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Published in: Cardiovascular Diabetology 1/2015

Open Access 01-12-2015 | Original investigation

Type 2 diabetes-associated carotid plaque burden is increased in patients with retinopathy compared to those without retinopathy

Authors: Núria Alonso, Alicia Traveset, Esther Rubinat, Emilio Ortega, Nuria Alcubierre, Jordi Sanahuja, Marta Hernández, Angels Betriu, Carmen Jurjo, Elvira Fernández, Didac Mauricio

Published in: Cardiovascular Diabetology | Issue 1/2015

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Abstract

Background

Cardiovascular disease (CVD) is the leading cause of mortality among subjects with type 2 diabetes (T2D), and diabetic retinopathy (DR) has been associated with an increased risk for CVD. The present study was designed to test the concept that T2D patients with DR, but without previous cardiovascular (CV) events and with normal renal function, have an increased atherosclerotic burden compared with patients without DR.

Methods

A cross-sectional study was performed using patients with normal renal function (estimated glomerular filtration rate (eGFR) >60 ml/min) and without previous CV events. A total of 312 patients (men, 51%; mean age, 57 yrs; age range 40–75 yrs) were included in the study; 153 (49%) of the patients had DR. B-mode carotid ultrasound imaging was performed for all of the study subjects to measure the carotid intima-media thickness (cIMT) and carotid plaques in the common carotid artery (CCA), bifurcation and internal carotid artery (ICA).

Results

The percentage of carotid plaques in T2D patients with DR was higher than in T2D patients without DR (68% vs. 52.2%, p = 0.0045), and patients with DR had a higher prevalence of ≥2 carotid plaques (44.4% vs. 21.4%; p < 0.0001). No differences were observed in the cIMT measured at different carotid regions between the patients with or without DR. Using multivariate logistic regression (adjustment for major risk factors for atherosclerosis), DR was independently associated with mean-internal cIMT (p = 0.0176), with the presence of carotid plaques (p = 0.0366) and with carotid plaque burden (≥2 plaques; p < 0.0001).

