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Published in: Cardiovascular Diabetology 1/2016

Open Access 01-12-2016 | Original investigation

Severely impaired microvascular reactivity in diabetic patients with an acute coronary syndrome

Authors: Nikolaos Östlund Papadogeorgos, Gun Jörneskog, Mattias Bengtsson, Thomas Kahan, Majid Kalani

Published in: Cardiovascular Diabetology | Issue 1/2016

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Abstract

Background

Microvascular function is impaired in patients with stable coronary artery disease. The aim was to study microvascular function in patients with diabetes and acute coronary syndrome (ACS).

Methods

Microvascular function was evaluated in 83 patients by laser Doppler fluxmetry (LDF) [PU; perfusion unit, median (interquartile range)] measuring resting LDF and peak LDF following a six min heating of the skin to 44 °C at the foot, respectively. All patients with ACS and without previously known diabetes underwent oral glucose tolerance test. Thirty-nine patients with type 2 diabetes mellitus free from coronary artery disease served as controls.

Results

Peak LDF was significantly (P = 0.03) lower in patients with ACS and diabetes (n = 22; 72 (52)) and diabetes without coronary artery disease (n = 39; 69 (51)) as compared to patients with ACS without diabetes (n = 46; 97 (60)), and patients without ACS (n = 15; 140 (121)), respectively. Patients with ACS (n = 68) had significantly (P = 0.04) lower peak LDF (92 (49)) as compared to patients without ACS (n = 15) (140 (121)).

