From Endothelial Dysfunction to Arterial Stiffness in Diabetes Mellitus

Author(s): Manuel Giraldo-Grueso*, Darío Echeverri.

Journal Name: Current Diabetes Reviews

Volume 16 , Issue 3 , 2020

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Abstract:

Prevalence of diabetes mellitus has increased drastically over time, especially in more populous countries such as the United States, India, and China. Patients with diabetes have an increased risk of major cardiovascular events such as acute myocardial infarction, cerebrovascular disease, and peripheral vascular disease. Arterial stiffness is a process related to aging and vascular, metabolic, cellular and physiological deterioration. In recent years, it has been described as an independent predictor of cardiovascular mortality and coronary artery disease. Additionally, it plays an important role in the measurement of chronic disease progression. Recent studies have suggested a strong relationship between diabetes mellitus and arterial stiffness since they share a similar pathophysiology involving endothelial dysfunction. The literature has shown that microvascular and macrovascular complications in diabetic patients could be screened and measured with arterial stiffness. Additionally, new evidence proposes that there is a relationship between blood glucose levels, microalbuminuria, and arterial stiffness. Moreover, arterial stiffness predicts cardiovascular risk and is independently associated with mortality in diabetic patients. Abnormal arterial stiffness values in diabetic patients should alert the clinician to the presence of vascular disease, which merits early study and treatment. We await more studies to determine if arterial stiffness could be considered a routine useful non-invasive tool in the evaluation of diabetic patients. There is enough evidence to conclude that arterial stiffness is related to the progression of diabetes mellitus.

Keywords: Diabetes mellitus, vascular stiffness, coronary heart disease, diabetic angiopathies, diabetic retinopathy, diabetic neuropathies.

[1]
Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and Its Burden in the United StatesAtlanta. GA: Centers for Disease Control and Prevention. US Dep Heal Hum Serv 2017; pp. 2009-19.
[2]
Li C, Balluz LS, Okoro CA, et al. Centers for Disease Control and Prevention (CDC). Surveillance of certain health behaviors and conditions among states and selected local areas --- Behavioral Risk Factor Surveillance System, United States, 2009. MMWR Surveill Summ 2011; 60(9): 1-250.
[PMID: 21849967]
[3]
Dieleman JL, Baral R, Birger M, et al. US spending on personal health care and public health, 1996-2013. JAMA 2016; 316(24): 2627-46.
[http://dx.doi.org/10.1001/jama.2016.16885] [PMID: 28027366]
[4]
Forouhi NG, Wareham NJ. Epidemiology of diabetes. Medicine (Abingdon) 2014; 42(12): 698-702.
[http://dx.doi.org/10.1016/j.mpmed.2014.09.007] [PMID: 25568613]
[5]
National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). Third report of the National Cholesterol Education Program (NCEP) expert panel on detection, Evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation 2002; 106(25): 3143-421.
[http://dx.doi.org/10.1161/circ.106.25.3143] [PMID: 12485966]
[6]
American Diabetes Association. The Staggering Costs of Diabetes in America 2013; 835.
[7]
Walker AM, Cubbon RM. Sudden cardiac death in patients with diabetes mellitus and chronic heart failure. Diab Vasc Dis Res 2015; 12(4): 228-33.
[http://dx.doi.org/10.1177/1479164115573225] [PMID: 25861812]
[8]
Schalkwijk CG, Stehouwer CD. Vascular complications in diabetes mellitus: the role of endothelial dysfunction. Clin Sci (Lond) 2005; 109(2): 143-59.
[http://dx.doi.org/10.1042/CS20050025] [PMID: 16033329]
[9]
Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 1993; 16(2): 434-44.
[http://dx.doi.org/10.2337/diacare.16.2.434] [PMID: 8432214]
[10]
Eckel RH, Wassef M, Chait A, et al. Prevention Conference VI: Diabetes and Cardiovascular Disease: Writing Group II: pathogenesis of atherosclerosis in diabetes. Circulation 2002; 105(18): e138-43.