Conclusions

The present study shows that DR in T2D patients without CVD and with normal renal function is associated with a higher atherosclerotic burden (presence and number of plaques) in the carotid arteries. These patients may be at a higher risk for future CV events; therefore, an ultrasound examination of the carotid arteries should be considered in patients with DR for more careful and individualised CV assessment and follow-up.
Literature
1.
go back to reference Papa G, Degano C, Iurato MP, Licciardello C, Maiorana R, Finocchiaro C. Macrovascular complication phenotypes in type 2 diabetic patients. Cardiovasc Diabetol. 2013;12:20.CrossRefPubMedPubMedCentral Papa G, Degano C, Iurato MP, Licciardello C, Maiorana R, Finocchiaro C. Macrovascular complication phenotypes in type 2 diabetic patients. Cardiovasc Diabetol. 2013;12:20.CrossRefPubMedPubMedCentral
2.
go back to reference Kramer CK, Rodrigues TC, Canani LH, Gross JL. Diabetic retinopathy predicts all-cause mortality and cardiovascular events in both type 1 and 2 diabetes: meta-analysis of observational studies. Diabetes Care. 2011;34:1238–44.CrossRefPubMedPubMedCentral Kramer CK, Rodrigues TC, Canani LH, Gross JL. Diabetic retinopathy predicts all-cause mortality and cardiovascular events in both type 1 and 2 diabetes: meta-analysis of observational studies. Diabetes Care. 2011;34:1238–44.CrossRefPubMedPubMedCentral
3.
go back to reference Cheung N, Wang JJ, Klein R, Couper DJ, Sharrett AR, Wong TY. Diabetic retinopathy and the risk of coronary heart disease: the Atherosclerosis Risk in Communities Study. Diabetes Care. 2007;30:1742–6.CrossRefPubMed Cheung N, Wang JJ, Klein R, Couper DJ, Sharrett AR, Wong TY. Diabetic retinopathy and the risk of coronary heart disease: the Atherosclerosis Risk in Communities Study. Diabetes Care. 2007;30:1742–6.CrossRefPubMed
4.
go back to reference Avogaro A, Giorda C, Maggini M, Mannucci E, Raschetti R, Lombardo F, et al. Diabetes and Informatics Study Group, Association of Clinical Diabetologists, Istituto Superiore di Sanità: Incidence of coronary heart disease in type 2 diabetic men and women: impact of microvascular complications, treatment, and geographic location. Diabetes Care. 2007;30:1241–7.CrossRefPubMed Avogaro A, Giorda C, Maggini M, Mannucci E, Raschetti R, Lombardo F, et al. Diabetes and Informatics Study Group, Association of Clinical Diabetologists, Istituto Superiore di Sanità: Incidence of coronary heart disease in type 2 diabetic men and women: impact of microvascular complications, treatment, and geographic location. Diabetes Care. 2007;30:1241–7.CrossRefPubMed
5.
go back to reference Cheung N, Rogers S, Couper DJ, Klein R, Sharrett AR, Wong TY. Is diabetic retinopathy an independent risk factor for ischemic stroke? Stroke. 2007;38:398–401.CrossRefPubMed Cheung N, Rogers S, Couper DJ, Klein R, Sharrett AR, Wong TY. Is diabetic retinopathy an independent risk factor for ischemic stroke? Stroke. 2007;38:398–401.CrossRefPubMed
7.
go back to reference Veerman KJ, Venegas-Pino DE, Shi Y, Khan MI, Gerstein HC, Werstuck GH. Hyperglycaemia is associated with impaired vasa vasorum neovascularization and accelerated atherosclerosis in apolipoprotein-E deficient mice. Atherosclerosis. 2013;227:250–8.CrossRefPubMed Veerman KJ, Venegas-Pino DE, Shi Y, Khan MI, Gerstein HC, Werstuck GH. Hyperglycaemia is associated with impaired vasa vasorum neovascularization and accelerated atherosclerosis in apolipoprotein-E deficient mice. Atherosclerosis. 2013;227:250–8.CrossRefPubMed
9.
go back to reference Arcidiacono MV, Traveset A, Rubinat E, Ortega E, Betriu A, Hernández M, et al. Microangiopathy of large artery wall: a neglected complication of diabetes mellitus. Atherosclerosis. 2013;228:142–7.CrossRefPubMed Arcidiacono MV, Traveset A, Rubinat E, Ortega E, Betriu A, Hernández M, et al. Microangiopathy of large artery wall: a neglected complication of diabetes mellitus. Atherosclerosis. 2013;228:142–7.CrossRefPubMed
