Skip to main content
Top
Published in: Graefe's Archive for Clinical and Experimental Ophthalmology 11/2016

Open Access 01-11-2016 | Pathology

The relationship of systemic markers of renal function and vascular function with retinal blood vessel responses

Authors: R. Heitmar, C. Varma, P. De, Y. C. Lau, A. D. Blann

Published in: Graefe's Archive for Clinical and Experimental Ophthalmology | Issue 11/2016

Login to get access

Abstract

Purpose

To test the hypothesis of a significant relationship between systemic markers of renal and vascular function (processes linked to cardiovascular disease and its development) and retinal microvascular function in diabetes and/or cardiovascular disease.

Methods

Ocular microcirculatory function was measured in 116 patients with diabetes and/or cardiovascular disease using static and continuous retinal vessel responses to three cycles of flickering light. Endothelial function was evaluated by von Willebrand factor (vWf), endothelial microparticles and soluble E selectin, renal function by serum creatinine, creatinine clearance and estimated glomerular filtration rate (eGFR). HbA1c was used as a control index.

Results

Central retinal vein equivalence and venous maximum dilation to flicker were linked to HbA1c (both p < 0.05). Arterial reaction time was linked to serum creatinine (p = 0.036) and eGFR (p = 0.039); venous reaction time was linked to creatinine clearance (p = 0.018). Creatinine clearance and eGFR were linked to arterial maximum dilatation (p < 0.001 and p = 0.003, respectively) and the dilatation amplitude (p = 0.038 and p = 0.048, respectively) responses in the third flicker cycle. Of venous responses to the first flicker cycle, HbA1c was linked to the maximum dilation response (p = 0.004) and dilatation amplitude (p = 0.017), vWf was linked to the maximum constriction response (p = 0.016), and creatinine clearance to the baseline diameter fluctuation (p = 0.029). In the second flicker cycle, dilatation amplitude was linked to serum creatinine (p = 0.022).

Conclusions

Several retinal blood vessel responses to flickering light are linked to glycaemia and renal function, but only one index is linked to endothelial function. Renal function must be considered when interpreting retinal vessel responses.
Literature
1.
go back to reference Sayin N, Kara N, Pekel G (2015) Ocular complications of diabetes mellitus. World J Diab 15:92–108CrossRef Sayin N, Kara N, Pekel G (2015) Ocular complications of diabetes mellitus. World J Diab 15:92–108CrossRef
2.
go back to reference Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B (2005) Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat 206:319–348CrossRefPubMedPubMedCentral Patton N, Aslam T, Macgillivray T, Pattie A, Deary IJ, Dhillon B (2005) Retinal vascular image analysis as a potential screening tool for cerebrovascular disease: a rationale based on homology between cerebral and retinal microvasculatures. J Anat 206:319–348CrossRefPubMedPubMedCentral
3.
go back to reference Liew G, Wang JJ, Mitchell P, Wong TY (2008) Retinal vascular imaging: a new tool in microvascular disease research. Circ Cardiovasc Imaging 1:156–161CrossRefPubMed Liew G, Wang JJ, Mitchell P, Wong TY (2008) Retinal vascular imaging: a new tool in microvascular disease research. Circ Cardiovasc Imaging 1:156–161CrossRefPubMed
5.
go back to reference Kawasaki R, Cheung N, Mosley T et al (2010) Retinal microvascular signs and 10-year risk of cerebral atrophy: the Atherosclerosis Risk in Communities (ARIC) study. Stroke 41:1826–1828CrossRefPubMedPubMedCentral Kawasaki R, Cheung N, Mosley T et al (2010) Retinal microvascular signs and 10-year risk of cerebral atrophy: the Atherosclerosis Risk in Communities (ARIC) study. Stroke 41:1826–1828CrossRefPubMedPubMedCentral
6.
go back to reference Kawasaki R, Xie J, Cheung N, Lamoureux E, Klein R, Klein BE et al (2012) Retinal microvascular signs and risk of stroke: the Multi-Ethnic Study of Atherosclerosis (MESA). Stroke 43:3245–3251CrossRefPubMedPubMedCentral Kawasaki R, Xie J, Cheung N, Lamoureux E, Klein R, Klein BE et al (2012) Retinal microvascular signs and risk of stroke: the Multi-Ethnic Study of Atherosclerosis (MESA). Stroke 43:3245–3251CrossRefPubMedPubMedCentral
7.
go back to reference Liew G, Wang JJ, Rochtchina E, Wong TY, Mitchell P (2014) Complete blood count and retinal vessel calibers. PLoS One 18(9):e102230 Liew G, Wang JJ, Rochtchina E, Wong TY, Mitchell P (2014) Complete blood count and retinal vessel calibers. PLoS One 18(9):e102230
8.
go back to reference Wang JJ, Liew G, Wong TY, Smith W, Klein R, Leeder SR et al (2006) Retinal vascular calibre and the risk of coronary heart disease-related death. Heart 92:1583–1587CrossRefPubMedPubMedCentral Wang JJ, Liew G, Wong TY, Smith W, Klein R, Leeder SR et al (2006) Retinal vascular calibre and the risk of coronary heart disease-related death. Heart 92:1583–1587CrossRefPubMedPubMedCentral
9.
go back to reference von Hanno T, Bertelsen G, Sjølie AK, Mathiesen EB (2014) Retinal vascular calibres are significantly associated with cardiovascular risk factors: the Tromsø Eye Study. Acta Ophthalmol 92:40–46CrossRef von Hanno T, Bertelsen G, Sjølie AK, Mathiesen EB (2014) Retinal vascular calibres are significantly associated with cardiovascular risk factors: the Tromsø Eye Study. Acta Ophthalmol 92:40–46CrossRef
10.
go back to reference Ogagarue ER, Lutsey PL, Klein R, Klein BE, Folsom AR (2013) Association of ideal cardiovascular health metrics and retinal microvascular findings: the Atherosclerosis Risk in Communities Study. J Am Heart Assoc 19(2):e000430 Ogagarue ER, Lutsey PL, Klein R, Klein BE, Folsom AR (2013) Association of ideal cardiovascular health metrics and retinal microvascular findings: the Atherosclerosis Risk in Communities Study. J Am Heart Assoc 19(2):e000430
11.
go back to reference Pemp B, Weigert G, Karl K, Petzl U, Wolzt M, Schmetterer L et al (2009) Correlation of flicker-induced and flow-mediated vasodilatation in patients with endothelial dysfunction and healthy volunteers. Diabetes Care 32:1536–1541CrossRefPubMedPubMedCentral Pemp B, Weigert G, Karl K, Petzl U, Wolzt M, Schmetterer L et al (2009) Correlation of flicker-induced and flow-mediated vasodilatation in patients with endothelial dysfunction and healthy volunteers. Diabetes Care 32:1536–1541CrossRefPubMedPubMedCentral
12.
go back to reference Heitmar R, Cubbidge RP, Lip GY, Gherghel D, Blann AD (2011) Altered blood vessel responses in the eye and finger in coronary artery disease. Invest Ophthalmol Vis Sci 52:6199–6205CrossRefPubMed Heitmar R, Cubbidge RP, Lip GY, Gherghel D, Blann AD (2011) Altered blood vessel responses in the eye and finger in coronary artery disease. Invest Ophthalmol Vis Sci 52:6199–6205CrossRefPubMed
13.
go back to reference Al-Fiadh AH, Wong TY, Kawasaki R, Clark DJ, Patel SK, Freeman M et al (2015) Usefulness of retinal microvascular endothelial dysfunction as a predictor of coronary artery disease. Am J Cardiol 115:609–613CrossRefPubMed Al-Fiadh AH, Wong TY, Kawasaki R, Clark DJ, Patel SK, Freeman M et al (2015) Usefulness of retinal microvascular endothelial dysfunction as a predictor of coronary artery disease. Am J Cardiol 115:609–613CrossRefPubMed
14.
go back to reference Mandecka A, Dawczynski J, Blum M, Müller N, Kloos C, Wolf G et al (2007) Influence of flickering light on the retinal vessels in diabetic patients. Diabetes Care 30:3048–3052CrossRefPubMed Mandecka A, Dawczynski J, Blum M, Müller N, Kloos C, Wolf G et al (2007) Influence of flickering light on the retinal vessels in diabetic patients. Diabetes Care 30:3048–3052CrossRefPubMed
15.
go back to reference Nguyen TT, Kawasaki R, Kreis AJ, Wang JJ, Shaw J, Vilser W et al (2009) Correlation of light-flicker-induced retinal vasodilation and retinal vascular caliber measurements in diabetes. Invest Ophthalmol Vis Sci 50:5609–5613CrossRefPubMed Nguyen TT, Kawasaki R, Kreis AJ, Wang JJ, Shaw J, Vilser W et al (2009) Correlation of light-flicker-induced retinal vasodilation and retinal vascular caliber measurements in diabetes. Invest Ophthalmol Vis Sci 50:5609–5613CrossRefPubMed
16.
go back to reference Lim LS, Ling LH, Ong PG, Foulds W, Tai ES, Wong E (2014) Dynamic responses in retinal vessel caliber with flicker light stimulation in eyes with diabetic retinopathy. Invest Ophthalmol Vis Sci 55:5207–5213CrossRefPubMed Lim LS, Ling LH, Ong PG, Foulds W, Tai ES, Wong E (2014) Dynamic responses in retinal vessel caliber with flicker light stimulation in eyes with diabetic retinopathy. Invest Ophthalmol Vis Sci 55:5207–5213CrossRefPubMed
17.
go back to reference Fischer-Rasokat U, Spyridopoulos I, Walter J, Honold J, Zeiher AM, Fichtlscherer S (2012) Microvascular dysfunction and pulse wave reflection characterize different vascular pathologies in patients at cardiovascular risk. Vasa 41:192–199CrossRefPubMed Fischer-Rasokat U, Spyridopoulos I, Walter J, Honold J, Zeiher AM, Fichtlscherer S (2012) Microvascular dysfunction and pulse wave reflection characterize different vascular pathologies in patients at cardiovascular risk. Vasa 41:192–199CrossRefPubMed
18.
go back to reference Madonna R, De Caterina R (2011) Cellular and molecular mechanisms of vascular injury in diabetes–part I: pathways of vascular disease in diabetes. Vascul Pharmacol 54:68–74CrossRefPubMed Madonna R, De Caterina R (2011) Cellular and molecular mechanisms of vascular injury in diabetes–part I: pathways of vascular disease in diabetes. Vascul Pharmacol 54:68–74CrossRefPubMed
19.
go back to reference Blann AD, Taberner DA (1995) A reliable marker of endothelial cell dysfunction: does it exist? Br J Haematol 90:244–248CrossRefPubMed Blann AD, Taberner DA (1995) A reliable marker of endothelial cell dysfunction: does it exist? Br J Haematol 90:244–248CrossRefPubMed
20.
go back to reference Lekakis J, Abraham P, Balbarini A, Blann A, Boulanger CM, Cockcroft J et al (2011) Methods for evaluating endothelial function: a position statement from the European Society of Cardiology Working Group on Peripheral Circulation. Eur J Cardiovasc Prev Rehabil 18:775–789CrossRefPubMed Lekakis J, Abraham P, Balbarini A, Blann A, Boulanger CM, Cockcroft J et al (2011) Methods for evaluating endothelial function: a position statement from the European Society of Cardiology Working Group on Peripheral Circulation. Eur J Cardiovasc Prev Rehabil 18:775–789CrossRefPubMed
21.
go back to reference Berezin A, Zulli A, Kerrigan S, Petrovic D, Kruzliak P (2015) Predictive role of circulating endothelial-derived microparticles in cardiovascular diseases. Clin Biochem 48:562–568CrossRefPubMed Berezin A, Zulli A, Kerrigan S, Petrovic D, Kruzliak P (2015) Predictive role of circulating endothelial-derived microparticles in cardiovascular diseases. Clin Biochem 48:562–568CrossRefPubMed
22.
go back to reference James MT, Grams ME, Woodward M, Elley CR, Green JA (2015) A meta-analysis of the association of estimated GFR, albuminuria, diabetes mellitus, and hypertension with acute kidney injury. Am J Kidney Dis 66:602–612CrossRefPubMedPubMedCentral James MT, Grams ME, Woodward M, Elley CR, Green JA (2015) A meta-analysis of the association of estimated GFR, albuminuria, diabetes mellitus, and hypertension with acute kidney injury. Am J Kidney Dis 66:602–612CrossRefPubMedPubMedCentral
23.
go back to reference Garimella PS, Hirsch AT (2014) Peripheral artery disease and chronic kidney disease: clinical synergy to improve outcomes. Adv Chronic Kidney Dis 21:460–471CrossRefPubMedPubMedCentral Garimella PS, Hirsch AT (2014) Peripheral artery disease and chronic kidney disease: clinical synergy to improve outcomes. Adv Chronic Kidney Dis 21:460–471CrossRefPubMedPubMedCentral
24.
go back to reference Di Lullo L, House A, Gorini A, Santoboni A, Russo D, Ronco C (2015) Chronic kidney disease and cardiovascular complications. Heart Fail Rev 20:259–272CrossRefPubMed Di Lullo L, House A, Gorini A, Santoboni A, Russo D, Ronco C (2015) Chronic kidney disease and cardiovascular complications. Heart Fail Rev 20:259–272CrossRefPubMed
25.
go back to reference Shlipak MG, Fried LF, Crump C, Bleyer AJ, Manolio TA, Tracy RP et al (2002) Cardiovascular disease risk status in elderly persons with renal insufficiency. Kidney Int 62:997–1004CrossRefPubMed Shlipak MG, Fried LF, Crump C, Bleyer AJ, Manolio TA, Tracy RP et al (2002) Cardiovascular disease risk status in elderly persons with renal insufficiency. Kidney Int 62:997–1004CrossRefPubMed
26.
go back to reference El Husseini N, Kaskar O, Goldstein LB (2014) Chronic kidney disease and stroke. Adv Chronic Kidney Dis 21:500–508CrossRefPubMed El Husseini N, Kaskar O, Goldstein LB (2014) Chronic kidney disease and stroke. Adv Chronic Kidney Dis 21:500–508CrossRefPubMed
27.
28.
go back to reference Hubbard LD, Brothers RJ, King WN, Clegg LX, Klein R et al (1999) Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the atherosclerosis risk in communities study. Ophthalmology 106:2269–2280CrossRefPubMed Hubbard LD, Brothers RJ, King WN, Clegg LX, Klein R et al (1999) Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the atherosclerosis risk in communities study. Ophthalmology 106:2269–2280CrossRefPubMed
29.
go back to reference Parr JC, Spears GF (1974) General caliber of the retinal arteries expressed as the equivalent width of the central retinal artery. Am J Ophthalmol 77:472–477CrossRefPubMed Parr JC, Spears GF (1974) General caliber of the retinal arteries expressed as the equivalent width of the central retinal artery. Am J Ophthalmol 77:472–477CrossRefPubMed
30.
go back to reference Blum M, Bachmann K, Wintzer D, Riemer T, Vilser W, Strobel J (1999) Noninvasive measurement of the Bayliss effect in retinal autoregulation. Graefes Arch Clin Exp Ophthalmol 237:296–300CrossRefPubMed Blum M, Bachmann K, Wintzer D, Riemer T, Vilser W, Strobel J (1999) Noninvasive measurement of the Bayliss effect in retinal autoregulation. Graefes Arch Clin Exp Ophthalmol 237:296–300CrossRefPubMed
31.
go back to reference Seifertl BU, Vilser W (2002) Retinal Vessel Analyzer (RVA)–design and function. Biomed Tech 47(Suppl 1 Pt 2):678–681 Seifertl BU, Vilser W (2002) Retinal Vessel Analyzer (RVA)–design and function. Biomed Tech 47(Suppl 1 Pt 2):678–681
32.
go back to reference Garhofer G, Bek T, Boehm AG, Gherghel D, Grunwald J, Jeppesen P et al (2010) Use of the retinal vessel analyzer in ocular blood flow research. Acta Ophthalmol 88:717–722CrossRefPubMed Garhofer G, Bek T, Boehm AG, Gherghel D, Grunwald J, Jeppesen P et al (2010) Use of the retinal vessel analyzer in ocular blood flow research. Acta Ophthalmol 88:717–722CrossRefPubMed
33.
go back to reference Heitmar R, Blann AD, Cubbidge RP, Lip GYH, Gherghel D (2010) Continuous retinal vessel diameter measurements - the future of retinal vessel assessment? Invest Ophthalmol Vis Sci 51:5833–5839CrossRefPubMed Heitmar R, Blann AD, Cubbidge RP, Lip GYH, Gherghel D (2010) Continuous retinal vessel diameter measurements - the future of retinal vessel assessment? Invest Ophthalmol Vis Sci 51:5833–5839CrossRefPubMed
34.
go back to reference Montoro-García S, Shantsila E, Tapp LD, López-Cuenca A, Romero AI, Hernández-Romero D et al (2013) Small-size circulating microparticles in acute coronary syndromes: relevance to fibrinolytic status, reparative markers and outcomes. Atherosclerosis 227:313–322CrossRefPubMed Montoro-García S, Shantsila E, Tapp LD, López-Cuenca A, Romero AI, Hernández-Romero D et al (2013) Small-size circulating microparticles in acute coronary syndromes: relevance to fibrinolytic status, reparative markers and outcomes. Atherosclerosis 227:313–322CrossRefPubMed
35.
go back to reference Cockcroft DW, Gault MH (1976) Prediction of creatinine clearance from serum creatinine. Nephron 16:31–41CrossRefPubMed Cockcroft DW, Gault MH (1976) Prediction of creatinine clearance from serum creatinine. Nephron 16:31–41CrossRefPubMed
36.
go back to reference Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) 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 130:461–470CrossRefPubMed Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) 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 130:461–470CrossRefPubMed
37.
go back to reference Altman DG (1991) Practical statistics for medical research. Chapman and Hall, London Altman DG (1991) Practical statistics for medical research. Chapman and Hall, London
38.
go back to reference Wong TY, Klein R, Klein BE, Tielsch JM, Hubbard L, Nieto FJ (2001) Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv Ophthalmol 46:59–80CrossRefPubMed Wong TY, Klein R, Klein BE, Tielsch JM, Hubbard L, Nieto FJ (2001) Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv Ophthalmol 46:59–80CrossRefPubMed
39.
go back to reference Fujioka S, Karashima K, Nishikawa N, Saito Y (2006) Ocular circulation in diabetic patients with coronary artery disease. Graefes Arch Clin Exp Ophthalmol 244:163–169CrossRefPubMed Fujioka S, Karashima K, Nishikawa N, Saito Y (2006) Ocular circulation in diabetic patients with coronary artery disease. Graefes Arch Clin Exp Ophthalmol 244:163–169CrossRefPubMed
40.
go back to reference Patton N, Aslam TM, Macgillivray T, Deary IJ, Dhillon B, Eikelboom RH et al (2006) Retinal image analysis: concepts, applications and potential. Prog Retin Eye Res 25:99–127CrossRefPubMed Patton N, Aslam TM, Macgillivray T, Deary IJ, Dhillon B, Eikelboom RH et al (2006) Retinal image analysis: concepts, applications and potential. Prog Retin Eye Res 25:99–127CrossRefPubMed
41.
go back to reference Nguyen TT, Kawasaki R, Wang JJ, Kreis AJ, Shaw J, Vilser W et al (2009) Flicker light-induced retinal vasodilation in diabetes and diabetic retinopathy. Diabetes Care 32:2075–2080CrossRefPubMedPubMedCentral Nguyen TT, Kawasaki R, Wang JJ, Kreis AJ, Shaw J, Vilser W et al (2009) Flicker light-induced retinal vasodilation in diabetes and diabetic retinopathy. Diabetes Care 32:2075–2080CrossRefPubMedPubMedCentral
42.
go back to reference Gugleta K, Kochkorov A, Waldmann N, Polunina A, Katamay R, Flammer J et al (2012) Dynamics of retinal vessel response to flicker light in glaucoma patients and ocular hypertensives. Graefes Arch Clin Exp Ophthalmol 250:589–594CrossRefPubMed Gugleta K, Kochkorov A, Waldmann N, Polunina A, Katamay R, Flammer J et al (2012) Dynamics of retinal vessel response to flicker light in glaucoma patients and ocular hypertensives. Graefes Arch Clin Exp Ophthalmol 250:589–594CrossRefPubMed
43.
go back to reference Garhöfer G, Zawinka C, Resch H, Kothy P, Schmetterer L, Dorner GT (2004) Reduced response of retinal vessel diameters to flicker stimulation in patients with diabetes. Br J Ophthalmol 88:887–891CrossRefPubMedPubMedCentral Garhöfer G, Zawinka C, Resch H, Kothy P, Schmetterer L, Dorner GT (2004) Reduced response of retinal vessel diameters to flicker stimulation in patients with diabetes. Br J Ophthalmol 88:887–891CrossRefPubMedPubMedCentral
44.
go back to reference Lott ME, Slocomb JE, Shivkumar V, Smith B, Gabbay RA, Quillen D et al (2012) Comparison of retinal vasodilator and constrictor responses in type 2 diabetes. Acta Ophthalmol 90:e434–e441CrossRefPubMed Lott ME, Slocomb JE, Shivkumar V, Smith B, Gabbay RA, Quillen D et al (2012) Comparison of retinal vasodilator and constrictor responses in type 2 diabetes. Acta Ophthalmol 90:e434–e441CrossRefPubMed
45.
go back to reference Dorner GT, Garhofer G, Kiss B, Polska E, Polak K, Riva CE et al (2003) Nitric oxide regulates retinal vascular tone in humans. Am J Physiol Heart Circ Physiol 285:H631–H636CrossRefPubMed Dorner GT, Garhofer G, Kiss B, Polska E, Polak K, Riva CE et al (2003) Nitric oxide regulates retinal vascular tone in humans. Am J Physiol Heart Circ Physiol 285:H631–H636CrossRefPubMed
46.
go back to reference Lott ME, Slocomb JE, Shivkumar V, Smith B, Quillen D, Gabbay RA et al (2013) Impaired retinal vasodilator responses in prediabetes and type 2 diabetes. Acta Ophthalmol 91:e462–e469CrossRefPubMedPubMedCentral Lott ME, Slocomb JE, Shivkumar V, Smith B, Quillen D, Gabbay RA et al (2013) Impaired retinal vasodilator responses in prediabetes and type 2 diabetes. Acta Ophthalmol 91:e462–e469CrossRefPubMedPubMedCentral
47.
go back to reference Kubisz P, Stančiaková L, Staško J, Galajda P, Mokáň M (2015) Endothelial and platelet markers in diabetes mellitus type 2. World J Diab 6:423–431CrossRef Kubisz P, Stančiaková L, Staško J, Galajda P, Mokáň M (2015) Endothelial and platelet markers in diabetes mellitus type 2. World J Diab 6:423–431CrossRef
48.
go back to reference Lim HS, Chong AY, Freestone B, Blann AD, Lip GY (2005) The effect of multi-factorial intervention on plasma von Willebrand factor, soluble E-selectin and tissue factor in diabetes mellitus: implications for atherosclerotic vascular disease. Diabet Med 22:249–255 Lim HS, Chong AY, Freestone B, Blann AD, Lip GY (2005) The effect of multi-factorial intervention on plasma von Willebrand factor, soluble E-selectin and tissue factor in diabetes mellitus: implications for atherosclerotic vascular disease. Diabet Med 22:249–255
52.
go back to reference Landray MJ, Wheeler DC, Lip GY, Newman DJ, Blann AD, McGlynn FJ et al (2014) Inflammation, endothelial dysfunction, and platelet activation in patients with chronic kidney disease: the chronic renal impairment in Birmingham (CRIB) study. Am J Kidney Dis 43:244–253CrossRef Landray MJ, Wheeler DC, Lip GY, Newman DJ, Blann AD, McGlynn FJ et al (2014) Inflammation, endothelial dysfunction, and platelet activation in patients with chronic kidney disease: the chronic renal impairment in Birmingham (CRIB) study. Am J Kidney Dis 43:244–253CrossRef
53.
go back to reference Umemura T, Kawamura T, Hotta N, Koga H, Sugiyama S, Kugiyama K, Watanabe K, Fukushima H, Tanaka T, Sakamoto T, Yoshimura M, Jinnouchi H, Ogawa H (2005) Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 45:1622–1630CrossRef Umemura T, Kawamura T, Hotta N, Koga H, Sugiyama S, Kugiyama K, Watanabe K, Fukushima H, Tanaka T, Sakamoto T, Yoshimura M, Jinnouchi H, Ogawa H (2005) Elevated levels of VE-cadherin-positive endothelial microparticles in patients with type 2 diabetes mellitus and coronary artery disease. J Am Coll Cardiol 45:1622–1630CrossRef
54.
go back to reference Tramontano AF, Lyubarova R, Tsiakos J, Palaia T, Deleon JR, Ragolia L (2010) Circulating endothelial microparticles in diabetes mellitus. Mediat Inflamm 250476. doi:10.1155/2010/250476 Tramontano AF, Lyubarova R, Tsiakos J, Palaia T, Deleon JR, Ragolia L (2010) Circulating endothelial microparticles in diabetes mellitus. Mediat Inflamm 250476. doi:10.​1155/​2010/​250476
55.
go back to reference Lenting PJ, Christophe OD, Denis CV (2015) von Willebrand factor biosynthesis, secretion, and clearance: connecting the far ends. Blood 125:2019–2028CrossRefPubMed Lenting PJ, Christophe OD, Denis CV (2015) von Willebrand factor biosynthesis, secretion, and clearance: connecting the far ends. Blood 125:2019–2028CrossRefPubMed
56.
go back to reference Blann AD (2006) Plasma von Willebrand factor, thrombosis, and the endothelium: the first 30 years. Thromb Haemost 95:49–55PubMed Blann AD (2006) Plasma von Willebrand factor, thrombosis, and the endothelium: the first 30 years. Thromb Haemost 95:49–55PubMed
57.
go back to reference Porta M, Townsend C, Clover GM, Nanson M, Alderson AR, McCraw A, Kohner EM (1981) Evidence for functional endothelial cell damage in early diabetic retinopathy. Diabetologia 20:597–601CrossRefPubMed Porta M, Townsend C, Clover GM, Nanson M, Alderson AR, McCraw A, Kohner EM (1981) Evidence for functional endothelial cell damage in early diabetic retinopathy. Diabetologia 20:597–601CrossRefPubMed
58.
go back to reference Lufkin EG, Fass DN, O’Fallon WM, Bowie EJ (1979) Increased von Willebrand factor in diabetes mellitus. Metabolism 28:63–66CrossRefPubMed Lufkin EG, Fass DN, O’Fallon WM, Bowie EJ (1979) Increased von Willebrand factor in diabetes mellitus. Metabolism 28:63–66CrossRefPubMed
59.
go back to reference Zarbock A, Ley K, McEver RP, Hidalgo A (2011) Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118:6743–6751CrossRefPubMedPubMedCentral Zarbock A, Ley K, McEver RP, Hidalgo A (2011) Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118:6743–6751CrossRefPubMedPubMedCentral
60.
go back to reference Roldán V, Marín F, Lip GY, Blann AD (2003) Soluble E-selectin in cardiovascular disease and its risk factors. Thromb Haemost 90:1007–1020PubMed Roldán V, Marín F, Lip GY, Blann AD (2003) Soluble E-selectin in cardiovascular disease and its risk factors. Thromb Haemost 90:1007–1020PubMed
61.
go back to reference Gearing AJ, Hemingway I, Pigott R, Hughes J, Rees AJ, Cashman SJ (1992) Soluble forms of vascular adhesion molecules, E-selectin, ICAM-1, and VCAM-1: pathological significance. Ann N Y Acad Sci 667:324–331CrossRefPubMed Gearing AJ, Hemingway I, Pigott R, Hughes J, Rees AJ, Cashman SJ (1992) Soluble forms of vascular adhesion molecules, E-selectin, ICAM-1, and VCAM-1: pathological significance. Ann N Y Acad Sci 667:324–331CrossRefPubMed
62.
go back to reference Paneni F, Beckman JA, Creager MA, Cosentino F (2013) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J 34:2436–2443CrossRefPubMedPubMedCentral Paneni F, Beckman JA, Creager MA, Cosentino F (2013) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J 34:2436–2443CrossRefPubMedPubMedCentral
63.
go back to reference Kampoli AM, Tousoulis D, Briasoulis A, Latsios G, Papageorgiou N, Stefanadis C (2011) Potential pathogenic inflammatory mechanisms of endothelial dysfunction induced by type 2 diabetes mellitus. Curr Pharm Des 17:4147–4158CrossRefPubMed Kampoli AM, Tousoulis D, Briasoulis A, Latsios G, Papageorgiou N, Stefanadis C (2011) Potential pathogenic inflammatory mechanisms of endothelial dysfunction induced by type 2 diabetes mellitus. Curr Pharm Des 17:4147–4158CrossRefPubMed
64.
go back to reference Galada P, Martibka E, Mokan M, Kubisz P (1997) Endothelial markers in diabetes mellitus. Thrombosis Res 85:63–65CrossRef Galada P, Martibka E, Mokan M, Kubisz P (1997) Endothelial markers in diabetes mellitus. Thrombosis Res 85:63–65CrossRef
65.
go back to reference Chen Y, Feng B, Li X, Ni Y, Lou Y (2012) Plasma endothelial microparticles and their correlation with the presence of hypertension and arterial stiffness in patients with type 2 diabetes. J Clin Hypertens 14:455–460CrossRef Chen Y, Feng B, Li X, Ni Y, Lou Y (2012) Plasma endothelial microparticles and their correlation with the presence of hypertension and arterial stiffness in patients with type 2 diabetes. J Clin Hypertens 14:455–460CrossRef
66.
go back to reference Yip, WF, Sabanayagam C, Teo BW, Tay WT, Ikram MK, Tai ES et al (2015) Retinal microvascular abnormalities and risk of renal failure in Asian populations. PLOS ONE 10(2):e0118076 Yip, WF, Sabanayagam C, Teo BW, Tay WT, Ikram MK, Tai ES et al (2015) Retinal microvascular abnormalities and risk of renal failure in Asian populations. PLOS ONE 10(2):e0118076
67.
go back to reference Eriksen BO, Lochen ML, Arntzen KA, Bertelsen G, Winther EBA, von Hanno T et al (2015) Estimated and measured GFR associate differently with retinal vasculopathy in the general population. Nephron 131:175–184CrossRefPubMed Eriksen BO, Lochen ML, Arntzen KA, Bertelsen G, Winther EBA, von Hanno T et al (2015) Estimated and measured GFR associate differently with retinal vasculopathy in the general population. Nephron 131:175–184CrossRefPubMed
68.
go back to reference Lim LS, Cheung CY, Sabanayagam C, Lim SC, Tai ES, Hung L et al (2013) Structural changes in the retinal microvasculature and renal function. Invest Opthalm Vis Sci 54(4):2970–2976CrossRef Lim LS, Cheung CY, Sabanayagam C, Lim SC, Tai ES, Hung L et al (2013) Structural changes in the retinal microvasculature and renal function. Invest Opthalm Vis Sci 54(4):2970–2976CrossRef
Metadata
Title
The relationship of systemic markers of renal function and vascular function with retinal blood vessel responses
Authors
R. Heitmar
C. Varma
P. De
Y. C. Lau
A. D. Blann
Publication date
01-11-2016
Publisher
Springer Berlin Heidelberg
Published in
Graefe's Archive for Clinical and Experimental Ophthalmology / Issue 11/2016
Print ISSN: 0721-832X
Electronic ISSN: 1435-702X
DOI
https://doi.org/10.1007/s00417-016-3432-9

Other articles of this Issue 11/2016

Graefe's Archive for Clinical and Experimental Ophthalmology 11/2016 Go to the issue