Skip to main content
Top
Published in: BMC Ophthalmology 1/2020

Open Access 01-12-2020 | Diabetic Retinopathy | Research article

Assessment of retinal vascular oxygenation and morphology at stages of diabetic retinopathy in African Americans

Authors: Sarah L. Garvey, Maziyar M. Khansari, Xuejuan Jiang, Rohit Varma, Mahnaz Shahidi

Published in: BMC Ophthalmology | Issue 1/2020

Login to get access

Abstract

Background

Diabetic retinopathy (DR) is a microvascular complication of diabetes and a leading cause of blindness in working-age adults. The likelihood of visual impairment associated with DR is two-fold higher in the African-American (AA) compared to non-Hispanic white. Although alterations in retinal vessel oxygenation and morphology have been reported in DR, there is limited knowledge about these vascular changes in AA subjects. The purpose of the current study was to investigate alterations in retinal vascular oxygen saturation (SO2), vessel diameter (D) and tortuosity at severity stages of DR in AA subjects.

Methods

A nested case-control study of 56 AA subjects was conducted. Right eyes were grouped as non-diabetic (ND) (N = 26), no clinical DR (NDR) (N = 19), or moderate/severe non-proliferative DR (NPDR) (N = 11). Imaging was performed using a commercially available scanning laser ophthalmoscope. Images were analyzed to determine retinal arterial and venous SO2 (SO2A and SO2V), diameter (DA and DV), and vessel tortuosity index (VTI) (VTIA and VTIV).

Results

SO2V and DV were higher in NPDR compared to ND and NDR groups (P < 0.05). There were no significant differences in SO2A and DA among ND, NDR, and NPDR groups (P > 0.8). Maximum VTIA was higher in diabetics (NDR and NPDR) compared to non-diabetics (P < 0.03). There was no significant difference in maximum VTIV among the 3 groups (P = 0.5).

