Do patients with type 1 and type 2 diabetes really have an impaired endothelial function? A population-based propensity score matching analysis

Cardiovascular Diabetology

Volumn 12, Issue 1, 2013, Pages

  Empen, Klaus ^a   Lorbeer, Roberto ^b   Völzke, Henry ^b,d   Reffelmann, Thorsten ^a,d   Schipf, Sabine ^b   Nauck, Matthias ^b,d   Kerner, Wolfgang ^c   Wallaschofski, Henri ^b,d   Felix, Stephan B ^a,d   Dörr, Marcus ^a,d  

^a UNIVERSITY MEDICINE GREIFSWALD   (Germany)

^b Medical University of Greifswald   (Germany)

^c Diabetes Service Center   (Germany)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

Endothelial function; Epidemiology; Flow mediated dilation; FMD; Type 1 diabetes; Type 2 diabetes

Indexed keywords

ALBUMIN; ANTIHYPERTENSIVE AGENT; GLUCOSE; HEMOGLOBIN A1C; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL;

ADULT; AGED; ALBUMIN BLOOD LEVEL; ARTERY BLOOD FLOW; ARTERY DIAMETER; ARTERY DILATATION; ARTICLE; BLOOD SAMPLING; BODY MASS; BRACHIAL ARTERY; CONTROLLED STUDY; DIABETIC PATIENT; DIASTOLIC BLOOD PRESSURE; ENDOTHELIAL DYSFUNCTION; FEMALE; FLOW MEDIATED DILATION; GLUCOSE BLOOD LEVEL; HUMAN; HYPERTENSION; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OUTPATIENT; PROPENSITY SCORE; SMOKING; SYSTOLIC BLOOD PRESSURE; TRIACYLGLYCEROL BLOOD LEVEL; WAIST CIRCUMFERENCE;

ADULT; AGED; AGED, 80 AND OVER; BRACHIAL ARTERY; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; FEMALE; GERMANY; HUMANS; HYPEREMIA; MALE; MIDDLE AGED; PROPENSITY SCORE; REGIONAL BLOOD FLOW; RISK FACTORS; VASODILATION; YOUNG ADULT;

EID: 84889065169     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-12-174     Document Type: Article

References (29)

1. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the international brachial artery reactivity task force. J Am Coll Cardiol 2002, 39(2):257-265. 10.1016/S0735-1097(01)01746-6, 11788217.
2. Yeboah J, Folsom AR, Burke GL, Johnson C, Polak JF, Post W, Lima JA, Crouse JR, Herrington DM. Predictive value of brachial flow-mediated dilation for incident cardiovascular events in a population-based study: the multi-ethnic study of atherosclerosis. Circulation 2009, 120(6):502-509. 10.1161/CIRCULATIONAHA.109.864801, 2740975, 19635967.
3. Benjamin EJ, Larson MG, Keyes MJ, Mitchell GF, Vasan RS, Keaney JF, Lehman BT, Fan S, Osypiuk E, Vita JA. Clinical correlates and heritability of flow-mediated dilation in the community: the Framingham heart study. Circulation 2004, 109(5):613-619. 10.1161/01.CIR.0000112565.60887.1E, 14769683.
4. Simons LA, Sullivan D, Simons J, Celermajer DS. Effects of atorvastatin monotherapy and simvastatin plus cholestyramine on arterial endothelial function in patients with severe primary hypercholesterolaemia. Atherosclerosis 1998, 137(1):197-203. 10.1016/S0021-9150(97)00252-9, 9568752.
5. Celermajer DS, Sorensen KE, Georgakopoulos D, Bull C, Thomas O, Robinson J, Deanfield JE. Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults. Circulation 1993, 88(5 Pt 1):2149-2155.
6. Ce GV, Rohde LE, Da Silva AM, Punales MK, De Castro AC, Bertoluci MC. Endothelial dysfunction is related to poor glycemic control in adolescents with type 1 diabetes under 5 years of disease: evidence of metabolic memory. J Clin Endocrinol Metab 2011, 96(5):1499-1493.
7. Chan NN, Vallance P, Colhoun HM. Endothelium-dependent and -independent vascular dysfunction in type 1 diabetes: role of conventional risk factors, sex, and glycemic control. Arterioscler Thromb Vasc Biol 2003, 23(6):1048-1054. 10.1161/01.ATV.0000072968.00157.6B, 12714434.
8. Clarkson P, Celermajer DS, Donald AE, Sampson M, Sorensen KE, Adams M, Yue DK, Betteridge DJ, Deanfield JE. Impaired vascular reactivity in insulin-dependent diabetes mellitus is related to disease duration and low density lipoprotein cholesterol levels. J Am Coll Cardiol 1996, 28(3):573-579.
9. Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, Creager MA. Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 1993, 88(6):2510-2516. 10.1161/01.CIR.88.6.2510, 8080489.
10. Sibal L, Agarwal SC, Schwedhelm E, Luneburg N, Boger RH, Home PD. A study of endothelial function and circulating asymmetric dimethylarginine levels in people with Type 1 diabetes without macrovascular disease or microalbuminuria. Cardiovasc Diabetol 2009, 8:27. 10.1186/1475-2840-8-27, 2698883, 19486510.
11. Thorne S, Mullen MJ, Clarkson P, Donald AE, Deanfield JE. Early endothelial dysfunction in adults at risk from atherosclerosis: different responses to L-arginine. J Am Coll Cardiol 1998, 32(1):110-116. 10.1016/S0735-1097(98)00211-3, 9669257.
12. Donald AE, Halcox JP, Charakida M, Storry C, Wallace SM, Cole TJ, Friberg P, Deanfield JE. Methodological approaches to optimize reproducibility and power in clinical studies of flow-mediated dilation. J Am Coll Cardiol 2008, 51(20):1959-1964. 10.1016/j.jacc.2008.02.044, 18482664.
13. Henry RM, Ferreira I, Kostense PJ, Dekker JM, Nijpels G, Heine RJ, Kamp O, Bouter LM, Stehouwer CD. Type 2 diabetes is associated with impaired endothelium-dependent, flow-mediated dilation, but impaired glucose metabolism is not; the hoorn study. Atherosclerosis 2004, 174(1):49-56. 10.1016/j.atherosclerosis.2004.01.002, 15135250.
14. Irace C, Tschakovsky ME, Carallo C, Cortese C, Gnasso A. Endothelial dysfunction or dysfunctions? Identification of three different FMD responses in males with type 2 diabetes. Atherosclerosis 2008, 200(2):439-445. 10.1016/j.atherosclerosis.2007.12.036, 18262189.
15. Reyes-Soffer G, Holleran S, Di Tullio MR, Homma S, Boden-Albala B, Ramakrishnan R, Elkind MS, Sacco RL, Ginsberg HN. Endothelial function in individuals with coronary artery disease with and without type 2 diabetes mellitus. Metabolism 2010, 59(9):1365-1371. 10.1016/j.metabol.2009.12.023, 2891205, 20102776.
16. Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 1996, 27(3):567-574. 10.1016/0735-1097(95)00522-6, 8606266.
17. Naka KK, Papathanassiou K, Bechlioulis A, Kazakos N, Pappas K, Tigas S, Makriyiannis D, Tsatsoulis A, Michalis LK. Determinants of vascular function in patients with type 2 diabetes. Cardiovasc Diabetol 2012, 11:127. 10.1186/1475-2840-11-127, 3490819, 23062182.
18. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med 2007, 147(8):573-577. 10.7326/0003-4819-147-8-200710160-00010, 17938396.
19. Volzke H, Alte D, Schmidt CO, Radke D, Lorbeer R, Friedrich N, Aumann N, Lau K, Piontek M, Born G, et al. Cohort profile: the study of health in Pomerania. Int J Epidemiol 2011, 40(2):294-307. 10.1093/ije/dyp394, 20167617.
20. Lorbeer R, Empen K, Dorr M, Arndt M, Schipf S, Nauck M, Wallaschofski H, Felix SB, Volzke H. Association between glycosylated haemoglobin A(1c) and endothelial function in an adult non-diabetic population. Atherosclerosis 217(2):358-363.
21. Empen K, Lorbeer R, Dorr M, Haring R, Nauck M, Glaser S, Krebs A, Reffelmann T, Ewert R, Volzke H, et al. Association of testosterone levels with endothelial function in Men: results from a population-based study. Arterioscler Thromb Vasc Biol 2012, 32:481-486. 10.1161/ATVBAHA.111.232876, 22095984.
22. Volzke H, Robinson DM, Spielhagen T, Nauck M, Obst A, Ewert R, Wolff B, Wallaschofski H, Felix SB, Dorr M. Are serum thyrotropin levels within the reference range associated with endothelial function?. Eur Heart J 2009, 30(2):217-224.
23. Leuven ESB. PSMATCH2: Stata module to perform full Mahalanobis and propensity score matching, common support graphing, and covariate imbalance testing 2003
24. Feinstein AR. Experimental requirements and scientific principles in case-control studies. J Chronic Dis 1985, 38(2):127-133. 10.1016/0021-9681(85)90085-2, 3972955.
25. Lambert J, Aarsen M, Donker AJ, Stehouwer CD. Endothelium-dependent and -independent vasodilation of large arteries in normoalbuminuric insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 1996, 16(5):705-711. 10.1161/01.ATV.16.5.705, 8963729.
26. Witte DR, Westerink J, de Koning EJ, van der Graaf Y, Grobbee DE, Bots ML. Is the association between flow-mediated dilation and cardiovascular risk limited to low-risk populations?. J Am Coll Cardiol 2005, 45(12):1987-1993. 10.1016/j.jacc.2005.02.073, 15963397.
27. Ciftel M, Ertug H, Parlak M, Akcurin G, Kardelen F. Investigation of endothelial dysfunction and arterial stiffness in children with type 1 diabetes mellitus and the association with diastolic dysfunction. Diab Vasc Dis Res 2013, Epub ahead of print] doi:10.1177/1479164113508564.
28. Bruzzi P, Predieri B, Patianna VD, Salvini A, Rossi R, Modena MG, Iughetti L. Longitudinal evaluation of Endothelial Function in children and adolescents with Type 1 Diabetes Mellitus: a long term follow up study. Pediatr Int 2013, doi:10.1111/ped.12220. [Epub ahead of print.
29. Diagnosis and classification of diabetes mellitus. Diabetes Care 2010, 33(Suppl 1):S62-S69. 2797383, 20042775.