Validity and reproducibility of retinal arteriole and venule diameter measurements
ELSA-Brasil study. A cross‑sectional study
Keywords:
Microvessels, Retinal artery, Retinal vein, Reproducibility of resultsAbstract
BACKGROUND: Investigation of alterations to retinal microvasculature may contribute towards understanding the role of such changes in the pathophysiology of several chronic non-communicable diseases. The objective here was to evaluate the validity and reproducibility of retinal arteriole and venule diameter measurements made by Brazilian Longitudinal Study of Adult Health (ELSA-Brasil) graders. DESIGN AND SETTING: Cross-sectional study at six teaching and research institutions. METHODS: To evaluate validity, each of 25 retinal images from the University of Wisconsin (gold standard) was measured by five ELSA-Brasil graders. To evaluate reproducibility, 105 images across the spectrum of vessel diameters were selected from 12,257 retinal images that had been obtained between 2010 and 2012, and each image was reexamined by the same grader and by an independent grader. All measurements were made using the Interactive Vessel Analysis (IVAN) software. Bland-Altman plots, paired t tests and intraclass correlation coefficients (ICCs) were analyzed. RESULTS: Mean differences between ELSA-Brasil and gold-standard readings were 0.16 μm (95% CI -0.17‑0.50; P = 0.31) for central retinal artery equivalent (CRAE), -0.21 μm (95% CI -0.56-0.14; P = 0.22) for central retinal vein equivalent (CRVE) and 0.0005 (95% CI -0.008-0.009; P = 0.55) for arteriole/venule ratio (AVR). Intragrader ICCs were 0.77 (95% CI 0.67-0.86) for CRAE, 0.90 (95% CI 0.780.96) for CRVE and 0.70 (0.55‑0.83) for AVR. Intergrader ICCs were 0.75 (95% CI 0.64-0.85) for CRAE, 0.90 (95% CI 0.79-0.96) for CRVE and 0.68 (95% CI 0.55‑0.82) for AVR. CONCLUSIONS: Retinal microvascular diameter measurements are valid and present moderate to high intra and intergrader reproducibility in ELSA-Brasil.
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References
Hubbard LD, Brothers RJ, King WN, et al. Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the Atherosclerosis Risk in Communities Study. Ophthalmology. 1999;106(12):2269-80. PMID: 10599656.
Yip WF, Sabanayagam C, Teo BW, et al. Retinal Microvascular Abnormalities and Risk of Renal Failure in Asian Populations. PLoS One. 2015;10(2):e0118076. PMID: 25658337; doi:10.1371/journal.pone.0118076.
Yang X, Deng Y, Gu H, et al. Relationship of retinal vascular calibre and diabetic retinopathy in Chinese patients with type 2 diabetes mellitus: the Desheng Diabetic Eye Study. Br J Ophthalmol. 2016;100(10):1359-65. PMID: 26823397; doi: 10.1136/bjophthalmol-2014-306078.
Yuan Y, Ikram MK, Vingerling JR, et al. Retinal vascular caliber and metabolic syndrome in a Chinese population. Intern Med J. 2012;42(9):1014-22. PMID: 21395957; doi: 10.1111/j.1445-5994.2011.02470.x.
Wong TY, Klein R, Klein BE, et al. Retinal microvascular abnormalities and their relationship with hypertension, cardiovascular disease, and mortality. Surv Ophthalmol. 2001;46(1):59-80. PMID: 11525792; doi: 10.1016/S0039-6257(01)00234-X.
Wong TY, Klein R, Nieto FJ, et al. Retinal microvascular abnormalities and 10-year cardiovascular mortality: a population-based case-control study. Ophthalmology. 2003;110(5):933-40. PMID: 12750093; doi: 10.1016/S0161-6420(03)00084-8.
Cheung CYL, Ikram MK, Klein R, Wong TY. The clinical implications of recent studies on the structure and function of the retinal microvasculature in diabetes. Diabetologia. 2015;58(5):871-85. PMID: 25669631; doi: 10.1007/s00125-015-3511-1.
