Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Review Article

Arterial Stiffness and Type 1 Diabetes: The Current State of Knowledge

Author(s): Michal Kulecki*, Aleksandra Uruska, Dariusz Naskret and Dorota Zozulinska-Ziolkiewicz

Volume 18, Issue 3, 2022

Published on: 14 June, 2021

Article ID: e140621194054 Pages: 11

DOI: 10.2174/1573399817666210614113827

Price: $65

conference banner
Abstract

The most common cause of mortality among people with type 1 diabetes is cardiovascular diseases. Arterial stiffness allows predicting cardiovascular complications, cardiovascular mortality, and all-cause mortality. There are different ways to measure arterial stiffness; the gold standard is pulse wave velocity. Arterial stiffness is increased in people with type 1 diabetes compared to healthy controls. It increases with age and duration of type 1 diabetes. Arterial stiffness among people with type 1 diabetes positively correlates with systolic blood pressure, obesity, glycated hemoglobin, waist circumference, and waist to hip ratio. It has a negative correlation with the estimated glomerular filtration rate, high-density lipoprotein, and the absence of carotid plaques. The increased arterial stiffness could result from insulin resistance, collagen increase due to inadequate enzymatic glycation, and endothelial and autonomic dysfunction. The insulin-induced decrease in arterial stiffness is impaired in type 1 diabetes. There are not enough proofs to use pharmacotherapy in the prevention of arterial stiffness, but some of the medicaments got promising results in single studies, for example, renin-angiotensin-aldosterone system inhibitors, statins, and SGLT2 inhibitors. The main strategy of prevention of arterial stiffness progression remains glycemic control and a healthy lifestyle.

Keywords: Arterial stiffness, type 1 diabetes, pulse wave velocity, diabetic complications, cardiovascular diseases, cardiovascular risk.

[1]
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]
[2]
Mitchell GF, Hwang S-J, Vasan RS, et al. Arterial stiffness and cardiovascular events: The Framingham Heart Study. Circulation 2010; 121(4): 505-11.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.886655] [PMID: 20083680]
[3]
Theilade S, Lajer M, Jorsal A, Tarnow L, Parving H-H, Rossing P. Arterial stiffness and endothelial dysfunction independently and synergistically predict cardiovascular and renal outcome in patients with type 1 diabetes. Diabet Med 2012; 29(8): 990-4.
[http://dx.doi.org/10.1111/j.1464-5491.2012.03633.x] [PMID: 22414297]
[4]
Tougaard NH, Theilade S, Winther SA, et al. Carotid-femoral pulse wave velocity as a risk marker for development of complications in type 1 diabetes mellitus. J Am Heart Assoc 2020; 9(19): e017165.
[http://dx.doi.org/10.1161/JAHA.120.017165] [PMID: 32955366]
[5]
Tynjälä A, Forsblom C, Harjutsalo V, Groop P-H, Gordin D. Finndiane study group. Arterial stiffness predicts mortality in individuals with type 1 diabetes. Diabetes Care 2020; 43(9): 2266-2271.
[http://dx.doi.org/10.2337/dc20-0078] [PMID: 32647049]
[6]
Shirwany NA, Zou MH. Arterial stiffness: A brief review. Acta Pharmacol Sin 2010; 31(10): 1267-76.
[http://dx.doi.org/10.1038/aps.2010.123] [PMID: 20802505]
[7]
Lyle AN, Raaz U. Killing me un-softly: causes and mechanisms of arterial stiffness recent highlights of atvb: early career committee contribution. Arterioscler Thromb Vasc Biol 2017; 37(2): e1–e11.
[http://dx.doi.org/10.1161/ATVBAHA.116.308563] [PMID: 28122777]
[8]
Lurbe E, Agabiti-Rosei E, Cruickshank JK, et al. 2016 European Society of Hypertension guidelines for the management of high blood pressure in children and adolescents. J Hypertens 2016; 34(10): 1887-920.
[http://dx.doi.org/10.1097/HJH.0000000000001039] [PMID: 27467768]
[9]
Mameli C, Mazzantini S, Ben Nasr M, Fiorina P, Scaramuzza AE, Zuccotti GV. Explaining the increased mortality in type 1 diabetes. World J Diabetes 2015; 6(7): 889-95.
[http://dx.doi.org/10.4239/wjd.v6.i7.889] [PMID: 26185597]
[10]
Bebu I, Braffett BH, Orchard TJ, Lorenzi GM, Lachin JM. Mediation of the effect of glycemia on the risk of CVD outcomes in type 1 diabetes: the dcct/edic study. Diabetes Care 2019; 42(7): 1284-9.
[http://dx.doi.org/10.2337/dc18-1613] [PMID: 30894365]
[11]
Winston GJ, Palmas W, Lima J, et al. Pulse pressure and subclinical cardiovascular disease in the multi-ethnic study of atherosclerosis. Am J Hypertens 2013; 26(5): 636-42.
[http://dx.doi.org/10.1093/ajh/hps092] [PMID: 23388832]
[12]
Thijssen DHJ, Black MA, Pyke KE, et al. Assessment of flow-mediated dilation in humans: A methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2011; 300(1): H2-H12.
[http://dx.doi.org/10.1152/ajpheart.00471.2010] [PMID: 20952670]
[13]
Wang X, Keith JC Jr, Struthers AD, Feuerstein GZ. Assessment of arterial stiffness, a translational medicine biomarker system for evaluation of vascular risk. Cardiovasc Ther 2008; 26(3): 214-23.
