Aortic Stiffness as a Surrogate Endpoint to Micro- and Macrovascular Complications in Patients with Type 2 Diabetes

Claudia R L Cardoso, Gil F Salles, Claudia R L Cardoso, Gil F Salles

Abstract

Increased aortic stiffness has been recognized as a predictor of adverse cardiovascular outcomes in some clinical conditions, such as in patients with arterial hypertension and end-stage renal disease, in population-based samples and, more recently, in type 2 diabetic patients. Patients with type 2 diabetes have higher aortic stiffness than non-diabetic individuals, and increased aortic stiffness has been correlated to the presence of micro- and macrovascular chronic diabetic complications. We aimed to review the current knowledge on the relationships between aortic stiffness and diabetic complications, their possible underlying physiopathological mechanisms, and their potential applications to clinical type 2 diabetes management.

Keywords: arterial stiffness; carotid-femoral pulse wave velocity; microvascular and macrovascular complications; type 2 diabetes.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Schematic representation of the potential physiopathological pathways involved in the relationships between increased aortic stiffness and micro- and macrovascular complications in diabetes.

References

    1. Laurent S., Boutouyrie P. Recent advances in arterial stiffness and wave reflection in human hypertension. Hypertension. 2007;49:1202–1206. doi: 10.1161/HYPERTENSIONAHA.106.076166.
    1. Cavalcante J.L., Lima J.A., Redheuil A., Al-Mallah M.H. Aortic stiffness: Current understanding and future directions. J. Am. Coll. Cardiol. 2011;57:1511–1522. doi: 10.1016/j.jacc.2010.12.017.
    1. Cecelja M., Chowienczyk P. Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: A systematic review. Hypertension. 2009;54:1328–1336. doi: 10.1161/HYPERTENSIONAHA.109.137653.
    1. Laurent S., Cockcroft J., van Bortel L., Boutouyrie P., Giannattasio C., Hayoz D., Pannier B., Vlachopoulos C., Wilkinson I., Struijker-Boudier H. Expert consensus document on arterial stiffness: Methodological issues and clinical applications. Eur. Heart J. 2006;27:2588–2605. doi: 10.1093/eurheartj/ehl254.
    1. Boutouyrie P., Fliser D., Goldsmith D., Covic A., Wiecek A., Ortiz A., Martinez-Castelao A., Lindholm B., Massy Z.A., Suleymanlar G., et al. Assessment of arterial stiffness for clinical and epidemiological studies: Methodological considerations for validation and entry into the European Renal and Cardiovascular Medicine registry. Nephrol. Dial. Transplant. 2014;29:232–239. doi: 10.1093/ndt/gft309.
    1. Laurent S., Boutouyrie P., Asmar R., Gautier I., Laloux B., Guize L., Ducimetiere P., Benetos A. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension. 2001;37:1236–1241. doi: 10.1161/01.HYP.37.5.1236.
    1. Mattace-Raso F.U., van der Cammen T.J., Hofman A., van Popele N.M., Bos M.L., Schalekamp M.A., Asmar R., Reneman R.S., Hoeks A.P., Breteler M.M., et al. Arterial stiffness and risk of coronary heart disease and stroke: The Rotterdam study. Circulation. 2006;113:657–663. doi: 10.1161/CIRCULATIONAHA.105.555235.
    1. Cardoso C.R., Ferreira M.T., Leite N.C., Salles G.F. Prognostic impact of aortic stiffness in high-risk type 2 diabetic patients: The Rio de Janeiro type 2 diabetes cohort study. Diabetes Care. 2013;36:3772–3778. doi: 10.2337/dc13-0506.
    1. Wijkman M., Länne T., Östgren C.J., Nystrom F.H. Aortic pulse wave velocity predicts incident cardiovascular events in patients with type 2 diabetes treated in primary care. J. Diabetes Complicat. 2016;30:1223–1228. doi: 10.1016/j.jdiacomp.2016.06.008.
    1. Ben-Shlomo Y., Spears M., Boustred C., May M., Anderson S.G., Benjamin E.J., Boutouyrie P., Cameron J., Chen C.H., Cruickshank J.K., et al. Aortic pulse wave velocity improves cardiovascular event prediction: An individual participant meta-analysis of prospective observational data from 17,635 subjects. J. Am. Coll. Cardiol. 2014;63:636–646. doi: 10.1016/j.jacc.2013.09.063.
    1. Munakata M. Brachial-ankle pulse wave velocity: Background, method, and clinical evidence. Pulse (Basel) 2016;3:195–204. doi: 10.1159/000443740.
    1. Miyoshi T., Ito H. Assessment of arterial stiffness using the cardio-ankle vascular index. Pulse (Basel) 2016;4:11–23. doi: 10.1159/000445214.
    1. Huybrechts S.A., Devos D.G., Vermeersch S.J., Mahieu D., Achten E., de Backer T.L., Segers P., van Bortel L.M. Carotid to femoral pulse wave velocity: A comparison of real travelled aortic path length determined by MRI and superficial measurements. J. Hypertens. 2011;29:1577–1582. doi: 10.1097/HJH.0b013e3283487841.
    1. Taniwaki H., Kawagishi T., Emoto M., Shoji T., Kanda H., Maekawa K., Nishizawa Y., Morii H. Correlation between the intima-media thickness of carotid artery and aortic pulse wave velocity in patients with type 2 diabetes. Vessel wall properties in type 2 diabetes. Diabetes Care. 1999;22:1851–1857. doi: 10.2337/diacare.22.11.1851.
    1. Kimoto E., Shoji T., Shinohara K., Inaba M., Okuno Y., Miki T., Koyama H., Emoto M., Nishizawa Y. Preferential stiffening of central over peripheral arteries in type 2 diabetes. Diabetes. 2003;52:448–452. doi: 10.2337/diabetes.52.2.448.
    1. De Angelis L., Millasseau S.C., Smith A., Viberti G., Jones R.H., Ritter J.M., Chowienczyk P.J. Sex differences in age-related stiffening of aorta in subjects with type 2 diabetes. Hypertension. 2004;44:67–71. doi: 10.1161/01.HYP.0000130482.81883.fd.
    1. Stehouwer C.D., Henry R.M., Ferreira I. Arterial stiffness in diabetes and the metabolic syndrome: A pathway to cardiovascular disease. Diabetologia. 2008;51:527–539. doi: 10.1007/s00125-007-0918-3.
    1. Ishimura E., Taniwaki H., Tsuchida T., Obatake N., Emoto M., Shoji T., Shioi A., Inaba M., Nishizawa Y. Urinary albumin excretion associated with arterial stiffness rather than thickness in type 2 diabetes. J. Nephrol. 2007;20:204–211.
    1. Rema M., Mohan V., Deepa R., Ravikumar R. Chennai urban rural epidemiology study-2. Association of carotid intima-thickness and arterial stiffness with diabetic retinopathy: The Chennai Urban Rural Epidemiology Study (CURES-2) Diabetes Care. 2004;27:1962–1967. doi: 10.2337/diacare.27.8.1962.
    1. Cardoso C.R., Ferreira M.T., Leite N.C., Barros P.N., Conte P.H., Salles G.F. Microvascular degenerative complications are associated with increased aortic stiffness in type 2 diabetic patients. Atherosclerosis. 2009;205:472–476. doi: 10.1016/j.atherosclerosis.2008.12.027.
    1. Kim E.S., Moon S.D., Kim H.S., Lim D.J., Cho J.H., Kwon H.S., Ahn C.W., Yoon K.H., Kang M.I., Cha B.Y., et al. Diabetic peripheral neuropathy is associated with increased arterial stiffness without changes in carotid intima-media thickness in type 2 diabetes. Diabetes Care. 2011;34:1403–1405. doi: 10.2337/dc10-2222.
    1. Ha B.K., Kim B.G., Kim D.H., Lee S.I., Jung S.M., Park J.Y., Lee C.W., Kim S.S., Kim B.H., Kim I.J. Relationships between brachial-ankle pulse wave velocity and peripheral neuropathy in type 2 diabetes. Diabetes Metab. J. 2012;36:443–451. doi: 10.4093/dmj.2012.36.6.443.
    1. Yokoyama H., Yokota Y., Tada J., Kanno S. Diabetic neuropathy is closely associated with arterial stiffening and thickness in type 2 diabetes. Diabet. Med. 2007;24:1329–1335. doi: 10.1111/j.1464-5491.2007.02278.x.
    1. Meyer C., Milat F., McGrath B.P., Cameron J., Kotsopoulos D., Teede H.J. Vascular dysfunction and autonomic neuropathy in Type 2 diabetes. Diabet. Med. 2004;21:746–751. doi: 10.1111/j.1464-5491.2004.01241.x.
    1. 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;36:715–721. doi: 10.2337/dc12-0850.
    1. Kim W.J., Park C.Y., Park S.E., Rhee E.J., Lee W.Y., Oh K.W., Park S.W., Kim S.W., Song S. The association between regional arterial stiffness and diabetic retinopathy in type 2 diabetes. Atherosclerosis. 2012;225:237–241. doi: 10.1016/j.atherosclerosis.2012.08.034.
    1. 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;16:1069–1075. doi: 10.1681/ASN.2004090769.
    1. Liu J.J., Tavintharan S., Yeoh L.Y., Sum C.F., Ng X.W., Pek S.L., Lee S.B., Tang W.E., Lim S.C., SMART2D Study High normal albuminuria is independently associated with aortic stiffness in patients with Type 2 diabetes. Diabet. Med. 2014;31:1199–1204. doi: 10.1111/dme.12461.
    1. 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;66:448–454. doi: 10.1111/j.1523-1755.2004.00752.x.
    1. Kim K.J., Lee B.W., Kim H.M., Shin J.Y., Kang E.S., Cha B.S., Lee E.J., Lim S.K., Lee H.C. Associations between cardio-ankle vascular index and microvascular complications in type 2 diabetes mellitus patients. J. Atheroscler. Thromb. 2011;18:328–336. doi: 10.5551/jat.5983.
    1. Aoun S., Blacher J., Safar M.E., Mourad J.J. Diabetes mellitus and renal failure: Effects on large artery stiffness. J. Hum. Hypertens. 2001;15:693–700. doi: 10.1038/sj.jhh.1001253.
    1. Sjöblom P., Nystrom F.H., Länne T., Engvall J., Östgren C.J. Microalbuminuria, but not reduced eGFR, is associated with cardiovascular subclinical organ damage in type 2 diabetes. Diabetes Metab. 2014;40:49–55. doi: 10.1016/j.diabet.2013.09.008.
    1. Bouchi R., Babazono T., Mugishima M., Yoshida N., Nyumura I., Toya K., Hanai K., Tanaka N., Ishii A., Uchigata Y., et al. Arterial stiffness is associated with incident albuminuria and decreased glomerular filtration rate in type 2 diabetic patients. Diabetes Care. 2011;34:2570–2575. doi: 10.2337/dc11-1020.
    1. Cardoso C.R., Moran C.B., Marinho F.S., Ferreira M.T., Salles G.F. Increased aortic stiffness predicts future development and progression of peripheral neuropathy in patients with type 2 diabetes: The Rio de Janeiro type 2 diabetes cohort study. Diabetologia. 2015;58:2161–2168. doi: 10.1007/s00125-015-3658-9.
    1. Boutouyrie P., Tropeano A.I., Asmar R., Gautier I., Benetos A., Lacolley P., Laurent S. Aortic stiffness is an independent predictor of primary coronary events in hypertensive patients: A longitudinal study. Hypertension. 2002;39:10–15. doi: 10.1161/hy0102.099031.
    1. Blacher J., Guerin A.P., Pannier B., Marchais S.J., Safar M.E., London G.M. Impact of aortic stiffness on survival in end-stage renal disease. Circulation. 1999;99:2434–2439. doi: 10.1161/01.CIR.99.18.2434.
    1. Sutton-Tyrrell K., Najjar S.S., Boudreau R.M., Venkitachalam L., Kupelian V., Simonsick E.M., Havlik R., Lakatta E.G., Spurgeon H., Kritchevsky S., et al. Elevated aortic pulse wave velocity, a marker of arterial stiffness, predicts cardiovascular events in well-functioning older adults. Circulation. 2005;111:3384–3390. doi: 10.1161/CIRCULATIONAHA.104.483628.
    1. Willum-Hansen T., Staessen J.A., Torp-Pedersen C., Rasmussen S., Thijs L., Ibsen H., Jeppesen J. Prognostic value of aortic pulse wave velocity as index of arterial stiffness in the general population. Circulation. 2006;113:664–670. doi: 10.1161/CIRCULATIONAHA.105.579342.
    1. Mitchell G.F., Hwang S.J., Vasan R.S., Larson M.G., Pencina M.J., Hamburg N.M., Vita J.A., Levy D., Benjamin E.J. Arterial stiffness and cardiovascular events: The Framingham heart study. Circulation. 2010;121:505–511. doi: 10.1161/CIRCULATIONAHA.109.886655.
    1. Vlachopoulos C., Aznaouridis K., Stefanadis C. Prediction of cardiovascular events and all-cause mortality with arterial stiffness: A systematic review and meta-analysis. J. Am. Coll. Cardiol. 2010;55:1318–1327. doi: 10.1016/j.jacc.2009.10.061.
    1. Cruickshank K., Riste L., Anderson S.G., Wright J.S., Dunn G., Gosling R.G. Aortic pulse wave velocity and its relationship to mortality in diabetes and glucose intolerance: An integrated index of vascular function? Circulation. 2002;106:2085–2090. doi: 10.1161/01.CIR.0000033824.02722.F7.
    1. Cardoso C.R., Salles G.F. Aortic stiffness: Is it time to be included into clinical diabetes management? J. Diabetes Complicat. 2016;30:1207–1208. doi: 10.1016/j.jdiacomp.2016.06.010.
    1. Van Bortel L.M., Laurent S., Boutouyrie P., Chowienczyk P., Cruickshank J.K., de Backer T., Filipovsky J., Huybrechts S., Mattace-Raso F.U., Protogerou A.D., et al. Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J. Hypertens. 2012;30:445–448. doi: 10.1097/HJH.0b013e32834fa8b0.
    1. The Reference Values for Arterial Stiffness’ Collaboration Determinants of pulse wave velocity in healthy people and in the presence of cardiovascular risk factors: ‘Establishing normal and reference values’. Eur. Heart J. 2010;31:2338–2350.
    1. Ferreira M.T., Leite N.C., Cardoso C.R., Salles G.F. Correlates of aortic stiffness progression in patients with type 2 diabetes: Importance of glycemic control: The Rio de Janeiro type 2 diabetes cohort study. Diabetes Care. 2015;38:897–904. doi: 10.2337/dc14-2791.
    1. Mancia G., Fagard R., Narkiewicz K., Redón J., Zanchetti A., Böhm M., Christiaens T., Cifkova R., de Backer G., Dominiczak A., et al. 2013 ESH/ESC Guidelines for the management of arterial hypertension: The Task Force for the management of arterial hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC) J. Hypertens. 2013;31:1281–1357. doi: 10.1097/.
    1. Kovacic J.C., Moreno P., Hachinski V., Nabel E.G., Fuster V. Cellular senescence, vascular disease, and aging: Part 1 of a 2-part review. Circulation. 2011;123:1650–1660. doi: 10.1161/CIRCULATIONAHA.110.007021.
    1. Kovacic J.C., Moreno P., Hachinski V., Nabel E.G., Fuster V. Cellular senescence, vascular disease, and aging: Part 2 of a 2-part review: Clinical vascular disease in the elderly. Circulation. 2011;123:1900–1910. doi: 10.1161/CIRCULATIONAHA.110.009118.
    1. Rask-Madsen C., Kahn C.R. Tissue-specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 2012;32:2052–2059. doi: 10.1161/ATVBAHA.111.241919.
    1. Avogaro A., de Kreutzenberg S.V., Federici M., Fadini G.P. The endothelium abridges insulin resistance to premature aging. J. Am. Heart Assoc. 2013;2:e000262. doi: 10.1161/JAHA.113.000262.
    1. Costantino S., Paneni F., Cosentino F. Ageing, metabolism and cardiovascular disease. J. Physiol. 2016;594:2061–2073. doi: 10.1113/JP270538.
    1. Rubin J., Nambi V., Chambless L.E., Steffes M.W., Juraschek S.P., Coresh J., Sharrett A.R., Selvin E. Hyperglycemia and arterial stiffness: The Atherosclerosis Risk in the Communities study. Atherosclerosis. 2012;225:246–251. doi: 10.1016/j.atherosclerosis.2012.09.003.
    1. Teoh W.L., Price J.F., Williamson R.M., Payne R.A., van Look L.A., Reynolds R.M., Frier B.M., Wilkinson I.B., Webb D.J., Strachan M.W., et al. Metabolic parameters associated with arterial stiffness in older adults with type 2 diabetes: The Edinburgh type 2 diabetes study. J. Hypertens. 2013;31:1010–1017. doi: 10.1097/HJH.0b013e32835f7ecf.
    1. Pfeifle B., Ditschuneit H. Effect of insulin on growth of cultured human arterial smooth muscle cells. Diabetologia. 1981;20:155–158. doi: 10.1007/BF00262020.
    1. Kass D.A., Shapiro E.P., Kawaguchi M., Capriotti A.R., Scuteri A., de Groof R.C., Lakatta E.G. Improved arterial compliance by a novel advanced glycation end-product crosslink breaker. Circulation. 2001;104:1464–1470. doi: 10.1161/hc3801.097806.
    1. Utescu M.S., Couture V., Mac-Way F., de Serres S.A., Marquis K., Larivière R., Desmeules S., Lebel M., Boutouyrie P., Agharazii M. Determinants of progression of aortic stiffness in hemodialysis patients: A prospective longitudinal study. Hypertension. 2013;62:154–160. doi: 10.1161/HYPERTENSIONAHA.113.01200.
    1. Lakatta E.G. Arterial and cardiac aging: Major shareholders in cardiovascular disease enterprises: Part III: Cellular and molecular clues to heart and arterial aging. Circulation. 2003;107:490–497. doi: 10.1161/01.CIR.0000048894.99865.02.
    1. Perret-Guillaume C., Joly L., Jankowski P., Benetos A. Benefits of the RAS blockade: Clinical evidence before the ONTARGET study. J. Hypertens. 2009;27:S3–S7. doi: 10.1097/01.hjh.0000354511.14086.f1.
    1. Williams B., Lacy P.S., Thom S.M., Cruickshank K., Stanton A., Collier D., Hughes A.D., Thurston H., O’Rourke M., CAFE Investigators et al. Differential impact of blood pressure-lowering drugs on central aortic pressure and clinical outcomes: Principal results of the conduit artery function evaluation (CAFE) study. Circulation. 2006;113:1213–1225. doi: 10.1161/CIRCULATIONAHA.106.640870.
    1. Mallareddy M., Parikh C.R., Peixoto A.J. Effect of angiotensin converting enzyme inhibitors on arterial stiffness in hypertension: Systematic review and meta-analysis. J. Clin. Hypertens. (Greenwich) 2006;8:398–403. doi: 10.1111/j.1076-7460.2006.05418.x.
    1. Sohn S.I., Kim C.J. Modulation of renin-angiotensin system and arterial stiffness: Evidence from clinical trials. Curr. Hypertens. Rev. 2014;10:37–40. doi: 10.2174/157340211001141111160311.
    1. Cooper M.E. Interaction of metabolic and haemodynamic factors in mediating experimental diabetic nephropathy. Diabetologia. 2001;44:1957–1972. doi: 10.1007/s001250100000.
    1. Sjølie A.K., Dodson P., Hobbs F.R. Does renin-angiotensin system blockade have a role in preventing diabetic retinopathy? A clinical review. Int. J. Clin. Pract. 2011;65:148–153. doi: 10.1111/j.1742-1241.2010.02552.x.
    1. Persson F., Lindhardt M., Rossing P., Parving H.H. Prevention of microalbuminuria using early intervention with renin-angiotensin system inhibitors in patients with type 2 diabetes: A systematic review. J. Renin Angiotensin Aldosterone Syst. 2016;17:3. doi: 10.1177/1470320316652047.
    1. Petersen K.S., Blanch N., Keogh J.B., Clifton P.M. Effect of weight loss on pulse wave velocity: Systematic review and meta-analysis. Arterioscler. Thromb. Vasc. Biol. 2015;35:243–252. doi: 10.1161/ATVBAHA.114.304798.
    1. Madden K.M., Lockhart C., Cuff D., Potter T.F., Meneilly G.S. Short-term aerobic exercise reduces arterial stiffness in older adults with type 2 diabetes, hypertension, and hypercholesterolemia. Diabetes Care. 2009;32:1531–1535. doi: 10.2337/dc09-0149.
    1. Yokoyama H., Emoto M., Fujiwara S., Motoyama K., Morioka T., Koyama H., Shoji T., Inaba M., Nishizawa Y. Short-term aerobic exercise improves arterial stiffness in type 2 diabetes. Diabetes Res. Clin. Pract. 2004;65:85–93. doi: 10.1016/j.diabres.2003.12.005.
    1. Loimaala A., Groundstroem K., Rinne M., Nenonen A., Huhtala H., Parkkari J., Vuori I. Effect of long-term endurance and strength training on metabolic control and arterial elasticity in patients with type 2 diabetes mellitus. Am. J. Cardiol. 2009;103:972–977. doi: 10.1016/j.amjcard.2008.12.026.
    1. Way K.L., Keating S.E., Baker M.K., Chuter V.H., Johnson N.A. The effect of exercise on vascular function and stiffness in type 2 diabetes: A systematic review and meta-analysis. Curr. Diabetes Rev. 2016;12:369–383. doi: 10.2174/1573399811666150817124601.
    1. Hiukka A., Westerbacka J., Leinonen E.S., Watanabe H., Wiklund O., Hulten L.M., Salonen J.T., Tuomainen T.P., Yki-Järvinen H., Keech A.C., et al. Long-term effects of fenofibrate on carotid intima-media thickness and augmentation index in subjects with type 2 diabetes mellitus. J. Am. Coll. Cardiol. 2008;52:2190–2197. doi: 10.1016/j.jacc.2008.09.049.
    1. Mills C.E., Govoni V., Faconti L., Morant S., Casagrande M.L., Maskell P., Masani A., Crickmore H., Iqbal F., Webb A.J., et al. Reducing arterial stiffness independently of blood pressure: Proof or concept? The randomized, factorial ‘VASERA’ trial. J. Hypertens. 2016;34(Suppl. 2):e112. doi: 10.1097/01.hjh.0000491627.59731.0f.
    1. Tahara N., Yamagishi S.I., Bekki M., Kodama N., Nakamura T., Sugiyama Y., Oshige T., Kumashiro Y., Honda A., Tahara A., et al. Anagliptin, a dipeptidyl peptidase-4 inhibitor, ameliorates arterial stiffness in association with reduction of remnant-like particle cholesterol and alanine transaminase levels in type 2 diabetic patients. Curr. Vasc. Pharmacol. 2016;14:552–562. doi: 10.2174/1570161114666160625090212.
    1. Guerin A.P., Blacher J., Pannier B., Marchais S.J., Safar M.E., London G.M. Impact of aortic stiffness attenuation on survival of patients in end-stage renal failure. Circulation. 2001;103:987–992. doi: 10.1161/01.CIR.103.7.987.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться