Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2018

Open Access 01-12-2018 | Review

Diabetes, cardiovascular disease and the microcirculation

Authors: W. David Strain, P. M. Paldánius

Published in: Cardiovascular Diabetology | Issue 1/2018

Login to get access

Abstract

Cardiovascular disease (CVD) is the leading cause of mortality in people with type 2 diabetes mellitus (T2DM), yet a significant proportion of the disease burden cannot be accounted for by conventional cardiovascular risk factors. Hypertension occurs in majority of people with T2DM, which is substantially more frequent than would be anticipated based on general population samples. The impact of hypertension is considerably higher in people with diabetes than it is in the general population, suggesting either an increased sensitivity to its effect or a confounding underlying aetiopathogenic mechanism of hypertension associated with CVD within diabetes. In this contribution, we aim to review the changes observed in the vascular tree in people with T2DM compared to the general population, the effects of established anti-diabetes drugs on microvascular outcomes, and explore the hypotheses to account for common causalities of the increased prevalence of CVD and hypertension in people with T2DM.
Literature
2.
go back to reference Struijker-Boudier AHJ. The burden of vascular disease in diabetes and hypertension: from micro- to macrovascular disease—the “bad loop”. Medicographia. 2009;31:251–6. Struijker-Boudier AHJ. The burden of vascular disease in diabetes and hypertension: from micro- to macrovascular disease—the “bad loop”. Medicographia. 2009;31:251–6.
3.
go back to reference Chantler PD, Frisbee JC. Arterial function in cardio-metabolic diseases: from the microcirculation to the large conduits. Prog Cardiovasc Dis. 2015;57:489–96.PubMedCrossRef Chantler PD, Frisbee JC. Arterial function in cardio-metabolic diseases: from the microcirculation to the large conduits. Prog Cardiovasc Dis. 2015;57:489–96.PubMedCrossRef
4.
go back to reference Niiranen TJ, Kalesan B, Hamburg NM, Benjamin EJ, Mitchell GF, Vasan RS. Relative contributions of arterial stiffness and hypertension to cardiovascular disease: the Framingham Heart Study. J Am Heart Assoc. 2016;5:e004271.PubMedPubMedCentralCrossRef Niiranen TJ, Kalesan B, Hamburg NM, Benjamin EJ, Mitchell GF, Vasan RS. Relative contributions of arterial stiffness and hypertension to cardiovascular disease: the Framingham Heart Study. J Am Heart Assoc. 2016;5:e004271.PubMedPubMedCentralCrossRef
5.
go back to reference Bastos JM, Bertoquini S, Polónia J. Prognostic significance of ambulatory arterial stiffness index in hypertensives followed for 8.2 years: its relation with new events and cardiovascular risk estimation. Rev Port Cardiol. 2010;29:1287–303.PubMed Bastos JM, Bertoquini S, Polónia J. Prognostic significance of ambulatory arterial stiffness index in hypertensives followed for 8.2 years: its relation with new events and cardiovascular risk estimation. Rev Port Cardiol. 2010;29:1287–303.PubMed
6.
go back to reference Cardoso CR, Ferreira MT, Leite NC, Salles GF. Prognostic impact of aortic stiffness in high-risk type 2 diabetic patients: the Rio deJaneiro type 2 diabetes cohort study. Diabetes Care. 2013;36:3772–8.PubMedPubMedCentralCrossRef Cardoso CR, Ferreira MT, Leite NC, Salles GF. Prognostic impact of aortic stiffness in high-risk type 2 diabetic patients: the Rio deJaneiro type 2 diabetes cohort study. Diabetes Care. 2013;36:3772–8.PubMedPubMedCentralCrossRef
7.
go back to reference Smulyan H, Lieber A, Safar ME. Hypertension, diabetes type II, and their association: role of arterial stiffness. Am J Hypertens. 2016;29:5–13.PubMedCrossRef Smulyan H, Lieber A, Safar ME. Hypertension, diabetes type II, and their association: role of arterial stiffness. Am J Hypertens. 2016;29:5–13.PubMedCrossRef
8.
go back to reference Natali A, Toschi E, Baldeweg S, Ciociaro D, Favilla S, Saccà L, et al. Clustering of insulin resistance with vascular dysfunction and low-grade inflammation in type 2 diabetes. Diabetes. 2006;55:1133–40.PubMedCrossRef Natali A, Toschi E, Baldeweg S, Ciociaro D, Favilla S, Saccà L, et al. Clustering of insulin resistance with vascular dysfunction and low-grade inflammation in type 2 diabetes. Diabetes. 2006;55:1133–40.PubMedCrossRef
9.
go back to reference Strain WD, Chaturvedi N, Dockery F, Shiff R, Shore AC, Bulpitt CJ, et al. Increased arterial stiffness in Europeans and African Caribbeans with type 2 diabetes cannot be accounted for by conventional cardiovascular risk factors. Am J Hypertens. 2006;19:889–96.PubMedCrossRef Strain WD, Chaturvedi N, Dockery F, Shiff R, Shore AC, Bulpitt CJ, et al. Increased arterial stiffness in Europeans and African Caribbeans with type 2 diabetes cannot be accounted for by conventional cardiovascular risk factors. Am J Hypertens. 2006;19:889–96.PubMedCrossRef
10.
go back to reference Park CM, Tillin T, March K, Jones S, Whincup PH, Mayet J, et al. Adverse effect of diabetes and hyperglycaemia on arterial stiffness in Europeans, South Asians, and African Caribbeans in the SABRE study. J Hypertens. 2016;34:282–9.PubMedPubMedCentralCrossRef Park CM, Tillin T, March K, Jones S, Whincup PH, Mayet J, et al. Adverse effect of diabetes and hyperglycaemia on arterial stiffness in Europeans, South Asians, and African Caribbeans in the SABRE study. J Hypertens. 2016;34:282–9.PubMedPubMedCentralCrossRef
11.
go back to reference Madonna R, Balistreri CR, Geng YJ, De Caterina R. Diabetic microangiopathy: pathogenetic insights and novel therapeutic approaches. Vasc Pharmacol. 2017;90:1–7.CrossRef Madonna R, Balistreri CR, Geng YJ, De Caterina R. Diabetic microangiopathy: pathogenetic insights and novel therapeutic approaches. Vasc Pharmacol. 2017;90:1–7.CrossRef
12.
go back to reference Stehouwer CD, Ferreira I. Diabetes, lipids and other cardiovascular risk factors. In: Safar M, O’Rourke M, editors. Handbook of hypertension. Arterial stiffness hypertension, vol. 23. Edinburgh: Elsevier; 2006. p. 427–56. Stehouwer CD, Ferreira I. Diabetes, lipids and other cardiovascular risk factors. In: Safar M, O’Rourke M, editors. Handbook of hypertension. Arterial stiffness hypertension, vol. 23. Edinburgh: Elsevier; 2006. p. 427–56.