[http://dx.doi.org/10.1111/j.1755-5922.2008.00051.x] [PMID: 18786091]
[14]
Oliver JJ, Webb DJ. Noninvasive assessment of arterial stiffness and risk of atherosclerotic events. Arterioscler Thromb Vasc Biol 2003; 23(4): 554-66.
[http://dx.doi.org/10.1161/01.ATV.0000060460.52916.D6] [PMID: 12615661]
[15]
Laurent S, Cockcroft J, Van Bortel L, et al. 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]
[16]
Yasmin , Brown MJ. Similarities and differences between augmentation index and pulse wave velocity in the assessment of arterial stiffness. QJM 1999; 92(10): 595-600.
[http://dx.doi.org/10.1093/qjmed/92.10.595] [PMID: 10627881]
[17]
Laugesen E, Hansen KW, Knudsen ST, Erlandsen M, Ebbehøj E, Poulsen PL. Reproducibility of the ambulatory arterial stiffness index in patients with type 1 diabetes mellitus. Blood Press Monit 2010; 15(1): 18-22.
[http://dx.doi.org/10.1097/MBP.0b013e32833531f9] [PMID: 20038836]
[18]
Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ. The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 2000; 525(Pt 1): 263-70.
[http://dx.doi.org/10.1111/j.1469-7793.2000.t01-1-00263.x] [PMID: 10811742]
[19]
Dolan E, Thijs L, Li Y, et al. Ambulatory arterial stiffness index as a predictor of cardiovascular mortality in the Dublin Outcome Study. Hypertension 2006; 47(3): 365-70.
[http://dx.doi.org/10.1161/01.HYP.0000200699.74641.c5] [PMID: 16432047]
[20]
Nürnberger J, Keflioglu-Scheiber A, Opazo Saez AM, Wenzel RR, Philipp T, Schäfers RF. Augmentation index is associated with cardiovascular risk. J Hypertens 2002; 20(12): 2407-14.
[http://dx.doi.org/10.1097/00004872-200212000-00020] [PMID: 12473865]
[21]
Pini R, Cavallini MC, Palmieri V, et al. Central but not brachial blood pressure predicts cardiovascular events in an unselected geriatric population: the ICARe Dicomano Study. J Am Coll Cardiol 2008; 51(25): 2432-9.
[http://dx.doi.org/10.1016/j.jacc.2008.03.031] [PMID: 18565402]
[22]
Roman MJ, Devereux RB, Kizer JR, et al. High central pulse pressure is independently associated with adverse cardiovascular outcome the strong heart study. J Am Coll Cardiol 2009; 54(18): 1730-4.
[http://dx.doi.org/10.1016/j.jacc.2009.05.070] [PMID: 19850215]
[23]
Benetos A. Pulse pressure and arterial stiffness in type 1 diabetic patients. J Hypertens 2003; 21(11): 2005-7.
[http://dx.doi.org/10.1097/00004872-200311000-00005] [PMID: 14597839]
[24]
Gordin D, Groop P-H. Aspects of hyperglycemia contribution to arterial stiffness and cardiovascular complications in patients with type 1 diabetes. J Diabetes Sci Technol 2016; 10(5): 1059-64.
[http://dx.doi.org/10.1177/1932296816636894] [PMID: 26956240]
[25]
Cameron JD, Cruickshank JK. Glucose, insulin, diabetes and mechanisms of arterial dysfunction. Clin Exp Pharmacol Physiol 2007; 34(7): 677-82.
[http://dx.doi.org/10.1111/j.1440-1681.2007.04659.x] [PMID: 17581229]
[26]
Schram MT, Chaturvedi N, Fuller JH, Stehouwer CD. Pulse pressure is associated with age and cardiovascular disease in type 1 diabetes: The Eurodiab Prospective Complications Study. J Hypertens 2003; 21(11): 2035-44.
[http://dx.doi.org/10.1097/00004872-200311000-00012] [PMID: 14597846]
[27]
Guo J, Muldoon MF, Brooks MM, Orchard TJ, Costacou T. Prognostic significance of pulse pressure and other blood pressure components for coronary artery disease in type 1 diabetes. Am J Hypertens 2019; 32(11): 1075-81.
[http://dx.doi.org/10.1093/ajh/hpz099] [PMID: 31214692]
[28]
Williams B, Mancia G, Spiering W, et al. 2018 ESC/ESH Guidelines for the management of arterial hypertension. Eur Heart J 2018; 39(33): 3021-104.
[http://dx.doi.org/10.1093/eurheartj/ehy339] [PMID: 30165516]
[29]
Llauradó G, Cano A, Albert L, et al. Arterial stiffness is highly correlated with the scores obtained from the Steno Type 1 Risk Engine in subjects with T1DM. PLoS One 2019; 14(9): e0220206.
[http://dx.doi.org/10.1371/journal.pone.0220206] [PMID: 31483791]
[30]
Urbina E M, Wadwa R P, Davis C, et al. Prevalence of increased arterial stiffness in children with type 1 diabetes mellitus differs by measurement site and sex: The search for Diabetes in Youth Study. J Pediatr 2010; 156(5): 731-7.
[http://dx.doi.org/10.1016/j.jpeds.2009.11.011]
[31]
Dabelea D, Stafford JM, Mayer-Davis EJ, et al. Association of type 1 diabetes vs type 2 diabetes diagnosed during childhood and adolescence with complications during teenage years and young adulthood. JAMA 2017; 317(8): 825-35.
[http://dx.doi.org/10.1001/jama.2017.0686] [PMID: 28245334]
[32]
Galler A, Heitmann A, Siekmeyer W, et al. Increased arterial stiffness in children and adolescents with type 1 diabetes: No association between arterial stiffness and serum levels of adiponectin. Pediatr Diabetes 2010; 11(1): 38-46.