10.
go back to reference Sampson UK, Harrell FE Jr, Fazio S, Nwosu S, Mercaldo N, Mensah GA, et al. Carotid adventitial Vasa vasorum and Intima-media thickness in a primary prevention population. Echocardiography. 2014. doi:10.1111/echo.12646. Sampson UK, Harrell FE Jr, Fazio S, Nwosu S, Mercaldo N, Mensah GA, et al. Carotid adventitial Vasa vasorum and Intima-media thickness in a primary prevention population. Echocardiography. 2014. doi:10.1111/echo.12646.
11.
go back to reference Negi SI, Nambi V. The role of carotid intimal thickness and plaque imaging in risk stratification for coronary heart disease. Curr Atheroscler Rep. 2012;14:115–23.CrossRefPubMed Negi SI, Nambi V. The role of carotid intimal thickness and plaque imaging in risk stratification for coronary heart disease. Curr Atheroscler Rep. 2012;14:115–23.CrossRefPubMed
12.
go back to reference Wannarong T, Parraga G, Buchanan D, Fenster A, House AA, Hackam DG, et al. Progression of carotid plaque volume predicts cardiovascular events. Stroke. 2013;44:1859–65.CrossRefPubMed Wannarong T, Parraga G, Buchanan D, Fenster A, House AA, Hackam DG, et al. Progression of carotid plaque volume predicts cardiovascular events. Stroke. 2013;44:1859–65.CrossRefPubMed
13.
go back to reference Inaba Y, Chen JA, Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis. 2012;220:128–33.CrossRefPubMed Inaba Y, Chen JA, Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis. 2012;220:128–33.CrossRefPubMed
14.
go back to reference Katakami N, Kaneto H, Osonoi T, Saitou M, Takahara M, Sakamoto F, et al. Usefulness of lipoprotein ratios in assessing carotid atherosclerosis in Japanese type 2 diabetic patients. Atherosclerosis. 2011;214:442–7.CrossRefPubMed Katakami N, Kaneto H, Osonoi T, Saitou M, Takahara M, Sakamoto F, et al. Usefulness of lipoprotein ratios in assessing carotid atherosclerosis in Japanese type 2 diabetic patients. Atherosclerosis. 2011;214:442–7.CrossRefPubMed
15.
go back to reference Bernard S, Sérusclat A, Targe F, Charrière S, Roth O, Beaune J, 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.CrossRefPubMed Bernard S, Sérusclat A, Targe F, Charrière S, Roth O, Beaune J, 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.CrossRefPubMed
16.
go back to reference Lau KK, Wong YK, Chan YH, Yiu KH, Teo KC, Li LS, et al. Prognostic implications of surrogate markers of atherosclerosis in low to intermediate risk patients with type 2 diabetes. Cardiovasc Diabetol. 2012;11:101.CrossRefPubMedPubMedCentral Lau KK, Wong YK, Chan YH, Yiu KH, Teo KC, Li LS, et al. Prognostic implications of surrogate markers of atherosclerosis in low to intermediate risk patients with type 2 diabetes. Cardiovasc Diabetol. 2012;11:101.CrossRefPubMedPubMedCentral
17.
go back to reference Kokubo Y, Nakamura S, Okamura T, Yoshimasa Y, Makino H, Watanabe M, et al. Relationship between blood pressure category and incidence of stroke and myocardial infarction in an urban Japanese population with and without chronic kidney disease: the Suita Study. Stroke. 2009;40:2674–9.CrossRefPubMed Kokubo Y, Nakamura S, Okamura T, Yoshimasa Y, Makino H, Watanabe M, et al. Relationship between blood pressure category and incidence of stroke and myocardial infarction in an urban Japanese population with and without chronic kidney disease: the Suita Study. Stroke. 2009;40:2674–9.CrossRefPubMed
18.
go back to reference Choi SW, Kim HY, Lee YH, Ryu SY, Kweon SS, Rhee JA, et al. eGFR is associated with subclinical atherosclerosis independent of albuminuria: the Dong-gu Study. Atherosclerosis. 2010;212:661–7.CrossRefPubMed Choi SW, Kim HY, Lee YH, Ryu SY, Kweon SS, Rhee JA, et al. eGFR is associated with subclinical atherosclerosis independent of albuminuria: the Dong-gu Study. Atherosclerosis. 2010;212:661–7.CrossRefPubMed