13.
go back to reference Urbina EM, Khoury PR, McCoy C, Daniels SR, Kimball TR, Dolan LM. Cardiac and vascular consequences of pre-hypertension in youth. J Clin Hypertens. 2011;13:332–42.CrossRef Urbina EM, Khoury PR, McCoy C, Daniels SR, Kimball TR, Dolan LM. Cardiac and vascular consequences of pre-hypertension in youth. J Clin Hypertens. 2011;13:332–42.CrossRef
14.
go back to reference Tropeano AI, Boutouyrie P, Katsahian S, Laloux B, Laurent S. Glucose level is a major determinant of carotid intima-media thickness in patients with hypertension and hyperglycemia. J Hypertens. 2004;22:2153–60.PubMedCrossRef Tropeano AI, Boutouyrie P, Katsahian S, Laloux B, Laurent S. Glucose level is a major determinant of carotid intima-media thickness in patients with hypertension and hyperglycemia. J Hypertens. 2004;22:2153–60.PubMedCrossRef
15.
go back to reference Rubin J, Nambi V, Chambless LE, Steffes MW, Juraschek SP, Coresh J, et al. Hyperglycemia and arterial stiffness: the atherosclerosis risk in the communities study. Atherosclerosis. 2012;225:246–51.PubMedPubMedCentralCrossRef Rubin J, Nambi V, Chambless LE, Steffes MW, Juraschek SP, Coresh J, et al. Hyperglycemia and arterial stiffness: the atherosclerosis risk in the communities study. Atherosclerosis. 2012;225:246–51.PubMedPubMedCentralCrossRef
16.
go back to reference Stirban A, Gawlowski T, Roden M. Vascular effects of advanced glycation endproducts: clinical effects and molecular mechanisms. Mol Metab. 2013;3:94–108.PubMedPubMedCentralCrossRef Stirban A, Gawlowski T, Roden M. Vascular effects of advanced glycation endproducts: clinical effects and molecular mechanisms. Mol Metab. 2013;3:94–108.PubMedPubMedCentralCrossRef
17.
go back to reference Brohall G, Odén A, Fagerberg B. Carotid artery intima-media thickness in patients with type 2 diabetes mellitus and impaired glucose tolerance: a systematic review. Diabet Med. 2006;23:609–16.PubMedCrossRef Brohall G, Odén A, Fagerberg B. Carotid artery intima-media thickness in patients with type 2 diabetes mellitus and impaired glucose tolerance: a systematic review. Diabet Med. 2006;23:609–16.PubMedCrossRef
18.
go back to reference Madonna R, Caterina RD. Cellular and molecular mechanisms of vascular injury in diabetes–part I: pathways of vascular disease in diabetes. Vasc Pharmacol. 2011;54:68–74.CrossRef Madonna R, Caterina RD. Cellular and molecular mechanisms of vascular injury in diabetes–part I: pathways of vascular disease in diabetes. Vasc Pharmacol. 2011;54:68–74.CrossRef
19.
go back to reference Madonna R, Caterina RD. Cellular and molecular mechanisms of vascular injury in diabetes–part II: cellular mechanisms and therapeutic targets. Vasc Pharmacol. 2011;54:75–9.CrossRef Madonna R, Caterina RD. Cellular and molecular mechanisms of vascular injury in diabetes–part II: cellular mechanisms and therapeutic targets. Vasc Pharmacol. 2011;54:75–9.CrossRef
20.
go back to reference Park SW, Jun HO, Kwon E, Yun JW, Kim JH, Park YJ, et al. Antiangiogenic effect of betaine on pathologic retinal neovascularization via suppression of reactive oxygen species mediated vascular endothelial growth factor signalling. Vasc Pharmacol. 2017;90:19–26.CrossRef Park SW, Jun HO, Kwon E, Yun JW, Kim JH, Park YJ, et al. Antiangiogenic effect of betaine on pathologic retinal neovascularization via suppression of reactive oxygen species mediated vascular endothelial growth factor signalling. Vasc Pharmacol. 2017;90:19–26.CrossRef
21.
go back to reference Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.PubMedCrossRef Monnier L, Mas E, Ginet C, Michel F, Villon L, Cristol JP, et al. Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA. 2006;295:1681–7.PubMedCrossRef
22.
go back to reference Zinman B, Marso SP, Poulter NR, Emerson SS, Pieber TR, Pratley RE, et al. Day-to-day fasting glycaemic variability in DEVOTE: associations with severe hypoglycaemia and cardiovascular outcomes (DEVOTE 2). Diabetologia. 2018;61:48–57.PubMedCrossRef Zinman B, Marso SP, Poulter NR, Emerson SS, Pieber TR, Pratley RE, et al. Day-to-day fasting glycaemic variability in DEVOTE: associations with severe hypoglycaemia and cardiovascular outcomes (DEVOTE 2). Diabetologia. 2018;61:48–57.PubMedCrossRef
23.
go back to reference Su G, Mi SH, Tao H, Li Z, Yang HX, Zheng H, et al. Impact of admission glycemic variability, glucose, and glycosylated hemoglobin on major adverse cardiac events after acute myocardial infarction. Diabetes Care. 2013;36:1026–32.PubMedPubMedCentralCrossRef Su G, Mi SH, Tao H, Li Z, Yang HX, Zheng H, et al. Impact of admission glycemic variability, glucose, and glycosylated hemoglobin on major adverse cardiac events after acute myocardial infarction. Diabetes Care. 2013;36:1026–32.PubMedPubMedCentralCrossRef
24.
go back to reference Rizzo MR, Barbieri M, Marfella R, Paolisso G. Reduction of oxidative stress and inflammation by blunting daily acute glucose fluctuations in patients with type 2 diabetes: role of dipeptidyl peptidase-IV inhibition. Diabetes Care. 2012;35:2076–82.PubMedPubMedCentralCrossRef Rizzo MR, Barbieri M, Marfella R, Paolisso G. Reduction of oxidative stress and inflammation by blunting daily acute glucose fluctuations in patients with type 2 diabetes: role of dipeptidyl peptidase-IV inhibition. Diabetes Care. 2012;35:2076–82.PubMedPubMedCentralCrossRef
25.
go back to reference Barbieri M, Rizzo MR, Marfella R, Boccardi V, Esposito A, Pansini A, et al. Decreased carotid atherosclerotic process by control of daily acute glucose fluctuations in diabetic patients treated by DPP-IV inhibitors. Atherosclerosis. 2013;227:349–54.PubMedCrossRef Barbieri M, Rizzo MR, Marfella R, Boccardi V, Esposito A, Pansini A, et al. Decreased carotid atherosclerotic process by control of daily acute glucose fluctuations in diabetic patients treated by DPP-IV inhibitors. Atherosclerosis. 2013;227:349–54.PubMedCrossRef
26.
go back to reference Frisbee JC, Butcher JT, Frisbee SJ, Olfert IM, Chantler PD, Tabone LE, et al. Increased peripheral vascular disease risk progressively constrains perfusion adaptability in the skeletal muscle microcirculation. Am J Physiol Heart Circ Physiol. 2016;310(4):H488–504.PubMedCrossRef Frisbee JC, Butcher JT, Frisbee SJ, Olfert IM, Chantler PD, Tabone LE, et al. Increased peripheral vascular disease risk progressively constrains perfusion adaptability in the skeletal muscle microcirculation. Am J Physiol Heart Circ Physiol. 2016;310(4):H488–504.PubMedCrossRef
27.