[http://dx.doi.org/10.1111/j.1399-5448.2009.00525.x] [PMID: 19496970]
[33]
Cherney DZI, Montanari A. Gender, clamped hyperglycemia and arterial stiffness in patients with uncomplicated type 1 diabetes mellitus. Clin Exp Hypertens 2014; 36(3): 187-93.
[http://dx.doi.org/10.3109/10641963.2013.804543] [PMID: 24164216]
[34]
Ljunggren P, Maahs DM, Johansson P, et al. Reduced brachial artery distensibility in patients with type 1 diabetes. J Diabetes Complications 2016; 30(5): 893-7.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.03.004] [PMID: 27056753]
[35]
Haller MJ, Samyn M, Nichols WW, et al. Radial artery tonometry demonstrates arterial stiffness in children with type 1 diabetes. Diabetes Care 2004; 27(12): 2911-7.
[http://dx.doi.org/10.2337/diacare.27.12.2911] [PMID: 15562206]
[36]
Dost A, Molz E, Krebs A, et al. Pulse pressure in children and adolescents with type 1 diabetes mellitus in Germany and Austria. Pediatr Diabetes 2014; 15(3): 236-43.
[http://dx.doi.org/10.1111/pedi.12083] [PMID: 25705749]
[37]
Palombo C, Kozakova M, Morizzo C, et al. Circulating endothelial progenitor cells and large artery structure and function in young subjects with uncomplicated type 1 diabetes. Cardiovasc Diabetol 2011; 10: 88.
[http://dx.doi.org/10.1186/1475-2840-10-88] [PMID: 21981808]
[38]
Wadwa RP, Urbina EM, Anderson AM, et al. Measures of arterial stiffness in youth with type 1 and type 2 diabetes: The SEARCH for diabetes in youth study. Diabetes Care 2010; 33(4): 881-6.
[http://dx.doi.org/10.2337/dc09-0747] [PMID: 20067960]
[39]
Rönnback M, Fagerudd J, Forsblom C, Pettersson-Fernholm K, Reunanen A, Groop P-H. Altered age-related blood pressure pattern in type 1 diabetes. Circulation 2004; 110(9): 1076-82.
[http://dx.doi.org/10.1161/01.CIR.0000139903.29522.8D] [PMID: 15326070]
[40]
Vastagh I, Horváth T, Nagy G, et al. Evolution and predictors of morphological and functional arterial changes in the course of type 1 diabetes mellitus. Diabetes Metab Res Rev 2010; 26(8): 646-55.
[http://dx.doi.org/10.1002/dmrr.1133] [PMID: 20922819]
[41]
Cherney DZI, Sochett EB. Evolution of renal hyperfiltration and arterial stiffness from adolescence into early adulthood in type 1 diabetes. Diabetes Care 2011; 34(8): 1821-6.
[http://dx.doi.org/10.2337/dc11-0167] [PMID: 21636797]
[42]
Lim SC, Tan CS. Comment on: Cherney and Sochett. Evolution of renal hyperfiltration and arterial stiffness from adolescence into early adulthood in type 1 diabetes. Diabetes Care 2011;34:1821-1826. Diabetes Care 2011; 34(12): e182.
[http://dx.doi.org/10.2337/dc11-1528] [PMID: 22110174]
[43]
Ahlgren AR, Astrand H, Sundkvist G, Länne T. Increased aortic stiffness is persistent in type 1 diabetic women: A follow-up study. Diabetologia 2005; 48(4): 780-3.
[http://dx.doi.org/10.1007/s00125-005-1685-7] [PMID: 15747108]
[44]
Adeva-Andany MM, Funcasta-Calderón R, Fernández-Fernández C, Ameneiros-Rodríguez E, Domínguez-Montero A. Subclinical vascular disease in patients with diabetes is associated with insulin resistance. Diabetes Metab Syndr 2019; 13(3): 2198-206.
[http://dx.doi.org/10.1016/j.dsx.2019.05.025] [PMID: 31235157]
[45]
George B, Bantwal G, Ayyar V, Mathew V. Occurrence of increased arterial stiffness in a cohort of adult patients with type 1 diabetes mellitus when compared to normoglycemic controls. J Diabetes Sci Technol 2015; 9(1): 138-44.
[http://dx.doi.org/10.1177/1932296814551982] [PMID: 25231115]
[46]
Bjornstad P, Nguyen N, Reinick C, et al. Association of apolipoprotein B, LDL-C and vascular stiffness in adolescents with type 1 diabetes. Acta Diabetol 2015; 52(3): 611-9.
[http://dx.doi.org/10.1007/s00592-014-0693-9] [PMID: 25539881]
[47]
Obermannova B, Petruzelkova L, Sulakova T, Sumnik Z. HbA1c but not diabetes duration predicts increased arterial stiffness in adolescents with poorly controlled type 1 diabetes. Pediatr Diabetes 2017; 18(4): 304-10.
[http://dx.doi.org/10.1111/pedi.12385] [PMID: 27075550]
[48]
Terlemez S, Bulut Y, Ünüvar T, Tokgöz Y, Eryilmaz U, Çelik B. Evaluation of arterial stiffness in children with type 1 diabetes using the oscillometric method. J Diabetes Complications 2016; 30(5): 864-7.
[http://dx.doi.org/10.1016/j.jdiacomp.2016.03.012] [PMID: 27068268]
[49]
Pietrzak I, Fendler W, Dróżdż I, Mianowska B, Młynarski W, Szadkowska A. Arterial stiffness, bmi, dipping status and ace d/i polymorphism in type 1 diabetic children. Exp Clin Endocrinol Diabetes 2016; 124(5): 283-7.
