr Metab Cardiovasc Dis 2012; 22: 626–634.
160. Papadogeorgos NO, Bengtsson M, Kalani M. Selective endothelin A-receptor blockade attenuates coronary microvascular dysfunction after coronary stenting in patients with type 2 diabetes. Vasc Health Risk Manag 2009; 5: 893–899.
161. Jadhav S, Ferrell W, Greer IA, Effects of metformin on microvascular function and exercise tolerance in women with angina and normal coronary arteries: a randomized, double-blind, placebo-controlled study. J Am Coll Cardiol 2006; 48: 956–963.
162. Davis BJ, Xie Z, Viollet B, Activation of the AMP activated kinase by antidiabetes drug metformin stimulates nitric oxide synthesis in vivo by promoting the association of heat shock protein 90 and endothelial nitric oxide synthase. Diabetes 2006; 55: 496–505.
163. Valenzuela-Garcia LF, Matsuzawa Y, Sara JD, Lack of correlation between the optimal glycaemic control and coronary micro vascular dysfunction in patients with diabetes mellitus: a cross sectional study. Cardiovasc Diabetol 2015; 14: 106–106.
164. Castagno D, Baird-Gunning J, Jhund PS, Intensive glycemic control has no impact on the risk of heart failure in type 2 diabetic patients: evidence from a 37,229 patient meta-analysis. Am Heart J 2011; 162: 938–948, e2.