go back to reference de Boer RA, Doehner W, van der Horst IC, Anker SD, Babalis D, Roughton M, et al. Influence of diabetes mellitus and hyperglycemia on prognosis in patients > or = 70 years old with heart failure and effects of nebivolol (data from the Study of Effects of Nebivolol Intervention on Outcomes and Rehospitalization in Seniors with heart failure [SENIORS]). Am J Cardiol. 2010;106:78–86.PubMedCrossRef de Boer RA, Doehner W, van der Horst IC, Anker SD, Babalis D, Roughton M, et al. Influence of diabetes mellitus and hyperglycemia on prognosis in patients > or = 70 years old with heart failure and effects of nebivolol (data from the Study of Effects of Nebivolol Intervention on Outcomes and Rehospitalization in Seniors with heart failure [SENIORS]). Am J Cardiol. 2010;106:78–86.PubMedCrossRef
28.
go back to reference Sarma S, Mentz RJ, Kwasny MJ, Fought AJ, Huffman M, Subacius H, et al. Association between diabetes mellitus and post-discharge outcomes in patients hospitalized with heart failure: findings from the EVEREST trial. Eur J Heart Fail. 2013;15:194–202.PubMedCrossRef Sarma S, Mentz RJ, Kwasny MJ, Fought AJ, Huffman M, Subacius H, et al. Association between diabetes mellitus and post-discharge outcomes in patients hospitalized with heart failure: findings from the EVEREST trial. Eur J Heart Fail. 2013;15:194–202.PubMedCrossRef
29.
go back to reference Bertoni AG, Hundley WG, Massing MW, Bonds DE, Burke GL, Goff DC Jr. Heart failure prevalence, incidence, and mortality in the elderly with diabetes. Diabetes Care. 2004;27:699–703.PubMedCrossRef Bertoni AG, Hundley WG, Massing MW, Bonds DE, Burke GL, Goff DC Jr. Heart failure prevalence, incidence, and mortality in the elderly with diabetes. Diabetes Care. 2004;27:699–703.PubMedCrossRef
30.
go back to reference Cavallo Perin P, Pacini G, Giunti S, Comune M, Conte MR, Cassader M, et al. Microvascular angina (cardiological syndrome X) per se is not associated with hyperinsulinemia or insulin resistance. Eur J Clin Invest. 2000;30:481–6.PubMedCrossRef Cavallo Perin P, Pacini G, Giunti S, Comune M, Conte MR, Cassader M, et al. Microvascular angina (cardiological syndrome X) per se is not associated with hyperinsulinemia or insulin resistance. Eur J Clin Invest. 2000;30:481–6.PubMedCrossRef
31.
go back to reference Ong P, Camici PG, Beltrame JF, Crea F, Shimokawa H, Sechtem U, et al. International standardization of diagnostic criteria for microvascular angina. Int J Cardiol. 2018;250:16–20.PubMedCrossRef Ong P, Camici PG, Beltrame JF, Crea F, Shimokawa H, Sechtem U, et al. International standardization of diagnostic criteria for microvascular angina. Int J Cardiol. 2018;250:16–20.PubMedCrossRef
32.
go back to reference Valenzuela-Garcia LF, Matsuzawa Y, Sara JD, Kwon TG, Lennon RJ, Lerman LO, et al. 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.PubMedPubMedCentralCrossRef Valenzuela-Garcia LF, Matsuzawa Y, Sara JD, Kwon TG, Lennon RJ, Lerman LO, et al. 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.PubMedPubMedCentralCrossRef
33.
go back to reference Smits MM, Tonneijck L, Muskiet MH, Hoekstra T, Kramer MH, Diamant M, et al. GLP-1-based therapies have no microvascular effects in type 2 diabetes mellitus: an acute and 12-week randomized, double-blind placebo-controlled trial. Arterioscler Thromb Vasc Biol. 2016;36:2125–32.PubMedCrossRef Smits MM, Tonneijck L, Muskiet MH, Hoekstra T, Kramer MH, Diamant M, et al. GLP-1-based therapies have no microvascular effects in type 2 diabetes mellitus: an acute and 12-week randomized, double-blind placebo-controlled trial. Arterioscler Thromb Vasc Biol. 2016;36:2125–32.PubMedCrossRef
34.
go back to reference Rizzoni D, Agabiti Rosei E. Small artery remodeling in hypertension and diabetes. Curr Hypertens Rep. 2006;8:90–5.PubMedCrossRef Rizzoni D, Agabiti Rosei E. Small artery remodeling in hypertension and diabetes. Curr Hypertens Rep. 2006;8:90–5.PubMedCrossRef
35.
go back to reference Laurent S, Boutouyrie P. The structural factor of hypertension: large and small artery alterations. Circ Res. 2015;116:1007–21.PubMedCrossRef Laurent S, Boutouyrie P. The structural factor of hypertension: large and small artery alterations. Circ Res. 2015;116:1007–21.PubMedCrossRef
36.
go back to reference Gliemann L, Buess R, Nyberg M, Hoppeler H, Odriozola A, Thaning P, et al. Capillary growth, ultrastructure remodelling and exercise training in skeletal muscle of essential hypertensive patients. Acta Physiol. 2015;214:210–20.CrossRef Gliemann L, Buess R, Nyberg M, Hoppeler H, Odriozola A, Thaning P, et al. Capillary growth, ultrastructure remodelling and exercise training in skeletal muscle of essential hypertensive patients. Acta Physiol. 2015;214:210–20.CrossRef
37.
go back to reference Rizzoni D, Porteri E, Guelfi D, Muiesan ML, Valentini U, Cimino A, et al. Structural alterations in subcutaneous small arteries of normotensive and hypertensive patients with non-insulin-dependent diabetes mellitus. Circulation. 2001;103:1238–44.PubMedCrossRef Rizzoni D, Porteri E, Guelfi D, Muiesan ML, Valentini U, Cimino A, et al. Structural alterations in subcutaneous small arteries of normotensive and hypertensive patients with non-insulin-dependent diabetes mellitus. Circulation. 2001;103:1238–44.PubMedCrossRef
38.
go back to reference Schofield I, Malik R, Izzard A, Austin C, Heagerty A. Vascular structural and functional changes in type 2 diabetes mellitus: evidence for the roles of abnormal myogenic responsiveness and dyslipidemia. Circulation. 2002;106:3037–43.PubMedCrossRef Schofield I, Malik R, Izzard A, Austin C, Heagerty A. Vascular structural and functional changes in type 2 diabetes mellitus: evidence for the roles of abnormal myogenic responsiveness and dyslipidemia. Circulation. 2002;106:3037–43.PubMedCrossRef
39.
go back to reference Scalia R, Gong Y. Berzins Bc. Hyperglycemia is a major determinant of albumin permeability in diabetic microcirculation: the role of mu-calpain. Diabetes. 2007;56:1842–9.PubMedCrossRef Scalia R, Gong Y. Berzins Bc. Hyperglycemia is a major determinant of albumin permeability in diabetic microcirculation: the role of mu-calpain. Diabetes. 2007;56:1842–9.PubMedCrossRef
40.