19.
go back to reference Yamashita T, Makino H, Nakatani R, Ohata Y, Miyamoto Y, Kishimoto I. Renal insufficiency without albuminuria is associated with peripheral artery atherosclerosis and lipid metabolism disorders in patients with type 2 diabetes. J Atheroscler Thromb. 2013;20:790–7.CrossRefPubMed Yamashita T, Makino H, Nakatani R, Ohata Y, Miyamoto Y, Kishimoto I. Renal insufficiency without albuminuria is associated with peripheral artery atherosclerosis and lipid metabolism disorders in patients with type 2 diabetes. J Atheroscler Thromb. 2013;20:790–7.CrossRefPubMed
20.
go back to reference Ito H, Komatsu Y, Mifune M, Antoku S, Ishida H, Takeuchi Y, et al. The estimated GFR, but not the stage of diabetic nephropathy graded by the urinary albumin excretion, is associated with the carotid intima-media thickness in patients with type 2 diabetes mellitus: a cross-sectional study. Cardiovasc Diabetol. 2010;9:18.CrossRefPubMedPubMedCentral Ito H, Komatsu Y, Mifune M, Antoku S, Ishida H, Takeuchi Y, et al. The estimated GFR, but not the stage of diabetic nephropathy graded by the urinary albumin excretion, is associated with the carotid intima-media thickness in patients with type 2 diabetes mellitus: a cross-sectional study. Cardiovasc Diabetol. 2010;9:18.CrossRefPubMedPubMedCentral
21.
go back to reference Son JW, Jang EH, Kim MK, Kim HL, Baek KH, Song KH, et al. Usefulness of albuminuria as predictor for coronary artery stenosis, regardless of estimated glomerular filtration rate, in patients with type 2 diabetes mellitus. Am J Cardiol. 2012;110:1434–9.CrossRefPubMed Son JW, Jang EH, Kim MK, Kim HL, Baek KH, Song KH, et al. Usefulness of albuminuria as predictor for coronary artery stenosis, regardless of estimated glomerular filtration rate, in patients with type 2 diabetes mellitus. Am J Cardiol. 2012;110:1434–9.CrossRefPubMed
22.
go back to reference Sjöblom P, Nystrom FH, Länne T, Engvall J, Östgren CJ. Microalbuminuria, but not reduced eGFR, is associated with cardiovascular subclinical organ damage in type 2 diabetes. Diabetes Metab. 2014;40:49–55.CrossRefPubMed Sjöblom P, Nystrom FH, Länne T, Engvall J, Östgren CJ. Microalbuminuria, but not reduced eGFR, is associated with cardiovascular subclinical organ damage in type 2 diabetes. Diabetes Metab. 2014;40:49–55.CrossRefPubMed
23.
go back to reference Wilkinson CP, Ferris 3rd FL, Klein RE, Lee PP, Agardh CD, Davis M, et al. Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRefPubMed Wilkinson CP, Ferris 3rd FL, Klein RE, Lee PP, Agardh CD, Davis M, et al. Global Diabetic Retinopathy Project Group. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRefPubMed
24.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
25.
go back to reference Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P, Bornstein N, 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.CrossRefPubMed Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P, Bornstein N, 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.CrossRefPubMed
26.
go back to reference Rosenson RS, Fioretto P, Dodson PM. Does microvascular disease predict macrovascular events in type 2 diabetes? Atherosclerosis. 2011;218:13–8.CrossRefPubMed Rosenson RS, Fioretto P, Dodson PM. Does microvascular disease predict macrovascular events in type 2 diabetes? Atherosclerosis. 2011;218:13–8.CrossRefPubMed
27.
go back to reference de Kreutzenberg SV, Coracina A, Volpi A, Fadini GP, Frigo AC, Guarneri G, et al. Microangiopathy is independently associated with presence, severity and composition of carotid atherosclerosis in type 2 diabetes. Nutr Metab Cardiovasc Dis. 2011;21:286–93.PubMed de Kreutzenberg SV, Coracina A, Volpi A, Fadini GP, Frigo AC, Guarneri G, et al. Microangiopathy is independently associated with presence, severity and composition of carotid atherosclerosis in type 2 diabetes. Nutr Metab Cardiovasc Dis. 2011;21:286–93.PubMed