[http://dx.doi.org/10.1161/01.CIR.0000013954.65303.C5] [PMID: 11994264]
[11]
Tabit CE, Chung WB, Hamburg NM, Vita JA. Endothelial dysfunction in diabetes mellitus: molecular mechanisms and clinical implications. Rev Endocr Metab Disord 2010; 11(1): 61-74.
[http://dx.doi.org/10.1007/s11154-010-9134-4] [PMID: 20186491]
[12]
Widlansky ME, Gokce N, Keaney JF Jr, Vita JA. The clinical implications of endothelial dysfunction. J Am Coll Cardiol 2003; 42(7): 1149-60.
[http://dx.doi.org/10.1016/S0735-1097(03)00994-X] [PMID: 14522472]
[13]
Silver AE, Vita JA. Shear-stress-mediated arterial remodeling in atherosclerosis: too much of a good thing? Circulation 2006; 113(24): 2787-9.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.634378] [PMID: 16785350]
[14]
Heil M, Schaper W. Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res 2004; 95(5): 449-58.
[http://dx.doi.org/10.1161/01.RES.0000141145.78900.44] [PMID: 15345667]
[15]
Caballero AE, Arora S, Saouaf R, et al. Microvascular and macrovascular reactivity is reduced in subjects at risk for type 2 diabetes. Diabetes 1999; 48(9): 1856-62.
[http://dx.doi.org/10.2337/diabetes.48.9.1856] [PMID: 10480619]
[16]
Tesauro M, Rizza S, Iantorno M, et al. Vascular, metabolic, and inflammatory abnormalities in normoglycemic offspring of patients with type 2 diabetes mellitus. Metabolism 2007; 56(3): 413-9.
[http://dx.doi.org/10.1016/j.metabol.2006.10.026] [PMID: 17292732]
[17]
Bucala R, Makita Z, Vega G, et al. Modification of low density lipoprotein by advanced glycation end products contributes to the dyslipidemia of diabetes and renal insufficiency. Proc Natl Acad Sci USA 1994; 91(20): 9441-5.
[http://dx.doi.org/10.1073/pnas.91.20.9441] [PMID: 7937786]
[18]
Stitt AW, Chakravarthy U, Archer DB, Gardiner TA. Increased endocytosis in retinal vascular endothelial cells grown in high glucose medium is modulated by inhibitors of nonenzymatic glycosylation. Diabetologia 1995; 38(11): 1271-5.
[http://dx.doi.org/10.1007/BF00401758] [PMID: 8582535]
[19]
Lee AT, Plump A, DeSimone C, Cerami A, Bucala R. A role for DNA mutations in diabetes-associated teratogenesis in transgenic embryos. Diabetes 1995; 44(1): 20-4.
[http://dx.doi.org/10.2337/diab.44.1.20] [PMID: 7813809]
[20]
Cohen E. La glicosilación no enzimática: una vía común en el diabetes y el envejecimiento. Med Cutan Ibero Lat Am 2011; 39(6): 243-6.
[21]
Dyck PJ, Hansen S, Karnes J, et al. Capillary number and percentage closed in human diabetic sural nerve. Proc Natl Acad Sci USA 1985; 82(8): 2513-7.
[http://dx.doi.org/10.1073/pnas.82.8.2513] [PMID: 3857597]
[22]
Li H, Cybulsky MI, Gimbrone MA Jr, Libby P. An atherogenic diet rapidly induces VCAM-1, a cytokine-regulatable mononuclear leukocyte adhesion molecule, in rabbit aortic endothelium. Arterioscler Thromb 1993; 13(2): 197-204.
[http://dx.doi.org/10.1161/01.ATV.13.2.197] [PMID: 7678986]
[23]
Calles-Escandon J, Cipolla M. Diabetes and endothelial dysfunction: a clinical perspective. Endocr Rev 2001; 22(1): 36-52.
[http://dx.doi.org/10.1210/edrv.22.1.0417] [PMID: 11159815]
[24]
Mäkimattila S, Virkamäki A, Groop PH, et al. Chronic hyperglycemia impairs endothelial function and insulin sensitivity via different mechanisms in insulin-dependent diabetes mellitus. Circulation 1996; 94(6): 1276-82.
[http://dx.doi.org/10.1161/01.CIR.94.6.1276] [PMID: 8822980]
[25]
Di Carli MF, Janisse J, Grunberger G, Ager J. Role of chronic hyperglycemia in the pathogenesis of coronary microvascular dysfunction in diabetes. J Am Coll Cardiol 2003; 41(8): 1387-93.
[http://dx.doi.org/10.1016/S0735-1097(03)00166-9] [PMID: 12706936]
[26]
Nitenberg A, Paycha F, Ledoux S, Sachs R, Attali JR, Valensi P. Coronary artery responses to physiological stimuli are improved by deferoxamine but not by L-arginine in non-insulin-dependent diabetic patients with angiographically normal coronary arteries and no other risk factors. Circulation 1998; 97(8): 736-43.
[http://dx.doi.org/10.1161/01.CIR.97.8.736] [PMID: 9498536]
[27]
Singh A, Boden G, Homko C, Gunawardana J, Rao AK. Whole-blood tissue factor procoagulant activity is elevated in type 1 diabetes: effects of hyperglycemia and hyperinsulinemia. Diabetes Care 2012; 35(6): 1322-7.
[http://dx.doi.org/10.2337/dc11-2114] [PMID: 22410811]
[28]
Friederich M, Hansell P, Palm F. Diabetes, oxidative stress, nitric oxide and mitochondria function. Curr Diabetes Rev 2009; 5(2): 120-44.
[http://dx.doi.org/10.2174/157339909788166800] [PMID: 19442097]
[29]
Gerrard JM, Stuart MJ, Rao GH, et al. Alteration in the balance of prostaglandin and thromboxane synthesis in diabetic rats. J Lab Clin Med 1980; 95(6): 950-8.
[PMID: 6445927]
[30]
Pistrosch F, Passauer J, Fischer S, Fuecker K, Hanefeld M, Gross P. In type 2 diabetes, rosiglitazone therapy for insulin resistance ameliorates endothelial dysfunction independent of glucose control. Diabetes Care 2004; 27(2): 484-90.
[http://dx.doi.org/10.2337/diacare.27.2.484] [PMID: 14747233]
[31]
Caballero AE, Saouaf R, Lim SC, et al. The effects of troglitazone, an insulin-sensitizing agent, on the endothelial function in early and late type 2 diabetes: a placebo-controlled randomized clinical trial. Metabolism 2003; 52(2): 173-80.
[http://dx.doi.org/10.1053/meta.2003.50023] [PMID: 12601628]
[32]
Mather KJ, Verma S, Anderson TJ. Improved endothelial function with metformin in type 2 diabetes mellitus. J Am Coll Cardiol 2001; 37(5): 1344-50.
[http://dx.doi.org/10.1016/S0735-1097(01)01129-9] [PMID: 11300445]
[33]
Turner RC. The U.K. Prospective Diabetes Study. A review. Diabetes Care 1998; 21(Suppl. 3): C35-8.
[http://dx.doi.org/10.2337/diacare.21.3.C35] [PMID: 9850487]
[34]
Moreno PR, Murcia AM, Palacios IF, et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation 2000; 102(18): 2180-4.
[http://dx.doi.org/10.1161/01.CIR.102.18.2180] [PMID: 11056089]
[35]
Virmani R, Burke AP, Kolodgie F. Morphological characteristics of coronary atherosclerosis in diabetes mellitus. Can J Cardiol 2006; 22(Suppl. B): 81B-4B.
[http://dx.doi.org/10.1016/S0828-282X(06)70991-6] [PMID: 16498517]
[36]
Laurent S, Cockcroft J, Van Bortel L, et al. European Network for Non-invasive Investigation of Large Arteries. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 2006; 27(21): 2588-605.
[http://dx.doi.org/10.1093/eurheartj/ehl254] [PMID: 17000623]
[37]
Prenner SB, Chirinos JA. Arterial stiffness in diabetes mellitus. Atherosclerosis 2015; 238(2): 370-9.