go back to reference Akerstrom T, Laub L, Vedel K, Brand CL, Pedersen BK, Lindqvist AK, et al. Increased skeletal muscle capillarization enhances insulin sensitivity. Am J Physiol Endocrinol Metab. 2014;307:E1105–16.PubMedCrossRef Akerstrom T, Laub L, Vedel K, Brand CL, Pedersen BK, Lindqvist AK, et al. Increased skeletal muscle capillarization enhances insulin sensitivity. Am J Physiol Endocrinol Metab. 2014;307:E1105–16.PubMedCrossRef
41.
go back to reference Strain WD, Chaturvedi N, Hughes A, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, et al. Associations between cardiac target organ damage and microvascular dysfunction: the role of blood pressure. J Hypertens. 2010;28:952–8.PubMedCrossRef Strain WD, Chaturvedi N, Hughes A, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, et al. Associations between cardiac target organ damage and microvascular dysfunction: the role of blood pressure. J Hypertens. 2010;28:952–8.PubMedCrossRef
42.
go back to reference Strain WD, Chaturvedi N, Bulpitt CJ, Rajkumar C, Shore AC. Albumin excretion rate and cardiovascular risk: could the association be explained by early microvascular dysfunction? Diabetes. 2005;54:1816–22.PubMedCrossRef Strain WD, Chaturvedi N, Bulpitt CJ, Rajkumar C, Shore AC. Albumin excretion rate and cardiovascular risk: could the association be explained by early microvascular dysfunction? Diabetes. 2005;54:1816–22.PubMedCrossRef
43.
go back to reference Jumar A, Ott C, Kistner I, Friedrich S, Michelson G, Harazny JM, et al. Early signs of end-organ damage in retinal arterioles in patients with type 2 diabetes compared to hypertensive patients. Microcirculation. 2016;23:447–55.PubMedCrossRef Jumar A, Ott C, Kistner I, Friedrich S, Michelson G, Harazny JM, et al. Early signs of end-organ damage in retinal arterioles in patients with type 2 diabetes compared to hypertensive patients. Microcirculation. 2016;23:447–55.PubMedCrossRef
44.
go back to reference Levy BI, Schiffrin EL, Mourad JJ, Agostini D, Vicaut E, Safar ME, et al. Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation. 2008;118:968–76.PubMedCrossRef Levy BI, Schiffrin EL, Mourad JJ, Agostini D, Vicaut E, Safar ME, et al. Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation. 2008;118:968–76.PubMedCrossRef
45.
go back to reference Buus NH, Bottcher M, Jorgensen CG, Christensen KL, Thygesen K, Nielsen TT, et al. Myocardial perfusion during long-term angiotensin-converting enzyme inhibition or β-blockade in patients with essential hypertension. Hypertension. 2004;44:465–70.PubMedCrossRef Buus NH, Bottcher M, Jorgensen CG, Christensen KL, Thygesen K, Nielsen TT, et al. Myocardial perfusion during long-term angiotensin-converting enzyme inhibition or β-blockade in patients with essential hypertension. Hypertension. 2004;44:465–70.PubMedCrossRef
46.
go back to reference von Scholten BJ, Rosendahl A, Hasbak P, Bergholdt R, Kjaer A, Rossing P, et al. Impaired coronary microcirculation in type 2 diabetic patients is associated with elevated circulating regulatory T cells and reduced number of IL-21R + T cells. Cardiovasc Diabetol. 2016;15:67.CrossRef von Scholten BJ, Rosendahl A, Hasbak P, Bergholdt R, Kjaer A, Rossing P, et al. Impaired coronary microcirculation in type 2 diabetic patients is associated with elevated circulating regulatory T cells and reduced number of IL-21R + T cells. Cardiovasc Diabetol. 2016;15:67.CrossRef
47.
go back to reference Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, et al. Attenuated systemic microvascular function in men with coronary artery disease is associated with angina but not explained by atherosclerosis. Microcirculation. 2013;20:670–7.PubMedCrossRef Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, et al. Attenuated systemic microvascular function in men with coronary artery disease is associated with angina but not explained by atherosclerosis. Microcirculation. 2013;20:670–7.PubMedCrossRef
48.
go back to reference Yip W, Sabanayagam C, Ong PG, Patel UD, Chow KY, Tai ES, Ling LH, Wong TY, Cheung CY. Joint effect of early microvascular damage in the eye & kidney on risk of cardiovascular events. Sci Rep. 2016;6:27442.PubMedPubMedCentralCrossRef Yip W, Sabanayagam C, Ong PG, Patel UD, Chow KY, Tai ES, Ling LH, Wong TY, Cheung CY. Joint effect of early microvascular damage in the eye & kidney on risk of cardiovascular events. Sci Rep. 2016;6:27442.PubMedPubMedCentralCrossRef
49.
go back to reference Mathur R, Bhaskaran K, Edwards E, Lee H, Chaturvedi N, Smeeth L, et al. Population trends in the 10-year incidence and prevalence of diabetic retinopathy in the UK: a cohort study in the Clinical Practice Research Datalink 2004–2014. BMJ Open. 2017;7:e014444.PubMedPubMedCentralCrossRef Mathur R, Bhaskaran K, Edwards E, Lee H, Chaturvedi N, Smeeth L, et al. Population trends in the 10-year incidence and prevalence of diabetic retinopathy in the UK: a cohort study in the Clinical Practice Research Datalink 2004–2014. BMJ Open. 2017;7:e014444.PubMedPubMedCentralCrossRef
50.
go back to reference Guo VY, Cao B, Wu X, Lee JJ, Zee BC. Prospective association between diabetic retinopathy and cardiovascular disease—a systematic review and meta-analysis of cohort studies. J Stroke Cerebrovasc Dis. 2016;25:1688–95.PubMedCrossRef Guo VY, Cao B, Wu X, Lee JJ, Zee BC. Prospective association between diabetic retinopathy and cardiovascular disease—a systematic review and meta-analysis of cohort studies. J Stroke Cerebrovasc Dis. 2016;25:1688–95.PubMedCrossRef
51.
go back to reference Wong TY, Klein R, Sharrett AR, Schmidt MI, Pankow JS, Couper DJ, et al. Retinal arteriolar narrowing and risk of diabetes mellitus in middle-aged persons. JAMA. 2002;287:2528–33.PubMedCrossRef Wong TY, Klein R, Sharrett AR, Schmidt MI, Pankow JS, Couper DJ, et al. Retinal arteriolar narrowing and risk of diabetes mellitus in middle-aged persons. JAMA. 2002;287:2528–33.PubMedCrossRef
52.
go back to reference Wong TY, Rosamond W, Chang PP, Couper DJ, Sharrett AR, Hubbard LD, et al. Retinopathy and risk of congestive heart failure. JAMA. 2005;293:63–9.PubMedCrossRef Wong TY, Rosamond W, Chang PP, Couper DJ, Sharrett AR, Hubbard LD, et al. Retinopathy and risk of congestive heart failure. JAMA. 2005;293:63–9.PubMedCrossRef
53.