[http://dx.doi.org/10.1055/s-0042-101243] [PMID: 27050070]
[50]
Urbina EM, Isom S, Bell RA, et al. Burden of cardiovascular risk factors over time and arterial stiffness in youth with type 1 diabetes mellitus: the search for diabetes in youth study. J Am Heart Assoc 2019; 8(13): e010150.
[http://dx.doi.org/10.1161/JAHA.118.010150] [PMID: 31213111]
[51]
van Elderen SGC, Westenberg JJM, Brandts A, et al. Increased aortic stiffness measured by MRI in patients with type 1 diabetes mellitus and relationship to renal function. AJR Am J Roentgenol 2011; 196(3): 697-701.
[http://dx.doi.org/10.2214/AJR.10.4898] [PMID: 21343516]
[52]
Vallée A, Yannoutsos A, Temmar M, et al. Determinants of the aortic pulse wave velocity index in hypertensive and diabetic patients: Predictive and therapeutic implications. J Hypertens 2018; 36(12): 2324-32.
[http://dx.doi.org/10.1097/HJH.0000000000001828] [PMID: 29995699]
[53]
Suláková T, Janda J, Cerná J, Janštová V, Feber J. Assessment of arterial stiffness from ambulatory blood pressure monitoring in children with diabetes mellitus type-1 (DMT1). J Hum Hypertens 2012; 26(6): 357-64.
[http://dx.doi.org/10.1038/jhh.2011.38] [PMID: 21544085]
[54]
Llauradó G, Amigó N, Cano A, et al. Specific Nuclear Magnetic Resonance Lipoprotein Subclass Profiles and Central Arterial Stiffness in Type 1 Diabetes Mellitus: A Case Control Study. J Clin Med 2019; 8(11): E1875.
[http://dx.doi.org/10.3390/jcm8111875] [PMID: 31694246]
[55]
Gourgari E, Stafford JM, D’Agostino R Jr, et al. The association of low-density lipoprotein cholesterol with elevated arterial stiffness in adolescents and young adults with type 1 and type 2 diabetes: The search for diabetes in youth study. Pediatr Diabetes 2020; 21(5): 863-70.
[http://dx.doi.org/10.1111/pedi.13021] [PMID: 32304144]
[56]
Tryfonopoulos D, Anastasiou E, Protogerou A, et al. Arterial stiffness in type 1 diabetes mellitus is aggravated by autoimmune thyroid disease. J Endocrinol Invest 2005; 28(7): 616-22.
[http://dx.doi.org/10.1007/BF03347260] [PMID: 16218044]
[57]
Shah AS, Dabelea D, Talton JW, et al. Smoking and arterial stiffness in youth with type 1 diabetes: The SEARCH Cardiovascular Disease Study. J Pediatr 2014; 165(1): 110-6.
[http://dx.doi.org/10.1016/j.jpeds.2014.02.024] [PMID: 24681182]
[58]
Inman M, Daneman D, Curtis J, et al. Social determinants of health are associated with modifiable risk factors for cardiovascular disease and vascular function in pediatric type 1 diabetes. J Pediatr 2016; 177: 167-72.
[http://dx.doi.org/10.1016/j.jpeds.2016.06.049] [PMID: 27476636]
[59]
Lithovius R, Gordin D, Forsblom C, Saraheimo M, Harjutsalo V, Groop P-H. Ambulatory blood pressure and arterial stiffness in individuals with type 1 diabetes. Diabetologia 2018; 61(9): 1935-45.
[http://dx.doi.org/10.1007/s00125-018-4648-5] [PMID: 29797021]
[60]
McCulloch MA, Mauras N, Canas JA, et al. Magnetic resonance imaging measures of decreased aortic strain and distensibility are proportionate to insulin resistance in adolescents with type 1 diabetes mellitus. Pediatr Diabetes 2015; 16(2): 90-7.
[http://dx.doi.org/10.1111/pedi.12241] [PMID: 25524487]
[61]
Shah AS, Black S, Wadwa RP, et al. Insulin sensitivity and arterial stiffness in youth with type 1 diabetes: The SEARCH CVD study. J Diabetes Complications 2015; 29(4): 512-6.
[http://dx.doi.org/10.1016/j.jdiacomp.2015.02.004] [PMID: 25736026]
[62]
Atabek ME, Kurtoglu S, Pirgon O, Baykara M. Arterial wall thickening and stiffening in children and adolescents with type 1 diabetes. Diabetes Res Clin Pract 2006; 74(1): 33-40.
[http://dx.doi.org/10.1016/j.diabres.2006.03.004] [PMID: 16621108]
[63]
Oxlund H, Rasmussen LM, Andreassen TT, Heickendorff L. Increased aortic stiffness in patients with type 1 (insulin-dependent) diabetes mellitus. Diabetologia 1989; 32(10): 748-52.
[http://dx.doi.org/10.1007/BF00274536] [PMID: 2591642]
[64]
Buckner T, Shao B, Eckel RH, Heinecke JW, Bornfeldt KE, Snell-Bergeon J. Association of apolipoprotein C3 with insulin resistance and coronary artery calcium in patients with type 1 diabetes. J Clin Lipidol 2021; 15(1): 235-42.
[http://dx.doi.org/10.1016/j.jacl.2020.10.006] [PMID: 33257283]
[65]
Bjarnegård N, Arnqvist HJ, Lindström T, Jonasson L, Jönsson A, Länne T. Long-term hyperglycaemia impairs vascular smooth muscle cell function in women with type 1 diabetes mellitus. Diab Vasc Dis Res 2009; 6(1): 25-31.
[http://dx.doi.org/10.3132/dvdr.2009.005] [PMID: 19156625]
[66]
Prince CT, Secrest AM, Mackey RH, Arena VC, Kingsley LA, Orchard TJ. Cardiovascular autonomic neuropathy, HDL cholesterol, and smoking correlate with arterial stiffness markers determined 18 years later in type 1 diabetes. Diabetes Care 2010; 33(3): 652-7.
[http://dx.doi.org/10.2337/dc09-1936] [PMID: 20040653]
[67]
Llauradó G, Megia A, Cano A, et al. FGF-23/Vitamin D axis in type 1 diabetes: the potential role of mineral metabolism in arterial stiffness. PLoS One 2015; 10(10): e0140222.
[http://dx.doi.org/10.1371/journal.pone.0140222] [PMID: 26462160]
[68]
Lieberman R, Wadwa RP, Nguyen N, et al. The association between vitamin D and vascular stiffness in adolescents with and without type 1 diabetes. PLoS One 2013; 8(10): e77272.
[http://dx.doi.org/10.1371/journal.pone.0077272] [PMID: 24204786]
[69]
Liuzzo G, Biasucci LM, Trotta G, et al. Unusual CD4+CD28null T lymphocytes and recurrence of acute coronary events. J Am Coll Cardiol 2007; 50(15): 1450-8.
[http://dx.doi.org/10.1016/j.jacc.2007.06.040] [PMID: 17919564]
[70]
El-Samahy MH, Tantawy AAG, Adly AAM, et al. Expression of CD4+ CD28null T lymphocytes in children and adolescents with type 1 diabetes mellitus: Relation to microvascular complications, aortic elastic properties, and carotid intima media thickness. Pediatr Diabetes 2017; 18(8): 785-93.
[http://dx.doi.org/10.1111/pedi.12484] [PMID: 28102614]
[71]
Belmadani S, Zerfaoui M, Boulares HA, Palen DI, Matrougui K. Microvessel vascular smooth muscle cells contribute to collagen type I deposition through ERK1/2 MAP kinase, alphavbeta3-integrin, and TGF-beta1 in response to ANG II and high glucose. Am J Physiol Heart Circ Physiol 2008; 295(1): H69-76.
[http://dx.doi.org/10.1152/ajpheart.00341.2008] [PMID: 18456735]
[72]
Vishwanath V, Frank KE, Elmets CA, Dauchot PJ, Monnier VM. Glycation of skin collagen in type I diabetes mellitus. Correlation with long-term complications. Diabetes 1986; 35(8): 916-21.
[http://dx.doi.org/10.2337/diab.35.8.916] [PMID: 3732633]
[73]
Tong J, Yang F, Li X, Xu X, Wang GX. Mechanical Characterization and Material Modeling of Diabetic Aortas in a Rabbit Model. Ann Biomed Eng 2018; 46(3): 429-42.
[http://dx.doi.org/10.1007/s10439-017-1955-9] [PMID: 29124551]
[74]
Kahlberg N, Qin CX, Anthonisz J, et al. Adverse vascular remodelling is more sensitive than endothelial dysfunction to hyperglycaemia in diabetic rat mesenteric arteries. Pharmacol Res 2016; 111: 325-35.
[http://dx.doi.org/10.1016/j.phrs.2016.06.025] [PMID: 27363948]
[75]
Akhtar R, Cruickshank JK, Zhao X, et al. Localized micro- and nano-scale remodelling in the diabetic aorta. Acta Biomater 2014; 10(11): 4843-51.
[http://dx.doi.org/10.1016/j.actbio.2014.07.001] [PMID: 25014552]
[76]
Salum E, Butlin M, Kals J, et al. Angiotensin II receptor blocker telmisartan attenuates aortic stiffening and remodelling in STZ-diabetic rats. Diabetol Metab Syndr 2014; 6: 57.
[http://dx.doi.org/10.1186/1758-5996-6-57] [PMID: 24920962]
[77]
Stabouli S, Kotsis V, Maliachova O, et al. Matrix metalloproteinase -2, -9 and arterial stiffness in children and adolescents: The role of chronic kidney disease, diabetes, and hypertension. Int J Cardiol Hypertens 2020; 4: 100025.
[http://dx.doi.org/10.1016/j.ijchy.2020.100025] [PMID: 33447754]
[78]
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]
[79]
Cherney DZI, Reich HN, Miller JA, et al. Age is a determinant of acute hemodynamic responses to hyperglycemia and angiotensin II in humans with uncomplicated type 1 diabetes mellitus. Am J Physiol Regul Integr Comp Physiol 2010; 299(1): R206-14.
[http://dx.doi.org/10.1152/ajpregu.00027.2010] [PMID: 20410477]
[80]
Meehan CS, Kethireddy PL, Ashcraft JK, Shuster JJ, Haller MJ. Premeal insulin decreases arterial stiffness in children with type 1 diabetes. Pediatr Diabetes 2017; 18(4): 311-4.
[http://dx.doi.org/10.1111/pedi.12389] [PMID: 27174580]
[81]
Rogowicz-Frontczak A, Araszkiewicz A, Pilacinski S, Zozulinska-Ziolkiewicz D, Wykretowicz A, Wierusz-Wysocka B. Carotid intima-media thickness and arterial stiffness in type 1 diabetic patients with and without microangiopathy. Arch Med Sci 2012; 8(3): 484-90.