28.
go back to reference Jung CH, Baek AR, Kim KJ, Kim BY, Kim CH, Kang SK, et al. Association between cardiac autonomic neuropathy, diabetic retinopathy and carotid atherosclerosis in patients with type 2 diabetes. Endocrinol Metab (Seoul). 2013;4:309–19.CrossRef Jung CH, Baek AR, Kim KJ, Kim BY, Kim CH, Kang SK, et al. Association between cardiac autonomic neuropathy, diabetic retinopathy and carotid atherosclerosis in patients with type 2 diabetes. Endocrinol Metab (Seoul). 2013;4:309–19.CrossRef
29.
go back to reference Saif A, Karawya S, Abdelhamid A. Retinopathy is a strong determinant of atherosclerosis in type 2 diabetes: correlation with carotid intima-media thickness. Endocr Pract. 2014;4:1–21. Saif A, Karawya S, Abdelhamid A. Retinopathy is a strong determinant of atherosclerosis in type 2 diabetes: correlation with carotid intima-media thickness. Endocr Pract. 2014;4:1–21.
30.
go back to reference Miyamoto M, Kotani K, Okada K, Fujii Y, Konno K, Ishibashi S, et al. The correlation of common carotid arterial diameter with atherosclerosis and diabetic retinopathy in patients with type 2 diabetes mellitus. Acta Diabetol. 2012;49:63–8.CrossRefPubMed Miyamoto M, Kotani K, Okada K, Fujii Y, Konno K, Ishibashi S, et al. The correlation of common carotid arterial diameter with atherosclerosis and diabetic retinopathy in patients with type 2 diabetes mellitus. Acta Diabetol. 2012;49:63–8.CrossRefPubMed
31.
go back to reference Akazawa S, Tojikubo M, Nakano Y, Nakamura S, Kawasaki T, Koga N. Usefulness of sum of the thickness of plaque in the carotid artery for predicting the presence and the extent of the coronary artery disease in patients with type 2 diabetes mellitus without known coronary artery disease. Diabetes Res Clin Pract. 2012;96:111–8.CrossRefPubMed Akazawa S, Tojikubo M, Nakano Y, Nakamura S, Kawasaki T, Koga N. Usefulness of sum of the thickness of plaque in the carotid artery for predicting the presence and the extent of the coronary artery disease in patients with type 2 diabetes mellitus without known coronary artery disease. Diabetes Res Clin Pract. 2012;96:111–8.CrossRefPubMed
32.
go back to reference Hollander M, Bots ML, Del Sol AI, Koudstaal PJ, Witteman JC, Grobbee DE, et al. Carotid plaques increase the risk of stroke and subtypes of cerebral infarction in asymptomatic elderly: the Rotterdam study. Circulation. 2002;105:2872–7.CrossRefPubMed Hollander M, Bots ML, Del Sol AI, Koudstaal PJ, Witteman JC, Grobbee DE, et al. Carotid plaques increase the risk of stroke and subtypes of cerebral infarction in asymptomatic elderly: the Rotterdam study. Circulation. 2002;105:2872–7.CrossRefPubMed
33.
go back to reference Mathiesen EB, Johnsen SH, Wilsgaard T, Bønaa KH, Løchen ML, Njølstad I. Carotid plaque area and intima-media thickness in prediction of first-ever ischemic stroke: a 10-year follow-up of 6584 men and women: the Tromsø Study. Stroke. 2011;42:972–8.CrossRefPubMed Mathiesen EB, Johnsen SH, Wilsgaard T, Bønaa KH, Løchen ML, Njølstad I. Carotid plaque area and intima-media thickness in prediction of first-ever ischemic stroke: a 10-year follow-up of 6584 men and women: the Tromsø Study. Stroke. 2011;42:972–8.CrossRefPubMed
34.
go back to reference van der Meer IM, Bots ML, Hofman A, del Sol AI, van der Kuip DA, Witteman JC. Predictive value of noninvasive measures of atherosclerosis for incident myocardial infarction: the Rotterdam Study. Circulation. 2004;109:1089–94.CrossRefPubMed van der Meer IM, Bots ML, Hofman A, del Sol AI, van der Kuip DA, Witteman JC. Predictive value of noninvasive measures of atherosclerosis for incident myocardial infarction: the Rotterdam Study. Circulation. 2004;109:1089–94.CrossRefPubMed
35.