go back to reference Hafner J, Ginner L, Karst S, Leitgeb R, Unterluggauer M, Sacu S, et al. Regional patterns of retinal oxygen saturation and microvascular hemodynamic parameters preceding retinopathy in patients with type II diabetes. Invest Ophthalmol Vis Sci. 2017;58:5541–7.PubMedCrossRef Hafner J, Ginner L, Karst S, Leitgeb R, Unterluggauer M, Sacu S, et al. Regional patterns of retinal oxygen saturation and microvascular hemodynamic parameters preceding retinopathy in patients with type II diabetes. Invest Ophthalmol Vis Sci. 2017;58:5541–7.PubMedCrossRef
54.
go back to reference Liew G, Wong TY, Mitchell P, Cheung N, Wang JJ. Retinopathy predicts coronary heart disease mortality. Heart. 2009;95:391–4.PubMedCrossRef Liew G, Wong TY, Mitchell P, Cheung N, Wang JJ. Retinopathy predicts coronary heart disease mortality. Heart. 2009;95:391–4.PubMedCrossRef
55.
go back to reference Forst T, Michelson G, Ratter F, Weber MM, Anders S, Mitry M, et al. Addition of liraglutide in patients with Type 2 diabetes well controlled on metformin monotherapy improves several markers of vascular function. Diabet Med. 2012;29:1115–8.PubMedCrossRef Forst T, Michelson G, Ratter F, Weber MM, Anders S, Mitry M, et al. Addition of liraglutide in patients with Type 2 diabetes well controlled on metformin monotherapy improves several markers of vascular function. Diabet Med. 2012;29:1115–8.PubMedCrossRef
56.
go back to reference Ott C, Raff U, Schmidt S, Kistner I, Friedrich S, Bramlage P, et al. Effects of saxagliptin on early microvascular changes in patients with type 2 diabetes. Cardiovasc Diabetol. 2014;13:19.PubMedPubMedCentralCrossRef Ott C, Raff U, Schmidt S, Kistner I, Friedrich S, Bramlage P, et al. Effects of saxagliptin on early microvascular changes in patients with type 2 diabetes. Cardiovasc Diabetol. 2014;13:19.PubMedPubMedCentralCrossRef
57.
go back to reference Berndt-Zipfel C, Michelson G, Dworak M, Mitry M, Löffler A, Pfützner A, et al. Vildagliptin in addition to metformin improves retinal blood flow and erythrocyte deformability in patients with type 2 diabetes mellitus—results from an exploratory study. Cardiovasc Diabetol. 2013;12:59.PubMedPubMedCentralCrossRef Berndt-Zipfel C, Michelson G, Dworak M, Mitry M, Löffler A, Pfützner A, et al. Vildagliptin in addition to metformin improves retinal blood flow and erythrocyte deformability in patients with type 2 diabetes mellitus—results from an exploratory study. Cardiovasc Diabetol. 2013;12:59.PubMedPubMedCentralCrossRef
58.
go back to reference Faber R, Zander M, Pena A, Michelsen MM, Mygind ND, Prescott E. Effect of the glucagon-like peptide-1 analogue liraglutide on coronary microvascular function in patients with type 2 diabetes—a randomized, single-blinded, cross-over pilot study. Cardiovasc Diabetol. 2015;14:41.PubMedPubMedCentralCrossRef Faber R, Zander M, Pena A, Michelsen MM, Mygind ND, Prescott E. Effect of the glucagon-like peptide-1 analogue liraglutide on coronary microvascular function in patients with type 2 diabetes—a randomized, single-blinded, cross-over pilot study. Cardiovasc Diabetol. 2015;14:41.PubMedPubMedCentralCrossRef
59.
go back to reference Jax T, Stirban A, Terjung A, Esmaeili H, Berk A, Thiemann S, et al. A randomised, active- and placebo-controlled, three-period crossover trial to investigate short-term effects of the dipeptidyl peptidase-4 inhibitor linagliptin on macro- and microvascular endothelial function in type 2 diabetes. Cardiovasc Diabetol. 2017;16:13.PubMedPubMedCentralCrossRef Jax T, Stirban A, Terjung A, Esmaeili H, Berk A, Thiemann S, et al. A randomised, active- and placebo-controlled, three-period crossover trial to investigate short-term effects of the dipeptidyl peptidase-4 inhibitor linagliptin on macro- and microvascular endothelial function in type 2 diabetes. Cardiovasc Diabetol. 2017;16:13.PubMedPubMedCentralCrossRef
60.
go back to reference Marso SP, Daniels GH, Brown-Frandsen K, Kristensen P, Mann JF, Nauck MA, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375:311–22.PubMedPubMedCentralCrossRef Marso SP, Daniels GH, Brown-Frandsen K, Kristensen P, Mann JF, Nauck MA, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375:311–22.PubMedPubMedCentralCrossRef
61.
go back to reference Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. New Engl J Med. 2007;356:2457–71.PubMedCrossRef Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. New Engl J Med. 2007;356:2457–71.PubMedCrossRef
64.
go back to reference Marso SP, Bain SC, Consoli A, Eliaschewitz FG, Jodar E, Leiter LA, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med. 2016;375:1834–44.PubMedCrossRef Marso SP, Bain SC, Consoli A, Eliaschewitz FG, Jodar E, Leiter LA, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med. 2016;375:1834–44.PubMedCrossRef
65.
go back to reference Pfeffer MA, Claggett B, Diaz R, Dickstein K, Gerstein HC, Køber LV, et al. Lixisenatide in patients with type 2 diabetes and acute coronary syndrome. N Engl J Med. 2015;373:2247–57.PubMedCrossRef Pfeffer MA, Claggett B, Diaz R, Dickstein K, Gerstein HC, Køber LV, et al. Lixisenatide in patients with type 2 diabetes and acute coronary syndrome. N Engl J Med. 2015;373:2247–57.PubMedCrossRef
66.
go back to reference Holman RR, Bethel MA, Mentz RJ, Thompson VP, Lokhnygina Y, Buse JB, et al. Effects of once-weekly exenatide on cardiovascular outcomes in Type 2 diabetes. N Engl J Med. 2017;377:1228–39.PubMedCrossRef Holman RR, Bethel MA, Mentz RJ, Thompson VP, Lokhnygina Y, Buse JB, et al. Effects of once-weekly exenatide on cardiovascular outcomes in Type 2 diabetes. N Engl J Med. 2017;377:1228–39.PubMedCrossRef
67.
go back to reference Ban K, Kim KH, Cho CK, Sauvé M, Diamandis EP, Backx PH, et al. Glucagon-like peptide (GLP)-1(9-36)amide-mediated cytoprotection is blocked by Exendin (9-39) yet does not require the known GLP-1 receptor. Endocrinology. 2010;151:1520–31.PubMedCrossRef Ban K, Kim KH, Cho CK, Sauvé M, Diamandis EP, Backx PH, et al. Glucagon-like peptide (GLP)-1(9-36)amide-mediated cytoprotection is blocked by Exendin (9-39) yet does not require the known GLP-1 receptor. Endocrinology. 2010;151:1520–31.PubMedCrossRef
68.