[http://dx.doi.org/10.5114/aoms.2012.29526] [PMID: 22852004]
[82]
Tjessem IH, Al-Far HFM, Fuglsang J, Lauszus FF. Microvascular disease during pregnancy in type 1 diabetes is associated with ambulatory arterial stiffness. Pregnancy Hypertens 2018; 12: 150-4.
[http://dx.doi.org/10.1016/j.preghy.2017.11.011] [PMID: 29199016]
[83]
Lauszus FF, Fuglsang J, Rosgaard A, Lousen T, Klebe JG. Ambulatory arterial stiffness index in type 1 diabetes mellitus: any different during pregnancy? Eur J Obstet Gynecol Reprod Biol 2013; 169(2): 234-8.
[http://dx.doi.org/10.1016/j.ejogrb.2013.04.010] [PMID: 23726250]
[84]
Lovshin JA, Lytvyn Y, Lovblom LE, et al. Retinopathy and raas activation: results from the canadian study of longevity in type 1 diabetes. Diabetes Care 2019; 42(2): 273-80.
[http://dx.doi.org/10.2337/dc18-1809] [PMID: 30523033]
[85]
Gordin D, Wadén J, Forsblom C, et al. Arterial stiffness and vascular complications in patients with type 1 diabetes: The Finnish Diabetic Nephropathy (FinnDiane) Study. Ann Med 2012; 44(2): 196-204.
[http://dx.doi.org/10.3109/07853890.2010.530681] [PMID: 21047152]
[86]
Lambert J, Smulders RA, Aarsen M, Donker AJ, Stehouwer CD. Carotid artery stiffness is increased in microalbuminuric IDDM patients. Diabetes Care 1998; 21(1): 99-103.
[http://dx.doi.org/10.2337/diacare.21.1.99] [PMID: 9538978]
[87]
Gordin D, Wadén J, Forsblom C, et al. Pulse pressure predicts incident cardiovascular disease but not diabetic nephropathy in patients with type 1 diabetes (The FinnDiane Study). Diabetes Care 2011; 34(4): 886-91.
[http://dx.doi.org/10.2337/dc10-2013] [PMID: 21330642]
[88]
Laugesen E, Hansen KW, Knudsen ST, et al. Increased ambulatory arterial stiffness index and pulse pressure in microalbuminuric patients with type 1 diabetes. Am J Hypertens 2009; 22(5): 513-9.
[http://dx.doi.org/10.1038/ajh.2009.27] [PMID: 19247265]
[89]
Szczyrba S, Kozera GM, Neubauer-Geryk J, Wolnik B, Nyka WM, Bieniaszewski L. Diabetic symmetric polyneuropathy is associated with increased aortal stiffening but not cerebral angiopathy in type 1 diabetes. J Diabetes Complications 2015; 29(1): 73-6.
[http://dx.doi.org/10.1016/j.jdiacomp.2014.10.002] [PMID: 25456818]
[90]
van Ittersum FJ, Schram MT, van der Heijden-Spek JJ, et al. Autonomic nervous function, arterial stiffness and blood pressure in patients with Type I diabetes mellitus and normal urinary albumin excretion. J Hum Hypertens 2004; 18(11): 761-8.
[http://dx.doi.org/10.1038/sj.jhh.1001751] [PMID: 15175635]
[91]
Ahlgren AR, Sundkvist G, Wollmer P, Sonesson B, Länne T. Increased aortic stiffness in women with type 1 diabetes mellitus is associated with diabetes duration and autonomic nerve function. Diabet Med 1999; 16(4): 291-7.
[http://dx.doi.org/10.1046/j.1464-5491.1999.00079.x] [PMID: 10220202]
[92]
Secrest AM, Marshall SL, Miller RG, Prince CT, Orchard TJ. Pulse wave analysis and cardiac autonomic neuropathy in type 1 diabetes: A report from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Technol Ther 2011; 13(12): 1264-8.
[http://dx.doi.org/10.1089/dia.2011.0126] [PMID: 21819228]
[93]
Liatis S, Alexiadou K, Tsiakou A, Makrilakis K, Katsilambros N, Tentolouris N. Cardiac autonomic function correlates with arterial stiffness in the early stage of type 1 diabetes. Exp Diabetes Res 2011; 2011: 957901.
[http://dx.doi.org/10.1155/2011/957901] [PMID: 21804819]
[94]
Matteucci E, Consani C, Masoni MC, Giampietro O. Circadian blood pressure variability in type 1 diabetes subjects and their nondiabetic siblings - influence of erythrocyte electron transfer. Cardiovasc Diabetol 2010; 9: 61.
[http://dx.doi.org/10.1186/1475-2840-9-61] [PMID: 20920366]
[95]
van Elderen SGC, Brandts A, Westenberg JJM, et al. Aortic stiffness is associated with cardiac function and cerebral small vessel disease in patients with type 1 diabetes mellitus: assessment by magnetic resonance imaging. Eur Radiol 2010; 20(5): 1132-8.
[http://dx.doi.org/10.1007/s00330-009-1655-4] [PMID: 19915847]
[96]
Wilkinson IB, MacCallum H, Rooijmans DF, et al. Increased augmentation index and systolic stress in type 1 diabetes mellitus. QJM 2000; 93(7): 441-8.
[http://dx.doi.org/10.1093/qjmed/93.7.441] [PMID: 10874053]
[97]
Ahlgren AR, Sundkvist G, Sandgren T, Länne T. Female gender increases stiffness of elastic but not of muscular arteries in type I diabetic patients. Clin Physiol Funct Imaging 2002; 22(6): 409-15.