Wong TY, Kamineni A, Klein R, et al. Quantitative retinal venular caliber and risk of cardiovascular disease in older persons: the cardiovascular health study. Arch Intern Med. 2006;166(21):2388-94. PMID: 17130394; doi: 10.1001/archinte.166.21.2388.
Wong TY, Knudtson MD, Klein R, Klein BEK, Hubbard LD. A prospective cohort study of retinal arteriolar narrowing and mortality. Am J Epidemiol. Oxford University Press. 2004;159(9):819-25. PMID: 15105174; doi: 10.1001/archinte.166.21.2388.
Wong TY, Hubbard LD, Klein R, et al. Retinal microvascular abnormalities and blood pressure in older people: the Cardiovascular Health Study. Br J Ophthalmol. 2002;86(9):1007-13. PMID: 12185128.
Cheung CYL, Reich D, Wong TY, et al. Admixture mapping scans identify a locus affecting retinal vascular caliber in hypertensive African Americans: the Atherosclerosis Risk in Communities (ARIC) study. PLoS Genet. 2010;6(4):e1000908. PMID: 20419148; doi: 10.1371/journal.pgen.1000908.
Ding J, Wai KL, McGeechan K, et al. Retinal vascular caliber and the development of hypertension: a meta-analysis of individual participant data. J Hypertens. 2014;32(2):207-15. PMID: 24322199; doi: 10.1097/HJH.0b013e32836586f4.
Moss HE. Retinal Vascular Changes are a Marker for Cerebral Vascular Diseases. Curr Neurol Neurosci Rep. 2015;15(7):40. PMID: 26008809; doi: 10.1007/s11910-015-0561-1.
Sabanayagam C, Lye WK, Klein R, et al. Retinal microvascular calibre and risk of diabetes mellitus: a systematic review and participant-level meta-analysis. Diabetologia. 2015;58(11):2476-85. PMID: 26232097; doi: 10.1007/s00125-015-3717-2.
Aquino EM, Barreto SM, Bensenor IM, et al. Brazilian Longitudinal Study of Adult health (ELSA-Brasil): objectives and design. Am J Epidemiol. 2012;175(4):315-24. PMID: 22234482; doi: 10.1093/aje/kwr294.
Lotufo PA. Construção do Estudo Longitudinal de Saúde do Adulto (ELSA-Brasil) [Setting up the Longitudinal Study for Adult Health (ELSA-Brasil)]. Rev Saúde Pública. 2013;47Supl 2:3-9. PMID: 24346715; doi: 10.1590/S0034-8910.2013047S20002.
Schmidt MI, Griep RH, Passos VM, et al. Estratégias e desenvolvimento de garantia e controle de qualidade no ELSA-Brasil [Strategies and development of quality assurance and control in the ELSA-Brasil]. Rev Saúde Pública. 2013;47Supl 2:105-12. PMID: 24346727; doi: 10.1590/S0034-8910.2013047003889.
Pauli TW, Gangaputra S, Hubbard LD, et al. Effect of image compression and resolution on retinal vascular caliber. Invest Ophthalmol Vis Sci. 2012;53(9):5117-23. PMID: 22736618; doi: 10.1167/iovs.12-9643.
Couper DJ, Klein R, Hubbard LD, et al. Reliability of retinal photography in the assessment of retinal microvascular characteristics: the Atherosclerosis Risk in Communities Study. Am J Ophthalmol. 2002;133(1):78-88. PMID: 11755842; doi: 10.1016/S0002-9394(01)01315-0.
Knudtson MD, Lee KE, Hubbard LD, et al. Revised formulas for summarizing retinal vessel diameters. Curr Eye Res. 2003;27(3):143-9. PMID: 14562179. doi: 10.1076/ceyr.27.3.143.16049.