go back to reference Zinman B, Wanner C, Lachin JM, Fitchett D, Bluhmki E, Hantel S, et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373:2117–28.PubMedCrossRef Zinman B, Wanner C, Lachin JM, Fitchett D, Bluhmki E, Hantel S, et al. Empagliflozin, cardiovascular outcomes, and mortality in type 2 diabetes. N Engl J Med. 2015;373:2117–28.PubMedCrossRef
69.
go back to reference Wanner C, Inzucchi SE, Lachin JM, Fitchett D, von Eynatten M, Mattheus M, et al. Empagliflozin and progression of kidney disease in type 2 diabetes. N Engl J Med. 2016;375:323–34.PubMedCrossRef Wanner C, Inzucchi SE, Lachin JM, Fitchett D, von Eynatten M, Mattheus M, et al. Empagliflozin and progression of kidney disease in type 2 diabetes. N Engl J Med. 2016;375:323–34.PubMedCrossRef
70.
go back to reference Neal B, Perkovic V, Mahaffey KW, de Zeeuw D, Fulcher G, Erondu N, et al. Canagliflozin and cardiovascular and renal events in type 2 diabetes. N Engl J Med. 2017;377:644–57.PubMedCrossRef Neal B, Perkovic V, Mahaffey KW, de Zeeuw D, Fulcher G, Erondu N, et al. Canagliflozin and cardiovascular and renal events in type 2 diabetes. N Engl J Med. 2017;377:644–57.PubMedCrossRef
71.
go back to reference Ott C, Jumar A, Striepe K, Friedrich S, Karg MV, Bramlage P, et al. A randomised study of the impact of the SGLT2 inhibitor dapagliflozin on microvascular and macrovascular circulation. Cardiovasc Diabetol. 2017;16:26.PubMedPubMedCentralCrossRef Ott C, Jumar A, Striepe K, Friedrich S, Karg MV, Bramlage P, et al. A randomised study of the impact of the SGLT2 inhibitor dapagliflozin on microvascular and macrovascular circulation. Cardiovasc Diabetol. 2017;16:26.PubMedPubMedCentralCrossRef
72.
go back to reference Kim KM, Jung KY, Yun HM, Lee SY, Oh TJ, Jang HC, et al. Effect of rosuvastatin on fasting and postprandial endothelial biomarker levels and microvascular reactivity in patients with type 2 diabetes and dyslipidemia: a preliminary report. Cardiovasc Diabetol. 2017;16:146.PubMedPubMedCentralCrossRef Kim KM, Jung KY, Yun HM, Lee SY, Oh TJ, Jang HC, et al. Effect of rosuvastatin on fasting and postprandial endothelial biomarker levels and microvascular reactivity in patients with type 2 diabetes and dyslipidemia: a preliminary report. Cardiovasc Diabetol. 2017;16:146.PubMedPubMedCentralCrossRef
73.
go back to reference Iacobellis G, Cipriani R, Gabriele A, Di Mario U, Morano S. High circulating vascular endothelial growth factor (VEGF) is related to a better systolic function in diabetic hypertensive patients. Cytokine. 2004;27:25–30.PubMedCrossRef Iacobellis G, Cipriani R, Gabriele A, Di Mario U, Morano S. High circulating vascular endothelial growth factor (VEGF) is related to a better systolic function in diabetic hypertensive patients. Cytokine. 2004;27:25–30.PubMedCrossRef
74.
go back to reference Mourad JJ, des Guetz G, Debbabi H, Levy BI. Blood pressure rise following angiogenesis inhibition by bevacizumab. A crucial role for microcirculation. Ann Oncol. 2008;19:927–34.PubMedCrossRef Mourad JJ, des Guetz G, Debbabi H, Levy BI. Blood pressure rise following angiogenesis inhibition by bevacizumab. A crucial role for microcirculation. Ann Oncol. 2008;19:927–34.PubMedCrossRef
75.
go back to reference Fukami M, Iwase T, Yamamoto K, Kaneko H, Yasuda S, Terasaki H. Changes in retinal microcirculation after intravitreal ranibizumab injection in eyes with macular edema secondary to branch retinal vein occlusion. Invest Ophthalmol Vis Sci. 2017;58:1246–55.PubMedCrossRef Fukami M, Iwase T, Yamamoto K, Kaneko H, Yasuda S, Terasaki H. Changes in retinal microcirculation after intravitreal ranibizumab injection in eyes with macular edema secondary to branch retinal vein occlusion. Invest Ophthalmol Vis Sci. 2017;58:1246–55.PubMedCrossRef
76.
go back to reference Svensson MK, Cederholm J, Eliasson B, Zethelius B, Gudbjörnsdottir S. Albuminuria and renal function as predictors of cardiovascular events and mortality in a general population of patients with type 2 diabetes: a nationwide observational study from the Swedish National Diabetes Register. Diab Vasc Dis Res. 2013;10:520–9.PubMedCrossRef Svensson MK, Cederholm J, Eliasson B, Zethelius B, Gudbjörnsdottir S. Albuminuria and renal function as predictors of cardiovascular events and mortality in a general population of patients with type 2 diabetes: a nationwide observational study from the Swedish National Diabetes Register. Diab Vasc Dis Res. 2013;10:520–9.PubMedCrossRef
77.
go back to reference Wachtell K, Ibsen H, Olsen MH, Borch-Johnsen K, Lindholm LH, Mogensen CE, et al. Albuminuria and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE study. Ann Intern Med. 2003;139:901–6.PubMedCrossRef Wachtell K, Ibsen H, Olsen MH, Borch-Johnsen K, Lindholm LH, Mogensen CE, et al. Albuminuria and cardiovascular risk in hypertensive patients with left ventricular hypertrophy: the LIFE study. Ann Intern Med. 2003;139:901–6.PubMedCrossRef
78.
go back to reference Xia F, Liu G, Shi Y, Zhang Y. Impact of microalbuminuria on incident coronary heart disease, cardiovascular and all-cause mortality: a meta-analysis of prospective studies. Int J Clin Exp Med. 2015;8:1–9.PubMedPubMedCentral Xia F, Liu G, Shi Y, Zhang Y. Impact of microalbuminuria on incident coronary heart disease, cardiovascular and all-cause mortality: a meta-analysis of prospective studies. Int J Clin Exp Med. 2015;8:1–9.PubMedPubMedCentral
79.
go back to reference Klausen KP, Scharling H, Jensen JS. Very low level of microalbuminuria is associated with increased risk of death in subjects with cardiovascular or cerebrovascular diseases. J Intern Med. 2006;260:231–7.PubMedCrossRef Klausen KP, Scharling H, Jensen JS. Very low level of microalbuminuria is associated with increased risk of death in subjects with cardiovascular or cerebrovascular diseases. J Intern Med. 2006;260:231–7.PubMedCrossRef
80.
go back to reference Strain WD, Shore AC, Melzer D. Albumin:creatinine ratio predicts mortality after stroke: analysis of the NHANES III. J Am Geriatr Soc. 2010;58:2434–5.PubMedCrossRef Strain WD, Shore AC, Melzer D. Albumin:creatinine ratio predicts mortality after stroke: analysis of the NHANES III. J Am Geriatr Soc. 2010;58:2434–5.PubMedCrossRef
81.