Conclusion

Microvascular reactivity is severely impaired in patients with diabetes and ACS. Diabetes has a major influence on microvascular function in patients with coronary artery disease.
Literature
1.
go back to reference Ijzerman RG, de Jongh RT, Beijk MA, van Weissenbruch MM, de Delemarre-van HA, Serné EH, Stehouwer CD. Individuals at increased coronary heart disease risk are characterised by an impaired microvascular function in skin. Eur J Clin Invest. 2003;33:536–42.CrossRefPubMed Ijzerman RG, de Jongh RT, Beijk MA, van Weissenbruch MM, de Delemarre-van HA, Serné EH, Stehouwer CD. Individuals at increased coronary heart disease risk are characterised by an impaired microvascular function in skin. Eur J Clin Invest. 2003;33:536–42.CrossRefPubMed
2.
go back to reference Strain WD, Chaturvedi N, Hughes A, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, Shore AC. Associations between cardiac target organ damage and microvascular dysfunction: the role of blood pressure. J Hypertens. 2010;28:952–8.CrossRefPubMed Strain WD, Chaturvedi N, Hughes A, Nihoyannopoulos P, Bulpitt CJ, Rajkumar C, Shore AC. Associations between cardiac target organ damage and microvascular dysfunction: the role of blood pressure. J Hypertens. 2010;28:952–8.CrossRefPubMed
3.
go back to reference Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Hallé JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286:421–6.CrossRefPubMed Gerstein HC, Mann JF, Yi Q, Zinman B, Dinneen SF, Hoogwerf B, Hallé JP, Young J, Rashkow A, Joyce C, Nawaz S, Yusuf S. Albuminuria and risk of cardiovascular events, death, and heart failure in diabetic and nondiabetic individuals. JAMA. 2001;286:421–6.CrossRefPubMed
4.
go back to reference Ljungman S, Wikstrand J, Hartford M, Berglund G. Urinary albumin excretion: a predictor of risk of cardiovascular disease. A prospective 10-year follow-up of middle-aged nondiabetic normal and hypertensive men. Am J Hypertens. 1996;9:770–8.CrossRefPubMed Ljungman S, Wikstrand J, Hartford M, Berglund G. Urinary albumin excretion: a predictor of risk of cardiovascular disease. A prospective 10-year follow-up of middle-aged nondiabetic normal and hypertensive men. Am J Hypertens. 1996;9:770–8.CrossRefPubMed
5.
go back to reference Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR, Lerman A. Longterm follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation. 2000;101:948–54.CrossRefPubMed Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR, Lerman A. Longterm follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation. 2000;101:948–54.CrossRefPubMed
6.
go back to reference Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003;23:168–75.CrossRefPubMed Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: a marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol. 2003;23:168–75.CrossRefPubMed
7.
go back to reference Widlansky ME, Gokce N, Keaney JF, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol. 2003;42:1149–60.CrossRefPubMed Widlansky ME, Gokce N, Keaney JF, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol. 2003;42:1149–60.CrossRefPubMed
8.
go back to reference Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation. 2000;101:1899–906.CrossRefPubMed Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation. 2000;101:1899–906.CrossRefPubMed
9.
go back to reference Seino Y. Cardiac function and peripheral circulatory adjustments in patients with acute myocardial infarction. Observations during the early stage of AMI. Jpn Heart J. 1983;24:515–28.CrossRefPubMed Seino Y. Cardiac function and peripheral circulatory adjustments in patients with acute myocardial infarction. Observations during the early stage of AMI. Jpn Heart J. 1983;24:515–28.CrossRefPubMed
10.
go back to reference Skagen K, Henriksen O, Amtorp O, Fog-Moller F, Lam H. Local regulation of blood flow in subcutaneous tissue in patients with acute myocardial infarction. Clin Sci. 1981;60:157–64.CrossRefPubMed Skagen K, Henriksen O, Amtorp O, Fog-Moller F, Lam H. Local regulation of blood flow in subcutaneous tissue in patients with acute myocardial infarction. Clin Sci. 1981;60:157–64.CrossRefPubMed
11.
go back to reference Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, Shore AC. Attenuation of microvascular function in those with cardiovascular disease is similar in patients of Indian Asian and European descent. BMC Cardiovasc Disord. 2010;15(10):3.CrossRef Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, Shore AC. Attenuation of microvascular function in those with cardiovascular disease is similar in patients of Indian Asian and European descent. BMC Cardiovasc Disord. 2010;15(10):3.CrossRef
12.