Wong TY, Knudtson MD, Klein R, et al. Computer-assisted measurement of retinal vessel diameters in the Beaver Dam Eye Study: methodology, correlation between eyes, and effect of refractive errors. Ophthalmology. 2004;111(6):1183-90. PMID: 15177969; doi: 10.1016/j.ophtha.2003.09.039.
Searle SR. An overview of variance component estimation. Metrika. 1995;42(1):215-30. doi: 10.1007/BF01894301.
Efron B, Tibshirani RJ. An Introduction to the Bootstrap. New York: Chapman & Hall; 1993. ISBN-10: 0412042312; ISBN-13: 978-0412042317
Hinkle DE, Wiersma W, Jurs SG. Applied Statistics for the Behavioral Sciences. 5th ed. Boston: Houghton Mifflin; 2003. ISBN-10: 0495808857; ISBN-13: 9780495808855.
Wong TY, Klein R, Klein BEK, Meuer SM, Hubbard LD. Retinal vessel diameters and their associations with age and blood pressure. Investig Ophthalmol Vis Sci. 2003;44(11):4644-50. PMID: 14578380; doi: 10.1167/iovs.03-0079.
Wong TY, Klein R, Sharrett AR, et al. Retinal arteriolar narrowing and risk of diabetes mellitus in middle-aged persons. JAMA. 2002;287(19):2528-33. PMID: 12020333; doi: 10.1001/jama.287.19.2528.
Cheung N, Islam FMA, Saw SM, et al. Distribution and associations of retinal vascular caliber with ethnicity, gender, and birth parameters in young children. Investig Ophthalmol Vis Sci. 2007;48(3):1018-24. PMID: 17325141; doi: 10.1167/iovs.06-0978.
Bhuiyan A, Karmakar C, Kawasaki R, et al. Retinal artery and venular caliber grading: a semi-automated evaluation tool. Comput Biol Med. 2014;44(1):1-9. PMID: 24377683; doi: 10.1016/j.compbiomed.2013.07.018.
Wong TY, Islam FM, Klein R, et al. Retinal vascular caliber, cardiovascular risk factors, and inflammation: the multi-ethnic study of atherosclerosis (MESA). Invest Ophthalmol Vis Sci. 2006;47(6):2341-50. PMID: 16723443; doi: 10.1167/iovs.05-1539.
Wong TY, Klein R, Sharrett AR, et al. The prevalence and risk factors of retinal microvascular abnormalities in older persons: The Cardiovascular Health Study. Ophthalmology. 2003;110(4):658-66. PMID: 12689883; doi: 10.1016/S0161-6420(02)01931-0.
Cheung CYL, Kamran Ikram M, Chen C, Wong TY. Imaging retina to study dementia and stroke. Prog Retin Eye Res. 2017;57:89-107. PMID: 28057562; doi: 10.1016/j.preteyeres.2017.01.00.
Cheung CY, Ong YT, Ikram MK, Chen C, Wong TY. Retinal microvasculature in Alzheimer's disease. J Alzheimers Dis. 2014;42 Suppl 4:S339-52. PMID: 25351108; doi: 10.3233/JAD-141596.
Kee AR, Wong TY, Li LJ. Retinal vascular imaging technology to monitor disease severity and complications in type 1 diabetes mellitus: A systematic review. Microcirculation. 2017;24(2). PMID: 27749000; doi: 10.1111/micc.12327.
Agladioglu K, Pekel G, Citisli V, Yagci R. Choroidal thickness and retinal vascular caliber correlations with internal carotid artery Doppler variables. J Clin Ultrasound. 2015;43(9):567-72. PMID: 25802013; doi: 10.1002/jcu.22269.
Beltrami-Moreira M, Qi L, Maestri MK, et al. Association between plasma adiponectin and arteriolar vessel caliber among elderly hypertensive subjects. J Am Soc Hypertens. 2015;9(8):620-7. PMID: 26116458; doi: 10.1016/j.jash.2015.