go back to reference Bottcher M, Madsen MM, Refsgaard J, Buus NH, Dørup I, Nielsen TT, et al. Peripheral flow response to transient arterial forearm occlusion does not reflect myocardial perfusion reserve. Circulation. 2001;103:1109–14.PubMedCrossRef Bottcher M, Madsen MM, Refsgaard J, Buus NH, Dørup I, Nielsen TT, et al. Peripheral flow response to transient arterial forearm occlusion does not reflect myocardial perfusion reserve. Circulation. 2001;103:1109–14.PubMedCrossRef
82.
go back to reference Solini A, Penno G, Bonora E, Fondelli C, Orsi E, Arosio M, et al. Diverging association of reduced glomerular filtration rate and albuminuria with coronary and non-coronary events in patients with type 2 diabetes: the renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care. 2012;35:143–9.PubMedCrossRef Solini A, Penno G, Bonora E, Fondelli C, Orsi E, Arosio M, et al. Diverging association of reduced glomerular filtration rate and albuminuria with coronary and non-coronary events in patients with type 2 diabetes: the renal insufficiency and cardiovascular events (RIACE) Italian multicenter study. Diabetes Care. 2012;35:143–9.PubMedCrossRef
83.
go back to reference Naidoo DP. The link between microalbuminuria, endothelial dysfunction and cardiovascular disease in diabetes. Cardiovasc J S Afr. 2002;13:194–9.PubMed Naidoo DP. The link between microalbuminuria, endothelial dysfunction and cardiovascular disease in diabetes. Cardiovasc J S Afr. 2002;13:194–9.PubMed
84.
go back to reference Collaboration Emerging Risk Factors, Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375:2215–22.CrossRef Collaboration Emerging Risk Factors, Sarwar N, Gao P, Seshasai SR, Gobin R, Kaptoge S, et al. Diabetes mellitus, fasting blood glucose concentration, and risk of vascular disease: a collaborative meta-analysis of 102 prospective studies. Lancet. 2010;375:2215–22.CrossRef
85.
go back to reference Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. 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;339:229–34.PubMedCrossRef Haffner SM, Lehto S, Rönnemaa T, Pyörälä K, Laakso M. 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;339:229–34.PubMedCrossRef
86.
go back to reference Sezer M, Kocaaga M, Aslanger E, Atici A, Demirkiran A, Bugra Z, et al. Bimodal pattern of coronary microvascular involvement in diabetes mellitus. J Am Heart Assoc. 2016;5(11):e003995.PubMedPubMedCentralCrossRef Sezer M, Kocaaga M, Aslanger E, Atici A, Demirkiran A, Bugra Z, et al. Bimodal pattern of coronary microvascular involvement in diabetes mellitus. J Am Heart Assoc. 2016;5(11):e003995.PubMedPubMedCentralCrossRef
87.
go back to reference El-Asrar MA, Andrawes NG, Ismail EA, Salem SM. Kallistatin as a marker of microvascular complications in children and adolescents with type 1 diabetes mellitus: relation to carotid intima media thickness. Vasc Med. 2015;20:509–17.PubMedCrossRef El-Asrar MA, Andrawes NG, Ismail EA, Salem SM. Kallistatin as a marker of microvascular complications in children and adolescents with type 1 diabetes mellitus: relation to carotid intima media thickness. Vasc Med. 2015;20:509–17.PubMedCrossRef
88.
go back to reference Hannemann MM, Liddell WG, Shore AC, Clark PM, Tooke JE. Vascular function in women with previous gestational diabetes mellitus. J Vasc Res. 2002;39:311–9.PubMedCrossRef Hannemann MM, Liddell WG, Shore AC, Clark PM, Tooke JE. Vascular function in women with previous gestational diabetes mellitus. J Vasc Res. 2002;39:311–9.PubMedCrossRef
89.
go back to reference Jaap AJ, Hammersley MS, Shore AC, Tooke JE. Reduced microvascular hyperaemia in subjects at risk of developing type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1994;37:214–6.PubMedCrossRef Jaap AJ, Hammersley MS, Shore AC, Tooke JE. Reduced microvascular hyperaemia in subjects at risk of developing type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia. 1994;37:214–6.PubMedCrossRef
90.
go back to reference Hsu PC, Liao PY, Chang HH, Chiang JY, Huang YC, Lo LC. Nailfold capillary abnormalities are associated with type 2 diabetes progression and correlated with peripheral neuropathy. Medicine. 2016;95:e5714.PubMedPubMedCentralCrossRef Hsu PC, Liao PY, Chang HH, Chiang JY, Huang YC, Lo LC. Nailfold capillary abnormalities are associated with type 2 diabetes progression and correlated with peripheral neuropathy. Medicine. 2016;95:e5714.PubMedPubMedCentralCrossRef
91.
go back to reference Jaap AJ, Pym CA, Seamark C, Shore AC, Tooke JE. Microvascular function in type 2 (non-insulin-dependent) diabetes: improved vasodilation after one year of good glycaemic control. Diabet Med. 1995;12:1086–91.PubMedCrossRef Jaap AJ, Pym CA, Seamark C, Shore AC, Tooke JE. Microvascular function in type 2 (non-insulin-dependent) diabetes: improved vasodilation after one year of good glycaemic control. Diabet Med. 1995;12:1086–91.PubMedCrossRef
92.
go back to reference Caballero AE, Arora S, Saouaf R, Lim SC, Smakowski P, Park JY, et al. Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes. 1999;48:1856–62.PubMedCrossRef Caballero AE, Arora S, Saouaf R, Lim SC, Smakowski P, Park JY, et al. Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes. 1999;48:1856–62.PubMedCrossRef
93.
go back to reference Jonasson H, Bergstrand S, Nystrom FH, Länne T, Östgren CJ, Bjarnegård N, et al. Skin microvascular endothelial dysfunction is associated with type 2 diabetes independently of microalbuminuria and arterial stiffness. Diab Vasc Dis Res. 2017;14:363–71.PubMedCrossRef Jonasson H, Bergstrand S, Nystrom FH, Länne T, Östgren CJ, Bjarnegård N, et al. Skin microvascular endothelial dysfunction is associated with type 2 diabetes independently of microalbuminuria and arterial stiffness. Diab Vasc Dis Res. 2017;14:363–71.PubMedCrossRef
94.
go back to reference Casanova F, Adingupu DD, Adams F, Gooding KM, Looker HC, Aizawa K, et al. The impact of cardiovascular co-morbidities and duration of diabetes on the association between microvascular function and glycaemic control Cardiovasc Diabetol. 2017;16:114.PubMed Casanova F, Adingupu DD, Adams F, Gooding KM, Looker HC, Aizawa K, et al. The impact of cardiovascular co-morbidities and duration of diabetes on the association between microvascular function and glycaemic control Cardiovasc Diabetol. 2017;16:114.PubMed
95.