Conclusions

The findings advance our understanding of DR pathophysiology in the AA population and may propel identification of race-specific retinal vascular biomarkers for improved diagnosis and monitoring of DR.
Literature
1.
go back to reference Stitt AW, Curtis TM, Chen M, et al. The progress in understanding and treatment of diabetic retinopathy. Prog Retin Eye Res. 2016;51:156–86.PubMed Stitt AW, Curtis TM, Chen M, et al. The progress in understanding and treatment of diabetic retinopathy. Prog Retin Eye Res. 2016;51:156–86.PubMed
2.
go back to reference Aubert R. Diabetes in America: National Institute of Diabetes and Digestive and Kidney Diseases; 1995. Aubert R. Diabetes in America: National Institute of Diabetes and Digestive and Kidney Diseases; 1995.
3.
go back to reference Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124–36.PubMed Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124–36.PubMed
4.
go back to reference Hirsch IB, Brownlee M. Beyond hemoglobin A1c--need for additional markers of risk for diabetic microvascular complications. JAMA. 2010;303:2291–2.PubMed Hirsch IB, Brownlee M. Beyond hemoglobin A1c--need for additional markers of risk for diabetic microvascular complications. JAMA. 2010;303:2291–2.PubMed
5.
go back to reference Harris EL, Sherman SH, Georgopoulos A. Black-white differences in risk of developing retinopathy among individuals with type 2 diabetes. Diabetes Care. 1999;22:779–83.PubMed Harris EL, Sherman SH, Georgopoulos A. Black-white differences in risk of developing retinopathy among individuals with type 2 diabetes. Diabetes Care. 1999;22:779–83.PubMed
6.
go back to reference Weiss DM, Casten RJ, Leiby BE, et al. Effect of Behavioral intervention on dilated fundus examination rates in older African American individuals with diabetes mellitus: a randomized clinical trial. JAMA Ophthalmol. 2015;133:1005–12.PubMed Weiss DM, Casten RJ, Leiby BE, et al. Effect of Behavioral intervention on dilated fundus examination rates in older African American individuals with diabetes mellitus: a randomized clinical trial. JAMA Ophthalmol. 2015;133:1005–12.PubMed
7.
go back to reference Zhang X, Cotch MF, Ryskulova A, et al. Vision health disparities in the United States by race/ethnicity, education, and economic status: findings from two nationally representative surveys. Am J Ophthalmol. 2012;154:S53–62 e51.PubMedPubMedCentral Zhang X, Cotch MF, Ryskulova A, et al. Vision health disparities in the United States by race/ethnicity, education, and economic status: findings from two nationally representative surveys. Am J Ophthalmol. 2012;154:S53–62 e51.PubMedPubMedCentral
8.
go back to reference Lipton RB, Liao Y, Cao G, Cooper RS, McGee D. Determinants of incident non-insulin-dependent diabetes mellitus among blacks and whites in a national sample. The NHANES I epidemiologic follow-up study. Am J Epidemiol. 1993;138:826–39.PubMed Lipton RB, Liao Y, Cao G, Cooper RS, McGee D. Determinants of incident non-insulin-dependent diabetes mellitus among blacks and whites in a national sample. The NHANES I epidemiologic follow-up study. Am J Epidemiol. 1993;138:826–39.PubMed
9.
go back to reference Rasooly RS, Akolkar B, Spain LM, Guill MH, Del Vecchio CT, Carroll LE. The National Institute of Diabetes and Digestive and Kidney Diseases central repositories: a valuable resource for nephrology research. Clin J Am Soc Nephrol. 2015;10:710–5.PubMed Rasooly RS, Akolkar B, Spain LM, Guill MH, Del Vecchio CT, Carroll LE. The National Institute of Diabetes and Digestive and Kidney Diseases central repositories: a valuable resource for nephrology research. Clin J Am Soc Nephrol. 2015;10:710–5.PubMed
11.
go back to reference Baker RS. Diabetic retinopathy in African Americans: vision impairment, prevalence, incidence, and risk factors. Int Ophthalmol Clin. 2003;43:105–22.PubMed Baker RS. Diabetic retinopathy in African Americans: vision impairment, prevalence, incidence, and risk factors. Int Ophthalmol Clin. 2003;43:105–22.PubMed
12.
go back to reference Munoz B, West SK, Rubin GS, et al. Causes of blindness and visual impairment in a population of older Americans: the Salisbury eye evaluation study. Arch Ophthalmol. 2000;118:819–25.PubMed Munoz B, West SK, Rubin GS, et al. Causes of blindness and visual impairment in a population of older Americans: the Salisbury eye evaluation study. Arch Ophthalmol. 2000;118:819–25.PubMed
13.
go back to reference Grauslund J, Hodgson L, Kawasaki R, Green A, Sjolie AK, Wong TY. Retinal vessel calibre and micro- and macrovascular complications in type 1 diabetes. Diabetologia. 2009;52:2213–7.PubMed Grauslund J, Hodgson L, Kawasaki R, Green A, Sjolie AK, Wong TY. Retinal vessel calibre and micro- and macrovascular complications in type 1 diabetes. Diabetologia. 2009;52:2213–7.PubMed
14.
go back to reference Nguyen TT, Wang JJ, Wong TY. Retinal vascular changes in pre-diabetes and prehypertension: new findings and their research and clinical implications. Diabetes Care. 2007;30:2708–15.PubMed Nguyen TT, Wang JJ, Wong TY. Retinal vascular changes in pre-diabetes and prehypertension: new findings and their research and clinical implications. Diabetes Care. 2007;30:2708–15.PubMed
15.
go back to reference Yau JW, Kawasaki R, Islam FM, et al. Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian diabetes, obesity and lifestyle (AusDiab) study. Diabetologia. 2010;53:2042–5.PubMed Yau JW, Kawasaki R, Islam FM, et al. Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian diabetes, obesity and lifestyle (AusDiab) study. Diabetologia. 2010;53:2042–5.PubMed
16.
go back to reference Hartnett ME, Martiniuk D, Byfield G, Geisen P, Zeng G, Bautch VL. Neutralizing VEGF decreases tortuosity and alters endothelial cell division orientation in arterioles and veins in a rat model of ROP: relevance to plus disease. Invest Ophthalmol Vis Sci. 2008;49:3107–14.PubMedPubMedCentral Hartnett ME, Martiniuk D, Byfield G, Geisen P, Zeng G, Bautch VL. Neutralizing VEGF decreases tortuosity and alters endothelial cell division orientation in arterioles and veins in a rat model of ROP: relevance to plus disease. Invest Ophthalmol Vis Sci. 2008;49:3107–14.PubMedPubMedCentral
17.
go back to reference Paques M, Krivosic V, Girmens JF, Giraud C, Sahel J, Gaudric A. Decreased venous tortuosity associated with resolution of macular edema after intravitreal injection of triamcinolone. Retina. 2005;25:1099–101.PubMed Paques M, Krivosic V, Girmens JF, Giraud C, Sahel J, Gaudric A. Decreased venous tortuosity associated with resolution of macular edema after intravitreal injection of triamcinolone. Retina. 2005;25:1099–101.PubMed
18.
go back to reference Palochak CMA, Lee HE, Song J, Geng A, Linsenmeier RA, Burns SA, Fawzi AA. Retinal Blood Velocity and Flow in Early Diabetes and Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy. J Clin Med. 2019;8(8):1165. https://doi.org/10.3390/jcm8081165. Palochak CMA, Lee HE, Song J, Geng A, Linsenmeier RA, Burns SA, Fawzi AA. Retinal Blood Velocity and Flow in Early Diabetes and Diabetic Retinopathy Using Adaptive Optics Scanning Laser Ophthalmoscopy. J Clin Med. 2019;8(8):1165. https://​doi.​org/​10.​3390/​jcm8081165.
19.
go back to reference Pemp B, Schmetterer L. Ocular blood flow in diabetes and age-related macular degeneration. Can J Ophthalmol. 2008;43:295–301.PubMed Pemp B, Schmetterer L. Ocular blood flow in diabetes and age-related macular degeneration. Can J Ophthalmol. 2008;43:295–301.PubMed
20.
go back to reference Pournaras CJ, Rungger-Brandle E, Riva CE, Hardarson SH, Stefansson E. Regulation of retinal blood flow in health and disease. Prog Retin Eye Res. 2008;27:284–330.PubMed Pournaras CJ, Rungger-Brandle E, Riva CE, Hardarson SH, Stefansson E. Regulation of retinal blood flow in health and disease. Prog Retin Eye Res. 2008;27:284–330.PubMed
21.
go back to reference Kristinsson JK, Gottfredsdottir MS, Stefansson E. Retinal vessel dilatation and elongation precedes diabetic macular oedema. Br J Ophthalmol. 1997;81:274–8.PubMedPubMedCentral Kristinsson JK, Gottfredsdottir MS, Stefansson E. Retinal vessel dilatation and elongation precedes diabetic macular oedema. Br J Ophthalmol. 1997;81:274–8.PubMedPubMedCentral
22.
go back to reference Robison WG Jr, Laver NM, Jacot JL, Glover JP. Sorbinil prevention of diabetic-like retinopathy in the galactose-fed rat model. Invest Ophthalmol Vis Sci. 1995;36:2368–80.PubMed Robison WG Jr, Laver NM, Jacot JL, Glover JP. Sorbinil prevention of diabetic-like retinopathy in the galactose-fed rat model. Invest Ophthalmol Vis Sci. 1995;36:2368–80.PubMed
23.
go back to reference Sasongko MB, Wang JJ, Donaghue KC, et al. Alterations in retinal microvascular geometry in young type 1 diabetes. Diabetes Care. 2010;33:1331–6.PubMedPubMedCentral Sasongko MB, Wang JJ, Donaghue KC, et al. Alterations in retinal microvascular geometry in young type 1 diabetes. Diabetes Care. 2010;33:1331–6.PubMedPubMedCentral
24.
go back to reference Blair NP, Wanek J, Felder AE, et al. Retinal Oximetry and vessel diameter measurements with a commercially available scanning laser ophthalmoscope in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2017;58:5556–63.PubMedPubMedCentral Blair NP, Wanek J, Felder AE, et al. Retinal Oximetry and vessel diameter measurements with a commercially available scanning laser ophthalmoscope in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2017;58:5556–63.PubMedPubMedCentral
25.
go back to reference Ernst BJ, Garcia-Aguirre G, Oliver SC, Olson JL, Mandava N, Quiroz-Mercado H. Intravitreal bevacizumab versus panretinal photocoagulation for treatment-naive proliferative and severe nonproliferative diabetic retinopathy. Acta Ophthalmol. 2012;90:e573–4.PubMed Ernst BJ, Garcia-Aguirre G, Oliver SC, Olson JL, Mandava N, Quiroz-Mercado H. Intravitreal bevacizumab versus panretinal photocoagulation for treatment-naive proliferative and severe nonproliferative diabetic retinopathy. Acta Ophthalmol. 2012;90:e573–4.PubMed
26.
go back to reference Simunovic MP, Maberley DA. Anti-vascular endothelial growth factor therapy for proliferative diabetic retinopathy: a systematic review and meta-analysis. Retina. 2015;35:1931–42.PubMed Simunovic MP, Maberley DA. Anti-vascular endothelial growth factor therapy for proliferative diabetic retinopathy: a systematic review and meta-analysis. Retina. 2015;35:1931–42.PubMed
27.
go back to reference Burgansky-Eliash Z, Barak A, Barash H, et al. Increased retinal blood flow velocity in patients with early diabetes mellitus. Retina. 2012;32:112–9.PubMed Burgansky-Eliash Z, Barak A, Barash H, et al. Increased retinal blood flow velocity in patients with early diabetes mellitus. Retina. 2012;32:112–9.PubMed
28.
go back to reference Alibrahim E, Donaghue KC, Rogers S, et al. Retinal vascular caliber and risk of retinopathy in young patients with type 1 diabetes. Ophthalmology. 2006;113:1499–503.PubMed Alibrahim E, Donaghue KC, Rogers S, et al. Retinal vascular caliber and risk of retinopathy in young patients with type 1 diabetes. Ophthalmology. 2006;113:1499–503.PubMed
29.
go back to reference Falck A, Laatikainen L. Retinal vasodilation and hyperglycaemia in diabetic children and adolescents. Acta Ophthalmol Scand. 1995;73:119–24.PubMed Falck A, Laatikainen L. Retinal vasodilation and hyperglycaemia in diabetic children and adolescents. Acta Ophthalmol Scand. 1995;73:119–24.PubMed
30.
go back to reference Yau JW, Xie J, Lamoureux E, et al. Retinal microvascular calibre and risk of incident diabetes: the multi-ethnic study of atherosclerosis. Diabetes Res Clin Pract. 2012;95:265–74.PubMed Yau JW, Xie J, Lamoureux E, et al. Retinal microvascular calibre and risk of incident diabetes: the multi-ethnic study of atherosclerosis. Diabetes Res Clin Pract. 2012;95:265–74.PubMed
31.
go back to reference Khoobehi B, Firn K, Thompson H, Reinoso M, Beach J. Retinal arterial and venous oxygen saturation is altered in diabetic patients. Invest Ophthalmol Vis Sci. 2013;54:7103–6.PubMed Khoobehi B, Firn K, Thompson H, Reinoso M, Beach J. Retinal arterial and venous oxygen saturation is altered in diabetic patients. Invest Ophthalmol Vis Sci. 2013;54:7103–6.PubMed
32.
go back to reference Early Treatment Diabetic Retinopathy Study Research G. Grading diabetic retinopathy from stereoscopic color fundus photographs - an extension of the modified Airlie house classification: ETDRS report number 10. Ophthalmology. 2020;127:S99–S119. Early Treatment Diabetic Retinopathy Study Research G. Grading diabetic retinopathy from stereoscopic color fundus photographs - an extension of the modified Airlie house classification: ETDRS report number 10. Ophthalmology. 2020;127:S99–S119.
33.
go back to reference McKean-Cowdin R, Fairbrother-Crisp A, Torres M, et al. The African American eye disease study: design and methods. Ophthalmic Epidemiol. 2018;25:306–14.PubMedPubMedCentral McKean-Cowdin R, Fairbrother-Crisp A, Torres M, et al. The African American eye disease study: design and methods. Ophthalmic Epidemiol. 2018;25:306–14.PubMedPubMedCentral
34.
go back to reference Khansari MM, Garvey SL, Farzad S, Shi Y, Shahidi M. Relationship between retinal vessel tortuosity and oxygenation in sickle cell retinopathy. Int J Retina Vitreous. 2019;5:47.PubMedPubMedCentral Khansari MM, Garvey SL, Farzad S, Shi Y, Shahidi M. Relationship between retinal vessel tortuosity and oxygenation in sickle cell retinopathy. Int J Retina Vitreous. 2019;5:47.PubMedPubMedCentral
35.
go back to reference Felder AE, Wanek J, Blair NP, Shahidi M. Inner retinal oxygen extraction fraction in response to light flicker stimulation in humans. Invest Ophthalmol Vis Sci. 2015;56:6633–7.PubMedPubMedCentral Felder AE, Wanek J, Blair NP, Shahidi M. Inner retinal oxygen extraction fraction in response to light flicker stimulation in humans. Invest Ophthalmol Vis Sci. 2015;56:6633–7.PubMedPubMedCentral
36.
go back to reference Frangi A, Niessen W, Vincken K, Viergever M. Multiscale vessel enhancement filtering. International conference on medical image computing and computer-assisted intervention. Berlin: Springer; 1998. p. 130–7. Frangi A, Niessen W, Vincken K, Viergever M. Multiscale vessel enhancement filtering. International conference on medical image computing and computer-assisted intervention. Berlin: Springer; 1998. p. 130–7.
37.
go back to reference Khansari MM, O'Neill W, Lim J, Shahidi M. Method for quantitative assessment of retinal vessel tortuosity in optical coherence tomography angiography applied to sickle cell retinopathy. Biomed Opt Express. 2017;8:3796–806.PubMedPubMedCentral Khansari MM, O'Neill W, Lim J, Shahidi M. Method for quantitative assessment of retinal vessel tortuosity in optical coherence tomography angiography applied to sickle cell retinopathy. Biomed Opt Express. 2017;8:3796–806.PubMedPubMedCentral
38.
go back to reference Hammer M, Vilser W, Riemer T, et al. Diabetic patients with retinopathy show increased retinal venous oxygen saturation. Graefes Arch Clin Exp Ophthalmol. 2009;247:1025–30.PubMed Hammer M, Vilser W, Riemer T, et al. Diabetic patients with retinopathy show increased retinal venous oxygen saturation. Graefes Arch Clin Exp Ophthalmol. 2009;247:1025–30.PubMed
39.
go back to reference Kashani AH, Lopez Jaime GR, Saati S, Martin G, Varma R, Humayun MS. Noninvasive assessment of retinal vascular oxygen content among normal and diabetic human subjects: a study using hyperspectral computed tomographic imaging spectroscopy. Retina. 2014;34:1854–60.PubMedPubMedCentral Kashani AH, Lopez Jaime GR, Saati S, Martin G, Varma R, Humayun MS. Noninvasive assessment of retinal vascular oxygen content among normal and diabetic human subjects: a study using hyperspectral computed tomographic imaging spectroscopy. Retina. 2014;34:1854–60.PubMedPubMedCentral
40.
go back to reference Felder AE, Wanek J, Blair NP, et al. The effects of diabetic retinopathy stage and light flicker on inner retinal oxygen extraction fraction. Invest Ophthalmol Vis Sci. 2016;57:5586–92.PubMed Felder AE, Wanek J, Blair NP, et al. The effects of diabetic retinopathy stage and light flicker on inner retinal oxygen extraction fraction. Invest Ophthalmol Vis Sci. 2016;57:5586–92.PubMed
41.
go back to reference Kifley A, Wang JJ, Cugati S, Wong TY, Mitchell P. Retinal vascular caliber, diabetes, and retinopathy. Am J Ophthalmol. 2007;143:1024–6.PubMed Kifley A, Wang JJ, Cugati S, Wong TY, Mitchell P. Retinal vascular caliber, diabetes, and retinopathy. Am J Ophthalmol. 2007;143:1024–6.PubMed
42.
go back to reference Kifley A, Wang JJ, Cugati S, Wong TY, Mitchell P. Retinal vascular caliber and the long-term risk of diabetes and impaired fasting glucose: the Blue Mountains eye study. Microcirculation. 2008;15:373–7.PubMed Kifley A, Wang JJ, Cugati S, Wong TY, Mitchell P. Retinal vascular caliber and the long-term risk of diabetes and impaired fasting glucose: the Blue Mountains eye study. Microcirculation. 2008;15:373–7.PubMed
43.
go back to reference Klein R, Klein BE, Moss SE, Wong TY. Retinal vessel caliber and microvascular and macrovascular disease in type 2 diabetes: XXI: the Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology. 2007;114:1884–92.PubMed Klein R, Klein BE, Moss SE, Wong TY. Retinal vessel caliber and microvascular and macrovascular disease in type 2 diabetes: XXI: the Wisconsin epidemiologic study of diabetic retinopathy. Ophthalmology. 2007;114:1884–92.PubMed
44.
go back to reference Klein R, Klein BE, Moss SE, et al. The relation of retinal vessel caliber to the incidence and progression of diabetic retinopathy: XIX: the Wisconsin epidemiologic study of diabetic retinopathy. Arch Ophthalmol. 2004;122:76–83.PubMed Klein R, Klein BE, Moss SE, et al. The relation of retinal vessel caliber to the incidence and progression of diabetic retinopathy: XIX: the Wisconsin epidemiologic study of diabetic retinopathy. Arch Ophthalmol. 2004;122:76–83.PubMed
45.
go back to reference Klein R, Myers CE, Lee KE, Gangnon R, Klein BE. Changes in retinal vessel diameter and incidence and progression of diabetic retinopathy. Arch Ophthalmol. 2012;130:749–55.PubMedPubMedCentral Klein R, Myers CE, Lee KE, Gangnon R, Klein BE. Changes in retinal vessel diameter and incidence and progression of diabetic retinopathy. Arch Ophthalmol. 2012;130:749–55.PubMedPubMedCentral
46.
go back to reference Roy MS, Klein R, Janal MN. Retinal venular diameter as an early indicator of progression to proliferative diabetic retinopathy with and without high-risk characteristics in African Americans with type 1 diabetes mellitus. Arch Ophthalmol. 2011;129:8–15.PubMed Roy MS, Klein R, Janal MN. Retinal venular diameter as an early indicator of progression to proliferative diabetic retinopathy with and without high-risk characteristics in African Americans with type 1 diabetes mellitus. Arch Ophthalmol. 2011;129:8–15.PubMed
47.
go back to reference Tsai AS, Wong TY, Lavanya R, et al. Differential association of retinal arteriolar and venular caliber with diabetes and retinopathy. Diabetes Res Clin Pract. 2011;94:291–8.PubMed Tsai AS, Wong TY, Lavanya R, et al. Differential association of retinal arteriolar and venular caliber with diabetes and retinopathy. Diabetes Res Clin Pract. 2011;94:291–8.PubMed
48.
go back to reference Sasongko MB, Wong TY, Nguyen TT, Cheung CY, Shaw JE, Wang JJ. Retinal vascular tortuosity in persons with diabetes and diabetic retinopathy. Diabetologia. 2011;54:2409–16.PubMed Sasongko MB, Wong TY, Nguyen TT, Cheung CY, Shaw JE, Wang JJ. Retinal vascular tortuosity in persons with diabetes and diabetic retinopathy. Diabetologia. 2011;54:2409–16.PubMed
49.
go back to reference Curtis TM, Gardiner TA, Stitt AW. Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis? Eye (Lond). 2009;23:1496–508. Curtis TM, Gardiner TA, Stitt AW. Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis? Eye (Lond). 2009;23:1496–508.
50.
go back to reference Dobrin PB, Schwarcz TH, Baker WH. Mechanisms of arterial and aneurysmal tortuosity. Surgery. 1988;104:568–71.PubMed Dobrin PB, Schwarcz TH, Baker WH. Mechanisms of arterial and aneurysmal tortuosity. Surgery. 1988;104:568–71.PubMed
51.
go back to reference Gould DB, Phalan FC, van Mil SE, et al. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med. 2006;354:1489–96.PubMed Gould DB, Phalan FC, van Mil SE, et al. Role of COL4A1 in small-vessel disease and hemorrhagic stroke. N Engl J Med. 2006;354:1489–96.PubMed
52.
go back to reference Jensen RA, Sim X, Smith AV, et al. Novel genetic loci associated with retinal microvascular diameter. Circ Cardiovasc Genet. 2016;9:45–54.PubMed Jensen RA, Sim X, Smith AV, et al. Novel genetic loci associated with retinal microvascular diameter. Circ Cardiovasc Genet. 2016;9:45–54.PubMed
53.
go back to reference Tandon A, Chen CJ, Penman A, et al. African ancestry analysis and admixture genetic mapping for proliferative diabetic retinopathy in African Americans. Invest Ophthalmol Vis Sci. 2015;56:3999–4005.PubMedPubMedCentral Tandon A, Chen CJ, Penman A, et al. African ancestry analysis and admixture genetic mapping for proliferative diabetic retinopathy in African Americans. Invest Ophthalmol Vis Sci. 2015;56:3999–4005.PubMedPubMedCentral
54.
go back to reference Penman A, Hancock H, Papavasileiou E, et al. Risk factors for proliferative diabetic retinopathy in African Americans with type 2 diabetes. Ophthalmic Epidemiol. 2016;23:88–93.PubMedPubMedCentral Penman A, Hancock H, Papavasileiou E, et al. Risk factors for proliferative diabetic retinopathy in African Americans with type 2 diabetes. Ophthalmic Epidemiol. 2016;23:88–93.PubMedPubMedCentral
55.
go back to reference Penman A, Hoadley S, Wilson JG, Taylor HA, Chen CJ, Sobrin L. P-selectin plasma levels and genetic variant associated with diabetic retinopathy in African Americans. Am J Ophthalmol. 2015;159:1152–60 e1152.PubMedPubMedCentral Penman A, Hoadley S, Wilson JG, Taylor HA, Chen CJ, Sobrin L. P-selectin plasma levels and genetic variant associated with diabetic retinopathy in African Americans. Am J Ophthalmol. 2015;159:1152–60 e1152.PubMedPubMedCentral
56.
go back to reference Kristjansdottir JV, Hardarson SH, Halldorsson GH, Karlsson RA, Eliasdottir TS, Stefansson E. Retinal oximetry with a scanning laser ophthalmoscope. Invest Ophthalmol Vis Sci. 2014;55:3120–6.PubMed Kristjansdottir JV, Hardarson SH, Halldorsson GH, Karlsson RA, Eliasdottir TS, Stefansson E. Retinal oximetry with a scanning laser ophthalmoscope. Invest Ophthalmol Vis Sci. 2014;55:3120–6.PubMed
57.
go back to reference Vehmeijer WB, Magnusdottir V, Eliasdottir TS, Hardarson SH, Schalij-Delfos NE, Stefansson E. Retinal Oximetry with scanning laser ophthalmoscope in infants. PLoS One. 2016;11:e0148077.PubMedPubMedCentral Vehmeijer WB, Magnusdottir V, Eliasdottir TS, Hardarson SH, Schalij-Delfos NE, Stefansson E. Retinal Oximetry with scanning laser ophthalmoscope in infants. PLoS One. 2016;11:e0148077.PubMedPubMedCentral
Metadata
Title
Assessment of retinal vascular oxygenation and morphology at stages of diabetic retinopathy in African Americans
Authors
Sarah L. Garvey
Maziyar M. Khansari
Xuejuan Jiang
Rohit Varma
Mahnaz Shahidi
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Ophthalmology / Issue 1/2020
Electronic ISSN: 1471-2415
DOI
https://doi.org/10.1186/s12886-020-01566-y

Other articles of this Issue 1/2020

BMC Ophthalmology 1/2020 Go to the issue