go back to reference Azman-Juvan K, Bernjak A, Urbancic-Rovan V, Stefanovska A, Stajer D. Skin blood flow and its oscillatory components in patients with acute myocardial infarction. J Vasc Res. 2008;45:164–72.CrossRefPubMed Azman-Juvan K, Bernjak A, Urbancic-Rovan V, Stefanovska A, Stajer D. Skin blood flow and its oscillatory components in patients with acute myocardial infarction. J Vasc Res. 2008;45:164–72.CrossRefPubMed
13.
go back to reference Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, Shore AC. Attenuated systemic microvascular function in men with coronary artery disease is associated with angina but not explained by atherosclerosis. Microcirculation. 2013;20:670–7.CrossRefPubMed Strain WD, Hughes AD, Mayet J, Wright AR, Kooner J, Chaturvedi N, Shore AC. Attenuated systemic microvascular function in men with coronary artery disease is associated with angina but not explained by atherosclerosis. Microcirculation. 2013;20:670–7.CrossRefPubMed
14.
go back to reference Agarwal SC, Allen J, Murray A, Purcell IF. Laser Doppler assessment of dermal circulatory changes in people with coronary artery disease. Microvasc Res. 2012;84:55–9.CrossRefPubMed Agarwal SC, Allen J, Murray A, Purcell IF. Laser Doppler assessment of dermal circulatory changes in people with coronary artery disease. Microvasc Res. 2012;84:55–9.CrossRefPubMed
15.
go back to reference Tibirica E, Souza EG, De Lorenzo A, Oliveira GM. Reduced systemic microvascular density and reactivity in individuals with early onset coronary artery disease. Microvasc Res. 2015;97:105–8.CrossRefPubMed Tibirica E, Souza EG, De Lorenzo A, Oliveira GM. Reduced systemic microvascular density and reactivity in individuals with early onset coronary artery disease. Microvasc Res. 2015;97:105–8.CrossRefPubMed
16.
go back to reference Souza EG, De Lorenzo A, Huguenot G, Oliveira GM, Tibirica E. Impairment of systemic microvascular endothelial and smooth muscle function in individuals with early-onset coronary artery disease: studies with laser speckle contrast imaging. Coron Artery Dis. 2014;25(1):23–8.CrossRefPubMed Souza EG, De Lorenzo A, Huguenot G, Oliveira GM, Tibirica E. Impairment of systemic microvascular endothelial and smooth muscle function in individuals with early-onset coronary artery disease: studies with laser speckle contrast imaging. Coron Artery Dis. 2014;25(1):23–8.CrossRefPubMed
17.
go back to reference Ovadia-Blechman Z, Avrahami I, Weizman-Shammai E, Sharir T, Eldar M, Chouraqui P. Peripheral microcirculatory hemodynamic changes in patients with myocardial ischemia. Biomed Pharmacother. 2015;74:83–8.CrossRefPubMed Ovadia-Blechman Z, Avrahami I, Weizman-Shammai E, Sharir T, Eldar M, Chouraqui P. Peripheral microcirculatory hemodynamic changes in patients with myocardial ischemia. Biomed Pharmacother. 2015;74:83–8.CrossRefPubMed
18.
go back to reference Trifunovic D, Stankovic S, Sobic-Saranovic D, Marinkovic J, Petrovic M, Orlic D, Beleslin B, Banovic M, Vujisic-Tesic B, Petrovic M, Nedeljkovic I, Stepanovic J, Djordjevic-Dikic A, Tesic M, Djukanovic N, Petrovic O, Vasovic O, Nestorovic E, Kostic J, Ristic A, Ostojic M. Acute insulin resistance in ST-segment elevation myocardial infarction in non-diabetic patients is associated with incomplete myocardial reperfusion and impaired coronary microcirculatory function. Cardiovasc Diabetol. 2014;13:73.CrossRefPubMedPubMedCentral Trifunovic D, Stankovic S, Sobic-Saranovic D, Marinkovic J, Petrovic M, Orlic D, Beleslin B, Banovic M, Vujisic-Tesic B, Petrovic M, Nedeljkovic I, Stepanovic J, Djordjevic-Dikic A, Tesic M, Djukanovic N, Petrovic O, Vasovic O, Nestorovic E, Kostic J, Ristic A, Ostojic M. Acute insulin resistance in ST-segment elevation myocardial infarction in non-diabetic patients is associated with incomplete myocardial reperfusion and impaired coronary microcirculatory function. Cardiovasc Diabetol. 2014;13:73.CrossRefPubMedPubMedCentral
19.
go back to reference Norhammar A, Tenerz Å, Nilsson G, Hamsten A, Efendic S, Rydén L, Malmberg K. Glucose metabolism in patients with acute myocardial infarction and no previous diagnosis of diabetes mellitus: a prospective study. Lancet. 2002;359:2140–4.CrossRefPubMed Norhammar A, Tenerz Å, Nilsson G, Hamsten A, Efendic S, Rydén L, Malmberg K. Glucose metabolism in patients with acute myocardial infarction and no previous diagnosis of diabetes mellitus: a prospective study. Lancet. 2002;359:2140–4.CrossRefPubMed
20.