go back to reference Vinik AI, Stansberry KB, Barlow PM. Rosiglitazone treatment increases nitric oxide production in human peripheral skin: a controlled clinical trial in patients with type 2 diabetes mellitus. J Diabetes Complications. 2003;17:279–85.PubMedCrossRef Vinik AI, Stansberry KB, Barlow PM. Rosiglitazone treatment increases nitric oxide production in human peripheral skin: a controlled clinical trial in patients with type 2 diabetes mellitus. J Diabetes Complications. 2003;17:279–85.PubMedCrossRef
96.
go back to reference Ijzerman RG, de Jongh RT, Beijk MA, van Weissenbruch MM, Delemarre-van de Waal HA, Serné EH, et al. Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur J Clin Invest. 2003;33:536–42.PubMedCrossRef Ijzerman RG, de Jongh RT, Beijk MA, van Weissenbruch MM, Delemarre-van de Waal HA, Serné EH, et al. Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur J Clin Invest. 2003;33:536–42.PubMedCrossRef
97.
go back to reference Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, et al. Attenuation of microvascular function in those with cardiovascular disease is similar in patients of Indian Asian and European descent. BMC Cardiovasc Disord. 2010;10:3.PubMedPubMedCentralCrossRef Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, et al. Attenuation of microvascular function in those with cardiovascular disease is similar in patients of Indian Asian and European descent. BMC Cardiovasc Disord. 2010;10:3.PubMedPubMedCentralCrossRef
98.
go back to reference Östlund Papadogeorgos N, Jörneskog G, Bengtsson M, Kahan T, Kalani M. Severely impaired microvascular reactivity in diabetic patients with an acute coronary syndrome. Cardiovasc Diabetol. 2016;15:66.PubMedPubMedCentralCrossRef Östlund Papadogeorgos N, Jörneskog G, Bengtsson M, Kahan T, Kalani M. Severely impaired microvascular reactivity in diabetic patients with an acute coronary syndrome. Cardiovasc Diabetol. 2016;15:66.PubMedPubMedCentralCrossRef
99.
go back to reference Rathsman B, Jensen-Urstad K, Nyström T. Intensified insulin treatment is associated with improvement in skin microcirculation and ischaemic foot ulcer in patients with type 1 diabetes mellitus: a long-term follow-up study. Diabetologia. 2014;57:1703–10.PubMedCrossRef Rathsman B, Jensen-Urstad K, Nyström T. Intensified insulin treatment is associated with improvement in skin microcirculation and ischaemic foot ulcer in patients with type 1 diabetes mellitus: a long-term follow-up study. Diabetologia. 2014;57:1703–10.PubMedCrossRef
100.
go back to reference Chaturvedi N, Jarrett J, Morrish N, Keen H, Fuller JH. Differences in mortality and morbidity in African Caribbean and European people with non-insulin dependent diabetes mellitus: results of 20 year follow up of a London cohort of a multinational study. BMJ. 1996;313:848–52.PubMedPubMedCentralCrossRef Chaturvedi N, Jarrett J, Morrish N, Keen H, Fuller JH. Differences in mortality and morbidity in African Caribbean and European people with non-insulin dependent diabetes mellitus: results of 20 year follow up of a London cohort of a multinational study. BMJ. 1996;313:848–52.PubMedPubMedCentralCrossRef
101.
go back to reference Strain WD, Chaturvedi N, Leggetter S, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, et al. Ethnic differences in skin microvascular function and their relation to cardiac target-organ damage. J Hypertens. 2005;23:133–40.PubMedCrossRef Strain WD, Chaturvedi N, Leggetter S, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, et al. Ethnic differences in skin microvascular function and their relation to cardiac target-organ damage. J Hypertens. 2005;23:133–40.PubMedCrossRef
102.
go back to reference Strain WD, Chaturvedi N, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, Shore AC. Differences in the association between type 2 diabetes and impaired microvascular function among Europeans and African Caribbeans. Diabetologia. 2005;48:2269–77.PubMedCrossRef Strain WD, Chaturvedi N, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, Shore AC. Differences in the association between type 2 diabetes and impaired microvascular function among Europeans and African Caribbeans. Diabetologia. 2005;48:2269–77.PubMedCrossRef
103.
go back to reference Lucas J, Schiller J, Benson V. Summary health statistics for US adults: National Health Interview Survey, 2001. National Center for Health Statistics. Vital Health Stat. 2004;2004(10):1–134. Lucas J, Schiller J, Benson V. Summary health statistics for US adults: National Health Interview Survey, 2001. National Center for Health Statistics. Vital Health Stat. 2004;2004(10):1–134.
104.
go back to reference Harris MI, Klein R, Cowie CC, Rowland M, Byrd-Holt DD. Is the risk of diabetic retinopathy greater in non-Hispanic blacks and Mexican Americans than in non-Hispanic whites with type 2 diabetes? A US population study. Diabetes Care. 1998;21:1230–5.PubMedCrossRef Harris MI, Klein R, Cowie CC, Rowland M, Byrd-Holt DD. Is the risk of diabetic retinopathy greater in non-Hispanic blacks and Mexican Americans than in non-Hispanic whites with type 2 diabetes? A US population study. Diabetes Care. 1998;21:1230–5.PubMedCrossRef
105.
go back to reference Wong TY, Klein R, Sharrett AR, Couper DJ, Klein BE, Liao DP, et al. Cerebral white matter lesions, retinopathy, and incident clinical stroke. JAMA. 2002;288:67–74.PubMedCrossRef Wong TY, Klein R, Sharrett AR, Couper DJ, Klein BE, Liao DP, et al. Cerebral white matter lesions, retinopathy, and incident clinical stroke. JAMA. 2002;288:67–74.PubMedCrossRef
106.
go back to reference Fuchs D, Dupon PP, Schaap LA, Draijer R. The association between diabetes and dermal microvascular dysfunction non-invasively assessed by laser Doppler with local thermal hyperemia: a systematic review with meta-analysis. Cardiovasc Diabetol. 2017;16:11.PubMedPubMedCentralCrossRef Fuchs D, Dupon PP, Schaap LA, Draijer R. The association between diabetes and dermal microvascular dysfunction non-invasively assessed by laser Doppler with local thermal hyperemia: a systematic review with meta-analysis. Cardiovasc Diabetol. 2017;16:11.PubMedPubMedCentralCrossRef
108.
go back to reference de Jong PE, Hillege HL, Pinto-Sietsma SJ, de Zeeuw D. Screening for microalbuminuria in the general population: a tool to detect subjects at risk for progressive renal failure in an early phase? Nephrol Dial Transplant. 2003;18:10–3.PubMedCrossRef de Jong PE, Hillege HL, Pinto-Sietsma SJ, de Zeeuw D. Screening for microalbuminuria in the general population: a tool to detect subjects at risk for progressive renal failure in an early phase? Nephrol Dial Transplant. 2003;18:10–3.PubMedCrossRef
Metadata
Title
Diabetes, cardiovascular disease and the microcirculation
Authors
W. David Strain
P. M. Paldánius
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2018
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-018-0703-2

Other articles of this Issue 1/2018

Cardiovascular Diabetology 1/2018 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.