[http://dx.doi.org/10.1046/j.1475-097X.2002.00451.x] [PMID: 12464146]
[98]
van Elderen SGC, Brandts A, van der Grond J, et al. Cerebral perfusion and aortic stiffness are independent predictors of white matter brain atrophy in type 1 diabetic patients assessed with magnetic resonance imaging. Diabetes Care 2011; 34(2): 459-63.
[http://dx.doi.org/10.2337/dc10-1446] [PMID: 21216862]
[99]
Tjeerdema N, Van Schinkel LD, Westenberg JJ, et al. Aortic stiffness is associated with white matter integrity in patients with type 1 diabetes. Eur Radiol 2014; 24(9): 2031-7.
[http://dx.doi.org/10.1007/s00330-014-3179-9] [PMID: 24828536]
[100]
Theilade S, Rossing P, Jensen JS, Jensen MT. Arterial-ventricular coupling in type 1 diabetes: arterial stiffness is associated with impaired global longitudinal strain in type 1 diabetes patients-the Thousand & 1 Study. Acta Diabetol 2018; 55(1): 21-9.
[http://dx.doi.org/10.1007/s00592-017-1062-2] [PMID: 29038853]
[101]
Diabetes Control and Complications Trial (DCCT)/Epidemiology of Diabetes Interventions and Complications (EDIC) Study Research Group. Intensive diabetes treatment and cardiovascular outcomes in type 1 diabetes: the dcct/edic study 30-year follow-up. Diabetes Care 2016; 39(5): 686-93.
[http://dx.doi.org/10.2337/dc15-1990] [PMID: 26861924]
[102]
Writing Group for the DCCT/EDIC Research Group. Coprogression of cardiovascular risk factors in type 1 diabetes during 30 years of follow-up in the dcct/edic study. Diabetes Care 2016; 39(9): 1621-30.
[http://dx.doi.org/10.2337/dc16-0502] [PMID: 27436274]
[103]
Jensen-Urstad KJ, Reichard PG, Rosfors JS, Lindblad LE, Jensen-Urstad MT. Early atherosclerosis is retarded by improved long-term blood glucose control in patients with IDDM. Diabetes 1996; 45(9): 1253-8.
[http://dx.doi.org/10.2337/diab.45.9.1253] [PMID: 8772731]
[104]
Pulkkinen M-A, Tuomaala A-K, Hero M, Gordin D, Sarkola T. Motivational Interview to improve vascular health in Adolescents with poorly controlled type 1 Diabetes (MIAD): A randomized controlled trial. BMJ Open Diabetes Res Care 2020; 8(1): e001216.
[http://dx.doi.org/10.1136/bmjdrc-2020-001216] [PMID: 32723754]
[105]
Bjornstad P, Pyle L, Nguyen N, et al. Achieving International Society for Pediatric and Adolescent Diabetes and American Diabetes Association clinical guidelines offers cardiorenal protection for youth with type 1 diabetes. Pediatr Diabetes 2015; 16(1): 22-30.
[http://dx.doi.org/10.1111/pedi.12252] [PMID: 25604668]
[106]
Petersen KS, Clifton PM, Lister N, Keogh JB. Effect of Improving Dietary Quality on Arterial Stiffness in Subjects with Type 1 and Type 2 Diabetes: A 12 Months Randomised Controlled Trial. Nutrients 2016; 8(6): E382.
[http://dx.doi.org/10.3390/nu8060382] [PMID: 27338467]
[107]
Jaacks LM, Crandell J, Liese AD, et al. No association of dietary fiber intake with inflammation or arterial stiffness in youth with type 1 diabetes. J Diabetes Complications 2014; 28(3): 305-10.
[http://dx.doi.org/10.1016/j.jdiacomp.2014.01.005] [PMID: 24613131]
[108]
Lamichhane AP, Liese AD, Urbina EM, et al. Associations of dietary intake patterns identified using reduced rank regression with markers of arterial stiffness among youth with type 1 diabetes. Eur J Clin Nutr 2014; 68(12): 1327-33.
[http://dx.doi.org/10.1038/ejcn.2014.96] [PMID: 24865480]
[109]
The NS, Couch SC, Urbina EM, et al. Body Mass index z-score modifies the association between added sugar intake and arterial stiffness in youth with type 1 diabetes: the search nutrition ancillary study. Nutrients 2019; 11(8): E1752.
[http://dx.doi.org/10.3390/nu11081752] [PMID: 31366063]
[110]
Petersen KS, Keogh JB, Meikle PJ, Garg ML, Clifton PM. Dietary predictors of arterial stiffness in a cohort with type 1 and type 2 diabetes. Atherosclerosis 2015; 238(2): 175-81.
[http://dx.doi.org/10.1016/j.atherosclerosis.2014.12.012] [PMID: 25528424]
[111]
Moloney MA, Casey RG, O’Donnell DH, Fitzgerald P, Thompson C, Bouchier-Hayes DJ. Two weeks taurine supplementation reverses endothelial dysfunction in young male type 1 diabetics. Diab Vasc Dis Res 2010; 7(4): 300-10.
[http://dx.doi.org/10.1177/1479164110375971] [PMID: 20667936]
[112]
Marshall ZA, Mackintosh KA, Lewis MJ, Ellins EA, McNarry MA. Association of physical activity metrics with indicators of cardiovascular function and control in children with and without type 1 diabetes. Pediatr Diabetes 2020.
[PMID: 33215796]
[113]
Rosenlund S, Theilade S, Hansen TW, Andersen S, Rossing P. Treatment with continuous subcutaneous insulin infusion is associated with lower arterial stiffness. Acta Diabetol 2014; 51(6): 955-62.