go back to reference Kuhl J, Jörneskog G, Wemminger M, Bengtsson M, Lundman P, Kalani M. Long-term clinical outcome in patients with acute coronary syndrome and dysglycaemia. Cardiovasc Diabetol. 2015;14(1):120.CrossRefPubMedPubMedCentral Kuhl J, Jörneskog G, Wemminger M, Bengtsson M, Lundman P, Kalani M. Long-term clinical outcome in patients with acute coronary syndrome and dysglycaemia. Cardiovasc Diabetol. 2015;14(1):120.CrossRefPubMedPubMedCentral
21.
go back to reference Jarnert C, Kalani M, Rydén L, Böhm F. Strict glycaemic control improves skin microcirculation in patients with type 2 diabetes: a report from the diabetes mellitus and diastolic dysfunction (DADD) study. Diab Vasc Dis Res. 2012;9(4):287–95.CrossRefPubMed Jarnert C, Kalani M, Rydén L, Böhm F. Strict glycaemic control improves skin microcirculation in patients with type 2 diabetes: a report from the diabetes mellitus and diastolic dysfunction (DADD) study. Diab Vasc Dis Res. 2012;9(4):287–95.CrossRefPubMed
22.
go back to reference Myocardial infarction redefined—a consensus document of The Joint European Society of Cardiology/American College of Cardiology Committee for the redefinition of myocardial infarction. Eur Heart J. 2000; 21(18):1502–13. Myocardial infarction redefined—a consensus document of The Joint European Society of Cardiology/American College of Cardiology Committee for the redefinition of myocardial infarction. Eur Heart J. 2000; 21(18):1502–13.
23.
go back to reference Report of the Expert Committee on the diagnosis and classification of diabetes mellitus. Diabetes care. 1997; 20(7):1183–97. Report of the Expert Committee on the diagnosis and classification of diabetes mellitus. Diabetes care. 1997; 20(7):1183–97.
24.
go back to reference Fagrell B, Jörneskog G, Intaglietta M. Disturbed microvascular reactivity and shunting—a major cause for diabetic complications. Vasc Med. 1999;4:125–7.CrossRefPubMed Fagrell B, Jörneskog G, Intaglietta M. Disturbed microvascular reactivity and shunting—a major cause for diabetic complications. Vasc Med. 1999;4:125–7.CrossRefPubMed
25.
go back to reference Tooke JE. Possible pathophysiological mechanisms for diabetic angiopathy in type 2 diabetes. J Diabetes Complications. 2000;14:197–200.CrossRefPubMed Tooke JE. Possible pathophysiological mechanisms for diabetic angiopathy in type 2 diabetes. J Diabetes Complications. 2000;14:197–200.CrossRefPubMed
26.
go back to reference Cheung N, Wang JJ, Rogers SL, et al. Diabetic retinopathy and risk of heart failure. J Am Coll Cardiol. 2008;51:1573–8.CrossRefPubMed Cheung N, Wang JJ, Rogers SL, et al. Diabetic retinopathy and risk of heart failure. J Am Coll Cardiol. 2008;51:1573–8.CrossRefPubMed
27.
go back to reference Papadogeorgos ÖN, 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;5:893–9.PubMed Papadogeorgos ÖN, 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;5:893–9.PubMed
28.
go back to reference Verouden NJW, Haeck JDE, Kuijt WJ, Meuwissen M, Koch KT, Henriques JPS, Baan J, Vis MM, Piek JJ, Tijssen JGP, Winter RJ. Clinical and angiographic predictors of ST-segment recovery after primary percutaneous coronary intervention. Am J Cardiol. 2010;105:1692–7.CrossRefPubMed Verouden NJW, Haeck JDE, Kuijt WJ, Meuwissen M, Koch KT, Henriques JPS, Baan J, Vis MM, Piek JJ, Tijssen JGP, Winter RJ. Clinical and angiographic predictors of ST-segment recovery after primary percutaneous coronary intervention. Am J Cardiol. 2010;105:1692–7.CrossRefPubMed
29.
go back to reference Hokama JY, Ritter LS, Davis-Gorman G, Cimetta AD, Copeland JG, McDonagh PF. Diabetes enhances leukocyte accumulation in the coronary microcirculation early in reperfusion following ischemia. J Diabetes Complication. 2000;14:96–107.CrossRef Hokama JY, Ritter LS, Davis-Gorman G, Cimetta AD, Copeland JG, McDonagh PF. Diabetes enhances leukocyte accumulation in the coronary microcirculation early in reperfusion following ischemia. J Diabetes Complication. 2000;14:96–107.CrossRef
30.
go back to reference Shechter M, Merz CN, Paul-Labrador MJ, Kaul S. Blood glucose and plateletdependent thrombosis in patients with coronary artery disease. J Am Coll Cardiol. 2000;35:300–7.CrossRefPubMed Shechter M, Merz CN, Paul-Labrador MJ, Kaul S. Blood glucose and plateletdependent thrombosis in patients with coronary artery disease. J Am Coll Cardiol. 2000;35:300–7.CrossRefPubMed
31.
go back to reference Sakuma T, Leong-Poi H, Fisher NG, Goodman NC, Kaul S. Further insights into the no-reflow phenomenon after primary angioplasty in acute myocardial infarction: the role of microthromboemboli. J Am Soc Echocardiogr. 2003;16:15–21.CrossRefPubMed Sakuma T, Leong-Poi H, Fisher NG, Goodman NC, Kaul S. Further insights into the no-reflow phenomenon after primary angioplasty in acute myocardial infarction: the role of microthromboemboli. J Am Soc Echocardiogr. 2003;16:15–21.CrossRefPubMed
32.
go back to reference Settergren M, Pernow J, Brismar K, Jörneskog G, Kalani M. Endothelin-A receptor blockade increases nutritive skin capillary circulation in patients with type 2 diabetes and microangiopathy. J Vasc Res. 2008;45:295–302.CrossRefPubMed Settergren M, Pernow J, Brismar K, Jörneskog G, Kalani M. Endothelin-A receptor blockade increases nutritive skin capillary circulation in patients with type 2 diabetes and microangiopathy. J Vasc Res. 2008;45:295–302.CrossRefPubMed
33.
go back to reference Jörneskog G, Brismar K, Fagrell B. Skin capillary circulation is more impaired in the toes of diabetic than non-diabetic patients with peripheral vascular disease. Diabet Med. 1995;12:36–41.CrossRefPubMed Jörneskog G, Brismar K, Fagrell B. Skin capillary circulation is more impaired in the toes of diabetic than non-diabetic patients with peripheral vascular disease. Diabet Med. 1995;12:36–41.CrossRefPubMed
34.
go back to reference Settergren M, Böhm F, Rydén L, Pernow J, Kalani M. Lipid lowering versus pleiotropic effects of statins on skin microvascular function in patients with dysglycaemia and coronary artery disease. J Intern Med. 2009;266:492–8.CrossRefPubMed Settergren M, Böhm F, Rydén L, Pernow J, Kalani M. Lipid lowering versus pleiotropic effects of statins on skin microvascular function in patients with dysglycaemia and coronary artery disease. J Intern Med. 2009;266:492–8.CrossRefPubMed
35.
go back to reference Jarnert C, Kalani M, Rydén L, Böhm F. Strict glycaemic control improves skin microcirculation in patients with type 2 diabetes: a report from the diabetes mellitus and diastolic dysfunction (DADD) study. Diab Vasc Dis Res. 2012;9(4):287–95.CrossRefPubMed Jarnert C, Kalani M, Rydén L, Böhm F. Strict glycaemic control improves skin microcirculation in patients with type 2 diabetes: a report from the diabetes mellitus and diastolic dysfunction (DADD) study. Diab Vasc Dis Res. 2012;9(4):287–95.CrossRefPubMed
36.
go back to reference Strain WD, Chaturvedi N, Leggetter S, Nihoyannopoulos P, Rajkumar C, Bulpitt CJ, Shore AC. Ethnic differences in skin microvascular function and their relation to cardiac target- organ damage. J Hypertens. 2005;23:133–40.CrossRefPubMed Strain WD, Chaturvedi N, Leggetter S, Nihoyannopoulos P, Rajkumar C, Bulpitt CJ, Shore AC. Ethnic differences in skin microvascular function and their relation to cardiac target- organ damage. J Hypertens. 2005;23:133–40.CrossRefPubMed
37.
go back to reference Gooding KM, Hannemann MM, Tooke JE, Clough GF, Shore AC. Maximum skin hyperaemia induced by local heating: possible mechanisms. J Vasc Res. 2006;43:270–7.CrossRefPubMed Gooding KM, Hannemann MM, Tooke JE, Clough GF, Shore AC. Maximum skin hyperaemia induced by local heating: possible mechanisms. J Vasc Res. 2006;43:270–7.CrossRefPubMed
38.
go back to reference Roustit M, Blaise S, Millet C, Cracowski JL. Reproducibility and methodological issues of skin post-occlusive and thermal hyperemia assessed by single-point laser Doppler flowmetry. Microvasc Res. 2010;79(2):102–8.CrossRefPubMed Roustit M, Blaise S, Millet C, Cracowski JL. Reproducibility and methodological issues of skin post-occlusive and thermal hyperemia assessed by single-point laser Doppler flowmetry. Microvasc Res. 2010;79(2):102–8.CrossRefPubMed
39.
go back to reference Millet C, Roustit M, Blaise S, Cracowski JL. Comparison between laser speckle contrast imaging and laser Doppler imaging to assess skin blood flow in humans. Microvasc Res. 2011;82(2):147–51.CrossRefPubMed Millet C, Roustit M, Blaise S, Cracowski JL. Comparison between laser speckle contrast imaging and laser Doppler imaging to assess skin blood flow in humans. Microvasc Res. 2011;82(2):147–51.CrossRefPubMed
40.
go back to reference Tibiriçá E, Matheus AS, Nunes B, Sperandei S, Gomes MB. Repeatability of the evaluation of systemic microvascular endothelial function using laser doppler perfusion monitoring: clinical and statistical implications. Clinics. 2011;66(4):599–605.PubMedPubMedCentral Tibiriçá E, Matheus AS, Nunes B, Sperandei S, Gomes MB. Repeatability of the evaluation of systemic microvascular endothelial function using laser doppler perfusion monitoring: clinical and statistical implications. Clinics. 2011;66(4):599–605.PubMedPubMedCentral
Metadata
Title
Severely impaired microvascular reactivity in diabetic patients with an acute coronary syndrome
Authors
Nikolaos Östlund Papadogeorgos
Gun Jörneskog
Mattias Bengtsson
Thomas Kahan
Majid Kalani
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2016
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-016-0385-6

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