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.12.023] [PMID: 25558032]
[38]
Pereira T, Correia C, Cardoso J. Novel methods for pulse wave velocity measurement. J Med Biol Eng 2015; 35(5): 555-65.
[http://dx.doi.org/10.1007/s40846-015-0086-8] [PMID: 26500469]
[39]
AlGhatrif M, Strait JB, Morrell CH, et al. Longitudinal trajectories of arterial stiffness and the role of blood pressure: the Baltimore Longitudinal Study of Aging. Hypertension 2013; 62(5): 934-41.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.113.01445] [PMID: 24001897]
[40]
O’Rourke MF, Staessen JA, Vlachopoulos C, Duprez D, Plante GE. Clinical applications of arterial stiffness; definitions and reference values. Am J Hypertens 2002; 15(5): 426-44.
[http://dx.doi.org/10.1016/S0895-7061(01)02319-6] [PMID: 12022246]
[41]
Van Bortel LM, Laurent S, Boutouyrie P, et al. Artery society; European society of hypertension working group on vascular structure and function; European network for noninvasive investigation of large arteries. Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 2012; 30(3): 445-8.
[http://dx.doi.org/10.1097/HJH.0b013e32834fa8b0] [PMID: 22278144]
[42]
Safar ME, Blacher J, Jankowski P. Arterial stiffness, pulse pressure, and cardiovascular disease-is it possible to break the vicious circle? Atherosclerosis 2011; 218(2): 263-71.
[http://dx.doi.org/10.1016/j.atherosclerosis.2011.04.039] [PMID: 21621778]
[43]
Willum-Hansen T, Staessen JA, Torp-Pedersen C, et al. Prognostic value of aortic pulse wave velocity as index of arterial stiffness in the general population. Circulation 2006; 113(5): 664-70.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.579342] [PMID: 16461839]
[44]
Parati G, De Buyzere M. Evaluating aortic stiffness through an arm cuff oscillometric device: is validation against invasive measurements enough? J Hypertens 2010; 28(10): 2003-6.
[http://dx.doi.org/10.1097/HJH.0b013e32833f0e93] [PMID: 20844367]
[45]
Mitchell GF, Guo C-Y, Benjamin EJ, et al. Cross-sectional correlates of increased aortic stiffness in the community: the Framingham Heart Study. Circulation 2007; 115(20): 2628-36.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.667733] [PMID: 17485578]
[46]
Schram MT, Henry RMA, van Dijk RAJM, et al. Increased central artery stiffness in impaired glucose metabolism and type 2 diabetes: the Hoorn Study. Hypertension 2004; 43(2): 176-81.
[http://dx.doi.org/10.1161/01.HYP.0000111829.46090.92] [PMID: 14698999]
[47]
Shin JY, Lee HR, Lee DC. Increased arterial stiffness in healthy subjects with high-normal glucose levels and in subjects with pre-diabetes. Cardiovasc Diabetol 2011; 10(1): 30.
[http://dx.doi.org/10.1186/1475-2840-10-30] [PMID: 21492487]
[48]
Fang FS, Liu MY, Cheng XL, et al. Insulin resistance correlates with the arterial stiffness before glucose intolerance. Intern Med 2014; 53(3): 189-94.
[http://dx.doi.org/10.2169/internalmedicine.53.0690] [PMID: 24492686]
[49]
Chirinos JA, Segers P, Gillebert TC, et al. Asklepios Investigators. Central pulse pressure and its hemodynamic determinants in middle-aged adults with impaired fasting glucose and diabetes: the Asklepios study. Diabetes Care 2013; 36(8): 2359-65.
[http://dx.doi.org/10.2337/dc12-1463] [PMID: 23610081]
[50]
Sweitzer NK, Shenoy M, Stein JH, et al. Increases in central aortic impedance precede alterations in arterial stiffness measures in type 1 diabetes. Diabetes Care 2007; 30(11): 2886-91.
[http://dx.doi.org/10.2337/dc07-0191] [PMID: 17686834]
[51]
Gordin D, Rönnback M, Forsblom C, Heikkilä O, Saraheimo M, Groop P-H. Acute hyperglycaemia rapidly increases arterial stiffness in young patients with type 1 diabetes. Diabetologia 2007; 50(9): 1808-14.
[http://dx.doi.org/10.1007/s00125-007-0730-0] [PMID: 17611734]
[52]
Çiftel M, Ertuğ H, Parlak M, Akçurin 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 2014; 11(1): 19-25.
[http://dx.doi.org/10.1177/1479164113508564] [PMID: 24169808]
[53]
Kimoto E, Shoji T, Shinohara K, et al. Regional arterial stiffness in patients with type 2 diabetes and chronic kidney disease. J Am Soc Nephrol 2006; 17(8): 2245-52.
[http://dx.doi.org/10.1681/ASN.2005101038] [PMID: 16837632]
[54]
Taniwaki H, Kawagishi T, Emoto M, et al. Correlation between the intima-media thickness of the carotid artery and aortic pulse-wave velocity in patients with type 2 diabetes. Vessel wall properties in type 2 diabetes. Diabetes Care 1999; 22(11): 1851-7.
[http://dx.doi.org/10.2337/diacare.22.11.1851] [PMID: 10546019]
[55]
Cockcroft JR, Wilkinson IB, Evans M, et al. Pulse pressure predicts cardiovascular risk in patients with type 2 diabetes mellitus. Am J Hypertens 2005; 18(11): 1463-7-9.
[http://dx.doi.org/10.1016/j.amjhyper.2005.05.009]
[56]
Dinneen SF, Gerstein HC. The association of microalbuminuria and mortality in non-insulin-dependent diabetes mellitus. A systematic overview of the literature. Arch Intern Med 1997; 157(13): 1413-8.
[http://dx.doi.org/10.1001/archinte.1997.00440340025002] [PMID: 9224218]
[57]
Yokoyama H, Aoki T, Imahori M, Kuramitsu M. Subclinical atherosclerosis is increased in type 2 diabetic patients with microalbuminuria evaluated by intima-media thickness and pulse wave velocity. Kidney Int 2004; 66(1): 448-54.
[http://dx.doi.org/10.1111/j.1523-1755.2004.00752.x] [PMID: 15200455]
[58]
Smith A, Karalliedde J, De Angelis L, Goldsmith D, Viberti G. Aortic pulse wave velocity and albuminuria in patients with type 2 diabetes. J Am Soc Nephrol 2005; 16(4): 1069-75.
[http://dx.doi.org/10.1681/ASN.2004090769] [PMID: 15743996]
[59]
Kim WJ, Park C-Y, Park SE, et al. The association between regional arterial stiffness and diabetic retinopathy in type 2 diabetes. Atherosclerosis 2012; 225(1): 237-41.
[http://dx.doi.org/10.1016/j.atherosclerosis.2012.08.034] [PMID: 23017354]
[60]
Rema M, Mohan V, Deepa R, Ravikumar R. Chennai Urban Rural Epidemiology Study-2. Association of carotid intima-media thickness and arterial stiffness with diabetic retinopathy: the Chennai Urban Rural Epidemiology Study (CURES-2). Diabetes Care 2004; 27(8): 1962-7.
[http://dx.doi.org/10.2337/diacare.27.8.1962] [PMID: 15277424]
[61]
Meyer C, Milat F, McGrath BP, Cameron J, Kotsopoulos D, Teede HJ. Vascular dysfunction and autonomic neuropathy in Type 2 diabetes. Diabet Med 2004; 21(7): 746-51.
[http://dx.doi.org/10.1111/j.1464-5491.2004.01241.x] [PMID: 15209768]
[62]
Theilade S, Lajer M, Persson F, Joergensen C, Rossing P. Arterial stiffness is associated with cardiovascular, renal, retinal, and autonomic disease in type 1 diabetes. Diabetes Care 2013; 36(3): 715-21.
[http://dx.doi.org/10.2337/dc12-0850] [PMID: 23193205]


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VOLUME: 16
ISSUE: 3
Year: 2020
Page: [230 - 237]
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DOI: 10.2174/1573399814666181017120415
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