[http://dx.doi.org/10.1007/s00592-014-0619-6] [PMID: 25274393]
[114]
Heier M, Stensæth KH, Brunborg C, et al. Increased arterial stiffness in childhood onset diabetes: a cardiovascular magnetic resonance study. Eur Heart J Cardiovasc Imaging 2018; 19(6): 694-700.
[http://dx.doi.org/10.1093/ehjci/jex178] [PMID: 28950341]
[115]
Castro-Correia C, Moura C, Mota C, et al. Arterial stiffness in children and adolescents with and without continuous insulin infusion. J Pediatr Endocrinol Metab 2019; 32(8): 837-41.
[http://dx.doi.org/10.1515/jpem-2019-0102] [PMID: 31228861]
[116]
Westerbacka J, Uosukainen A, Mäkimattila S, Schlenzka A, Yki-Järvinen H. Insulin-induced decrease in large artery stiffness is impaired in uncomplicated type 1 diabetes mellitus. Hypertension 2000; 35(5): 1043-8.
[http://dx.doi.org/10.1161/01.HYP.35.5.1043] [PMID: 10818062]
[117]
Westerbacka J, Yki-Järvinen H. Arterial stiffness and insulin resistance. Semin Vasc Med 2002; 2(2): 157-64.
[http://dx.doi.org/10.1055/s-2002-32039] [PMID: 16222607]
[118]
Wilhelm B, Weber MM, Kreisselmeier HP, et al. Endothelial function and arterial stiffness in uncomplicated type 1 diabetes and healthy controls and the impact of insulin on these parameters during an euglycemic clamp. J Diabetes Sci Technol 2007; 1(4): 582-9.
[http://dx.doi.org/10.1177/193229680700100417] [PMID: 19885122]
[119]
Gourgari E, Dabelea D, Rother K. Modifiable Risk Factors for Cardiovascular Disease in Children with Type 1 Diabetes: Can Early Intervention Prevent Future Cardiovascular Events? Curr Diab Rep 2017; 17(12): 134.
[http://dx.doi.org/10.1007/s11892-017-0968-y] [PMID: 29101482]
[120]
Gourgari E, Stafford JM, D’Agostino R Jr, et al. Association of metformin and statin medications with surrogate measures of cardiovascular disease in youth with type 1 diabetes: The search for diabetes in youth study. Ann Pediatr Endocrinol Metab 2019; 24(3): 187-94.
[http://dx.doi.org/10.6065/apem.2019.24.3.187] [PMID: 31607112]
[121]
Lytvyn Y, Har R, Locke A, et al. Renal and Vascular Effects of Uric Acid Lowering in Normouricemic Patients With Uncomplicated Type 1 Diabetes. Diabetes 2017; 66(7): 1939-49.
[http://dx.doi.org/10.2337/db17-0168] [PMID: 28408434]
[122]
Manolis AJ, Iraklianou S, Pittaras A, et al. Arterial compliance changes in diabetic normotensive patients after angiotensin-converting enzyme inhibition therapy. Am J Hypertens 2005; 18(1): 18-22.
[http://dx.doi.org/10.1016/j.amjhyper.2004.08.014] [PMID: 15691612]
[123]
Haller MJ, Stein JM, Shuster JJ, et al. Pediatric Atorvastatin in Diabetes Trial (PADIT): A pilot study to determine the effect of atorvastatin on arterial stiffness and endothelial function in children with type 1 diabetes mellitus. J Pediatr Endocrinol Metab 2009; 22(1): 65-8.
[http://dx.doi.org/10.1515/JPEM.2009.22.1.65] [PMID: 19344076]
[124]
Savić V, Eržen B, Janić M, et al. Improvement of arterial wall characteristics by the low-dose fluvastatin and valsartan combination in type 1 diabetes mellitus patients. Diab Vasc Dis Res 2013; 10(5): 420-5.
[http://dx.doi.org/10.1177/1479164113485102] [PMID: 23811602]
[125]
Cherney DZI, Lai V, Scholey JW, Miller JA, Zinman B, Reich HN. Effect of direct renin inhibition on renal hemodynamic function, arterial stiffness, and endothelial function in humans with uncomplicated type 1 diabetes: A pilot study. Diabetes Care 2010; 33(2): 361-5.
[http://dx.doi.org/10.2337/dc09-1303] [PMID: 19889802]
[126]
Cherney DZ, Perkins BA, Soleymanlou N, et al. The effect of empagliflozin on arterial stiffness and heart rate variability in subjects with uncomplicated type 1 diabetes mellitus. Cardiovasc Diabetol 2014; 13: 28.
[http://dx.doi.org/10.1186/1475-2840-13-28] [PMID: 24475922]
[127]
Rodbard HW, Giaccari A, Cariou B, et al. Effect of sotagliflozin as an adjunct to insulin therapy on blood pressure and arterial stiffness in adults with type 1 diabetes: A post hoc pooled analysis of inTandem1 and inTandem2. Diab Vasc Dis Res 2021; 18(1): 1479164121995928.
[http://dx.doi.org/10.1177/1479164121995928] [PMID: 33611925]
[128]
Gordin D, Bernardi L, Rosengård-Bärlund M, et al. Oxygen deteriorates arterial function in type 1 diabetes. Acta Diabetol 2016; 53(3): 349-57.
[http://dx.doi.org/10.1007/s00592-015-0775-3] [PMID: 26159114]
[129]
Stadler M, Theuer E, Anderwald C, et al. Persistent arterial stiffness and endothelial dysfunction following successful pancreas-kidney transplantation in Type 1 diabetes. Diabet Med 2009; 26(10): 1010-8.
[http://dx.doi.org/10.1111/j.1464-5491.2009.02817.x] [PMID: 19900233]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy