Abstract
Background: To examine the association of microalbuminuria (MAU) with the carotid intima-media thickness (CIMT) in Chinese Type 2 diabetic subjects. Materials and methods: Two hundred and thirty-nine patients (64±13 yr, 154 males) were divided into 2 groups: one with MAU (no.=119) or one without (no.=120). We recorded clinical and biochemical data as well as CIMT and ankle-brachial index (ABI). Results: The patients with MAU had had diabetes mellitus (DM) longer, had higher blood pressure (BP). They also had lower estimated glomerular filtration rate (eGFR) and higher levels of circulating glucose, glycated hemoglobin, high sensitivity C-reactive protein than those without. Lower mean ABI was found in those with MAU, however, they did not have higher mean CIMT (0.72±0.15 vs 0.71±0.16 mm, p=0.525). In patients without MAU, CIMT correlated with age, DM duration, systolic BP, eGFR, albumin-to-creatinine ratio, and ABI. However, in those with MAU, CIMT correlated only with age and eGFR. Multivariate regression analysis revealed that mean CIMT correlated only with age for patients without MAU, but correlated with age and body mass index for those with MAU. Dividing the patients into 5 age groups, we found that the older the patient, the higher the mean CIMT with no group differences between those with and without MAU in both genders. However, patients with eGFR below 60 ml/min/1.73 m2 had higher mean CIMT than those above (0.75±0.16 vs 0.69±0.14 mm, p=0.005). Conclusions: Type 2 diabetic patients with MAU were not associated with higher CIMT. Conversely, those with deterioration of renal function were more likely associated.
Similar content being viewed by others
References
Keen H, Jarrett RJ. The WHO multinational study of diabetes. Part 2. Macrovascular disease prevalence. Diabetes Care 1979, 2: 187–95.
Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE. Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 1997, 96: 1432–7.
Chambless LE, Heiss G, Folsom AR, et al. Association of coronary heart disease incidence with carotid arterial wall thickness and major risk factors: the Atherosclerosis Risk in Communities (ARIC) Study, 1987–1993. Am J Epidemiol 1997, 146: 483–94.
Lorenz MW, von Kegler S, Steinmetz H, Markus HS, Sitzer M. Carotid intima-media thickening indicates a higher vascular risk across a wide age range: prospective data from the Carotid Atherosclerosis Progression Study (CAPS). Stroke 2006, 37: 87–92.
Leinonen ES, Hiukka A, Hurt-Camejo E, et al. Low-grade inflammation, endothelial activation and carotid intima-media thickness in type 2 diabetes. J Intern Med 2004, 256: 119–27.
Kim CS, Kim HJ, Won YJ, et al. Normative values of carotid artery intima-media thickness in healthy Korean adults and estimation of macrovascular diseases relative risk using this data in type 2 diabetes patients. Diabetes Res Clin Pract 2006, 72: 183–9.
Temelkova-Kurktschiev TS, Koehler C, Leonhardt W, et al. Increased intimal-medial thickness in newly detected type 2 diabetes: risk factors. Diabetes Care 1999, 22: 333–8.
Bernard S, Serusclat A, Targe F, et al. Incremental predictive value of carotid ultrasonography in the assessment of coronary risk in a cohort of asymptomatic type 2 diabetic subjects. Diabetes Care 2005, 28: 1158–62.
van der Meer IM, Iglesias del Sol A, Hak AE, Bots ML, Hofman A, Witteman JC. Risk factors for progression of atherosclerosis measured at multiple sites in the arterial tree: the Rotterdam Study. Stroke 2003, 34: 2374–9.
Zandbergen AA, Vogt I, de Zeeuw D, et al. Change in albuminuria is predictive of cardiovascular outcome in normotensive patients with type 2 diabetes and microalbuminuria. Diabetes Care 2007, 30: 3119–21.
Schmiedel O, Schroeter ML, Harvey JN. Microalbuminuria in type 2 diabetes indicates impaired microvascular vasomotion and perfusion. Am J Physiol Heart Circ Physiol 2007, 293: H3424–31.
Hallan s, Astor B, Romundstad S, Aasarød K, Kvenild K, Coresh J. Association of kidney function and albuminuria With Cardiovascular Mortality in Older vs Younger Individuals: The HUNT II Study. Arch Intern Med 2007, 167: 2490–6.
Levey AS, Coresh J, Balk E, et al; National Kidney Foundation. National Kidney Foundation practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Ann Intern Med 2003, 139: 137–47.
Ouriel K, Zarins CK. Doppler ankle pressure: an evaluation of three methods of expression. Arch Surg 1982, 117: 1297–300.
McDermott MM, Liu K, Criqui MH, et al. Ankle-brachial index and subclinical cardiac and carotid disease: the multi-ethnic study of atherosclerosis. Am J Epidemiol 2005, 162: 33–41.
Newman AB, Sutton-Tyrrell K, Vogt MT, Kuller LH. Morbidity and mortality in hypertensive adults with a low ankle/arm blood pressure index. JAMA 1993, 270: 487–9.
Vogt MT, McKenna M, Anderson SJ, Wolfson SK, Kuller LH. The relationship between ankle-arm index and mortality in older men and women. J Am Geriatr Soc 1993, 41: 523–30.
Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 1999, 130: 461–70.
Touboul PJ, Hennerici MG, Meairs S, et al. Mannheim carotid intima-media thickness consensus (2004–2006). An update on behalf of the Advisory Board of the 3rd and 4th Watching the Risk Symposium, 13th and 15th European Stroke Conferences, Mannheim, Germany, 2004, and Brussels, Belgium, 2006. Cerebrovasc Dis 2007, 23: 75–80.
Matsagoura M, Andreadis E, Diamantopoulos EJ, Vassilopoulos C, Tentolouris N, Katsilambros N. Carotid intima-media thickness in patients with type 2 diabetes: the significance of microalbuminuria and different risk factors for atherosclerosis. Diabetes Care 2003, 26: 2966.
Nair BM. Viswanathan V, Snehalatha C, Mohan RS, Ramachandran A. Flow mediated dilatation and carotid intimal media thickness in South Indian type 2 diabetic subjects. Diabetes Res Clin Pract 2004, 65: 13–9.
Yilmaz MI, Saglam M, Qureshi AR, et al. Endothelial dysfunction in type-2 diabetics with early diabetic nephropathy is associated with low circulating adiponectin. Nephrol Dial Transplant 2008, 23: 1621–7.
Gall MA, Borch-Johnsen K, Hougaard P, Nielsen FS, Parving HH. Albuminuria and poor glycemic control predict mortality in NID-DM. Diabetes 1995, 44: 1303–9.
Mykkänen L, Zaccaro DJ, O’Leary DH, Howard G, Robbins DC, Haffner SM. Microalbuminuria and carotid artery intima-media thickness in nondiabetic and NIDDM subjects: the Insulin Resistance Atherosclerosis Study (IRAS). Stroke 1997, 28: 1710–6.
Jager A, van Hinsbergh VW, Kostense PJ, et al. C-reactive protein and soluble vascular cell adhesion molecule-1 are associated with elevated urinary albumin excretion but do not explain its link with cardiovascular risk. Arterioscler Thromb Vasc Biol 2002, 22: 593–8.
Navarro JF, Mora C, Maca M, Garca J. Inflammatory parameters are independently associated with urinary albumin in type 2 diabetes mellitus. Am J Kidney Dis 2003, 42: 53–61.
Fried LP, Kronmal RA, Newman AB, et al. Risk factors for 5-year mortality in older adults: the Cardiovascular Health Study. JAMA 1998, 279: 585–92.
Shlipak MG, Fried LF, Crump C, et al. Cardiovascular disease risk status in elderly persons with renal insufficiency. Kidney Int 2002, 62: 997–1004.
Manjunath G, Tighiouart H, Coresh J, et al. Level of kidney function as a risk factor for cardiovascular outcomes in the elderly. Kidney Int 2003, 63: 1121–9.
Kawamoto R, Ohtsuka N, Kusunoki T, Yorimitsu N. An association between the estimated glomerular filtration rate and carotid atherosclerosis. Intern Med 2008, 47: 391–8.
Kastarinen H, Ukkola O, Kesäniemi YA. Glomerular filtration rate is related to carotid intima-media thickness in middle-aged adults. Nephrol Dial Transplant 2009, 24: 2767–72.
Uusitupa M, Siitonen O, Aro A, Pyörälä K. Prevalence of coronary heart disease, left ventricular failure and hypertension in middle aged, newly diagnosed type 2 (non-insulin-dependent) diabetic subjects. Diabetologia 1985, 28: 22–7.
Mannami T, Konishi M, Baba S, Nishi N, Terao A. Prevalence of asymptomatic carotid atherosclerotic lesions detected by high-resolution ultrasonography and its relation to cardiovascular risk factors in the general population of a Japanese city: The Suita Study. Stroke 1997, 28: 518–25.
Lee AJ, Mowbray PI, Lowe GD, Rumley A, Fowkes FG, Allan PL. Blood viscosity and elevated carotid intima-media thickness in men and women: The Edirgh Artery Study. Circulation 1998, 97: 1467–73.
Bonithon-Kopp C, Touboul PJ, Berr C, et al. Relation of intima-media thickness to atherosclerotic plaques in carotid arteries: The Vascular Aging (EVA) Study. Arterioscler Thromb Vasc Biol 1996, 16: 310–6.
Salonen R, Tervahauta M, Salonen JT, Pekkanen J, Nissinen A, Karvonen MJ. Ultrasonographic manifestations of common carotid atherosclerosis in elderly eastern Finnish men: prevalence and associations with cardiovascular diseases and risk factors. Arterioscler Thromb 1994, 14: 1631–40.
Fabris F, Zanocchi M, Bo M, et al. Carotid plaque, aging, and risk factors: a study of 457 subjects. Stroke 1994, 25: 1133–40.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chu, CH., Lam, HC., Lee, JK. et al. Carotid intima-media thickness in Chinese Type 2 diabetic subjects with or without microalbuminuria. J Endocrinol Invest 35, 254–259 (2012). https://doi.org/10.3275/7756
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.3275/7756