go back to reference O'Leary DH, Bots ML. Imaging of atherosclerosis: carotid intima-media thickness. Eur Heart J. 2010;31:1682–9.CrossRefPubMed O'Leary DH, Bots ML. Imaging of atherosclerosis: carotid intima-media thickness. Eur Heart J. 2010;31:1682–9.CrossRefPubMed
36.
go back to reference Stratton IM, Kohner EM, Aldington SJ, Turner RC, Holman RR, Manley SE, et al. UKPDS 50: risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia. 2001;44:156–63.CrossRefPubMed Stratton IM, Kohner EM, Aldington SJ, Turner RC, Holman RR, Manley SE, et al. UKPDS 50: risk factors for incidence and progression of retinopathy in Type II diabetes over 6 years from diagnosis. Diabetologia. 2001;44:156–63.CrossRefPubMed
37.
go back to reference Inzitari D, Eliasziw M, Gates P, Sharpe BL, Chan RK, Meldrum HE, et al. The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 2000;342:1693–700.CrossRefPubMed Inzitari D, Eliasziw M, Gates P, Sharpe BL, Chan RK, Meldrum HE, et al. The causes and risk of stroke in patients with asymptomatic internal-carotid-artery stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med. 2000;342:1693–700.CrossRefPubMed
38.
go back to reference Betriu A, Martinez-Alonso M, Arcidiacono MV, Cannata-Andia J, Pascual J, Valdivielso JM, et al. Prevalence of subclinical atheromatosis and associated risk factors in chronic kidney disease: the NEFRONA study. Nephrol Dial Transplant. 2014;29:1415–22.CrossRefPubMed Betriu A, Martinez-Alonso M, Arcidiacono MV, Cannata-Andia J, Pascual J, Valdivielso JM, et al. Prevalence of subclinical atheromatosis and associated risk factors in chronic kidney disease: the NEFRONA study. Nephrol Dial Transplant. 2014;29:1415–22.CrossRefPubMed
39.
go back to reference Retnakaran R, Cull CA, Thorne KI, Adler AI, Holman RR, UKPDS Study Group. Risk factors for renal dysfunction in type 2 diabetes: U.K. Prospective Diabetes Study. Diabetes. 2006;55:1832–9.CrossRefPubMed Retnakaran R, Cull CA, Thorne KI, Adler AI, Holman RR, UKPDS Study Group. Risk factors for renal dysfunction in type 2 diabetes: U.K. Prospective Diabetes Study. Diabetes. 2006;55:1832–9.CrossRefPubMed
40.
go back to reference De Cosmo S, Rossi MC, Pellegrini F, Lucisano G, Bacci S, Gentile S, et al. AMD-Annals Study Group. Kidney dysfunction and related cardiovascular risk factors among patients with type 2 diabetes. Nephrol Dial Transplant. 2014;29:657–62.CrossRefPubMed De Cosmo S, Rossi MC, Pellegrini F, Lucisano G, Bacci S, Gentile S, et al. AMD-Annals Study Group. Kidney dysfunction and related cardiovascular risk factors among patients with type 2 diabetes. Nephrol Dial Transplant. 2014;29:657–62.CrossRefPubMed
41.
go back to reference O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999;340:14–22.CrossRefPubMed O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999;340:14–22.CrossRefPubMed
42.
go back to reference Finn AV, Kolodgie FD, Virmani R. Correlation between carotid intimal/medial thickness and atherosclerosis: a point of view from pathology. Arterioscler Thromb Vasc Biol. 2010;30:177–81.CrossRefPubMed Finn AV, Kolodgie FD, Virmani R. Correlation between carotid intimal/medial thickness and atherosclerosis: a point of view from pathology. Arterioscler Thromb Vasc Biol. 2010;30:177–81.CrossRefPubMed
43.
go back to reference Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging. 2014;7:1025–38.CrossRefPubMed Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging. 2014;7:1025–38.CrossRefPubMed
44.
go back to reference Klein R, Sharrett AR, Klein BE, Moss SE, Folsom AR, Wong TY, et al. The association of atherosclerosis, vascular risk factors, and retinopathy in adults with diabetes: the atherosclerosis risk in communities study. Ophthalmology. 2002;109:1225–34.CrossRefPubMed Klein R, Sharrett AR, Klein BE, Moss SE, Folsom AR, Wong TY, et al. The association of atherosclerosis, vascular risk factors, and retinopathy in adults with diabetes: the atherosclerosis risk in communities study. Ophthalmology. 2002;109:1225–34.CrossRefPubMed
45.
go back to reference Klein R, Marino EK, Kuller LH, Polak JF, Tracy RP, Gottdiener JS, et al. The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study. Br J Ophthalmol. 2002;86:84–90.CrossRefPubMedPubMedCentral Klein R, Marino EK, Kuller LH, Polak JF, Tracy RP, Gottdiener JS, et al. The relation of atherosclerotic cardiovascular disease to retinopathy in people with diabetes in the Cardiovascular Health Study. Br J Ophthalmol. 2002;86:84–90.CrossRefPubMedPubMedCentral
46.
go back to reference Kawasaki R, Cheung N, Islam FM, Klein R, Klein BE, Cotch MF, et al. Multi-Ethnic Study of Atherosclerosis. Is diabetic retinopathy related to subclinical cardiovascular disease? Ophthalmology. 2011;118:860–5.CrossRefPubMed Kawasaki R, Cheung N, Islam FM, Klein R, Klein BE, Cotch MF, et al. Multi-Ethnic Study of Atherosclerosis. Is diabetic retinopathy related to subclinical cardiovascular disease? Ophthalmology. 2011;118:860–5.CrossRefPubMed
47.
go back to reference Kawasaki R, Xie J, Cheung N, Lamoureux E, Klein R, Klein BE, et al. MESA: Retinal microvascular signs and risk of stroke: the Multi-Ethnic Study of Atherosclerosis (MESA). Stroke. 2012;43:3245–51.CrossRefPubMedPubMedCentral Kawasaki R, Xie J, Cheung N, Lamoureux E, Klein R, Klein BE, et al. MESA: Retinal microvascular signs and risk of stroke: the Multi-Ethnic Study of Atherosclerosis (MESA). Stroke. 2012;43:3245–51.CrossRefPubMedPubMedCentral
48.
go back to reference Wong TY, Rosamond W, Chang PP, Couper DJ, Sharrett AR, Hubbard LD, et al. Retinopathy and risk of congestive heart failure. JAMA. 2005;293:63–9.CrossRefPubMed Wong TY, Rosamond W, Chang PP, Couper DJ, Sharrett AR, Hubbard LD, et al. Retinopathy and risk of congestive heart failure. JAMA. 2005;293:63–9.CrossRefPubMed
49.
go back to reference Wong TY, Klein R, Nieto FJ, Klein BE, Sharrett AR, Meuer SM, et al. Retinal microvascular abnormalities and 10-year cardiovascular mortality: a population-based case–control study. Ophthalmology. 2003;110:933–40.CrossRefPubMed Wong TY, Klein R, Nieto FJ, Klein BE, Sharrett AR, Meuer SM, et al. Retinal microvascular abnormalities and 10-year cardiovascular mortality: a population-based case–control study. Ophthalmology. 2003;110:933–40.CrossRefPubMed
50.
go back to reference Ogagarue ER, Lutsey PL, Klein R, Klein BE, Folsom AR. Association of ideal cardiovascular health metrics and retinal microvascular findings: the Atherosclerosis Risk in Communities Study. J Am Heart Assoc. 2013;2:e000430.CrossRefPubMedPubMedCentral Ogagarue ER, Lutsey PL, Klein R, Klein BE, Folsom AR. Association of ideal cardiovascular health metrics and retinal microvascular findings: the Atherosclerosis Risk in Communities Study. J Am Heart Assoc. 2013;2:e000430.CrossRefPubMedPubMedCentral
51.
go back to reference Hanff TC, Sharrett AR, Mosley TH, Shibata D, Knopman DS, Klein R, et al. Retinal microvascular abnormalities predict progression of brain microvascular disease: an atherosclerosis risk in communities magnetic resonance imaging study. Stroke. 2014;45:1012–7.CrossRefPubMedPubMedCentral Hanff TC, Sharrett AR, Mosley TH, Shibata D, Knopman DS, Klein R, et al. Retinal microvascular abnormalities predict progression of brain microvascular disease: an atherosclerosis risk in communities magnetic resonance imaging study. Stroke. 2014;45:1012–7.CrossRefPubMedPubMedCentral
Metadata
Title
Type 2 diabetes-associated carotid plaque burden is increased in patients with retinopathy compared to those without retinopathy
Authors
Núria Alonso
Alicia Traveset
Esther Rubinat
Emilio Ortega
Nuria Alcubierre
Jordi Sanahuja
Marta Hernández
Angels Betriu
Carmen Jurjo
Elvira Fernández
Didac Mauricio
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2015
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-015-0196-1

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