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      Retinal Vessel Caliber Measurement Bias in Fundus Images in the Presence of the Central Light Reflex

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          Abstract

          Purpose

          To investigate the agreement between a fundus camera and a scanning laser ophthalmoscope in retinal vessel caliber measurements and to identify whether the presence of the central light reflex (CLR) explains potential discrepancies. 

          Methods

          For this cross-sectional study, we obtained fundus camera and scanning laser ophthalmoscope images from 85 eyes of 85 healthy individuals (aged 50–65 years) with different blood pressure status. We measured the central retinal artery equivalent (CRAE) and central retinal artery vein equivalent (CRVE) with the Knudtson–Parr–Hubbard algorithm and assessed the CLR using a semiautomatic grading method. We used Bland–Altman plots, 95% limits of agreement, and the two-way mixed effects intraclass correlation coefficient for consistency [ICC(3,1)] to describe interdevice agreement. We used multivariable regression to identify factors associated with differences in between-device measurements.

          Results

          The between-device difference in CRAE (9.5  µm; 95% confidence interval, 8.0–11.1  µm) was larger than the between-device difference in CRVE (2.9  µm; 95% confidence interval, 1.3–4.5  µm), with the fundus camera yielding higher measurements (both P < 0.001). The 95% fundus camera–scanning laser ophthalmoscope limits of agreement were –4.8 to 23.9  µm for CRAE and –12.0 to 17.8  µm for CRVE. The corresponding ICCs(3,1) were 0.89 (95% confidence interval, 0.83–0.92) and 0.91 (95% confidence interval, 0.86–0.94). The between-device CRAE difference was positively associated with the presence of a CLR ( P = 0.002).

          Conclusions

          Fundus cameras and scanning laser ophthalmoscopes yield correlated but not interchangeable caliber measurements. The CLR induces bias in arteriolar caliber in fundus camera images, compared with scanning laser ophthalmoscope images.

          Translational Relevance

          Refined measurements could yield better estimates of the association between retinal vessel caliber and ophthalmic or systemic disease.

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          Most cited references46

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          Split-spectrum amplitude-decorrelation angiography with optical coherence tomography

          Amplitude decorrelation measurement is sensitive to transverse flow and immune to phase noise in comparison to Doppler and other phase-based approaches. However, the high axial resolution of OCT makes it very sensitive to the pulsatile bulk motion noise in the axial direction. To overcome this limitation, we developed split-spectrum amplitude-decorrelation angiography (SSADA) to improve the signal-to-noise ratio (SNR) of flow detection. The full OCT spectrum was split into several narrower bands. Inter-B-scan decorrelation was computed using the spectral bands separately and then averaged. The SSADA algorithm was tested on in vivo images of the human macula and optic nerve head. It significantly improved both SNR for flow detection and connectivity of microvascular network when compared to other amplitude-decorrelation algorithms.
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            Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the Atherosclerosis Risk in Communities Study.

            To develop protocols to photograph and evaluate retinal vascular abnormalities in the Atherosclerosis Risk in Communities (ARIC) Study; to test reproducibility of the grading system; and to explore the relationship of these microvascular changes with blood pressure. Population-based, cross-sectional study. Among 4 examination centers, 11,114 participants (48-73 years of age) at their third triennial examination, after excluding persons with diabetes from this analysis. One eye of each participant was photographed by technicians with nonmydriatic fundus cameras. Reading center graders evaluated focal arteriolar narrowing, arteriovenous (AV) nicking, and retinopathy by examining slides on a light box and measured diameters of all vessels in a zone surrounding the optic disc on enhanced digitized images. To gauge generalized narrowing, vessel diameters were combined into central arteriolar and venular equivalents with formulas adjusting for branching, and the ratio of equivalents (A/V ratio) was calculated. Retinal vascular abnormalities, mean arteriolar blood pressure (MABP). Among 11,114 participants, photographs were obtained of 99%, with quality sufficient to perform retinal evaluations in 81%. In the 9040 subjects with usable photographs, A/V ratio (lower values indicate generalized arteriolar narrowing) ranged from 0.57 to 1.22 (median = 0.84, interquartile range = 0.10), focal arteriolar narrowing was found in 7%, AV nicking in 6%, and retinopathy in 4%. Because of attrition of subjects and limitation of methods, prevalence of abnormality was likely underestimated. Controlling for gender, race, age, and smoking status, these retinal changes were associated with higher blood pressure. For every 10-mmHg increase in MABP, A/V ratio decreased by 0.02 unit (P < 0.0001), focal arteriolar narrowing had an odds ratio (OR) of 2.00 (95% confidence interval [CI] = 1.87-2.14), AV nicking had an OR of 1.25 (95% CI = 1.16-1.34), and retinopathy had an OR of 1.25 (95% CI = 1.15-1.37). For any degree of generalized narrowing, individuals with focal narrowing had MABP approximately 8 mmHg higher than those without (P < 0.0001). Masked replicate assessment of a sample found the following reproducibility: for A/V ratio, correlation coefficient = 0.79 and median absolute difference = 0.03; for focal arteriolar narrowing, kappa = 0.45; for AV nicking, kappa = 0.61; and for retinopathy, kappa = 0.89. Protocols have been developed for nonmydriatic fundus photography and for evaluation of retinal vascular abnormalities. Several microvascular changes were significantly associated with higher blood pressure; follow-up will show whether these are predictive of later cerebrovascular or cardiovascular disease independently of other known risk factors.
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              Revised formulas for summarizing retinal vessel diameters.

              Background/Purpose. Recent findings suggest that an objective assessment of retinal vessel caliber from fundus photographs provide information about the association of microvascular characteristics with macrovascular disease. Current methods used to quantify retinal vessel caliber, introduced by Parr(1,2) and Hubbard,(3) are not independent of scale and are affected by the number of vessels. To improve upon these methods we introduce revised formulas for quantifying vessel caliber. Methods. Revised formulas were estimated using retinal vessel measurements from 44 young adults free of hypertension and diabetes. Comparisons between the two methods were done using digitized photographs from 4926 participants at the baseline examination of the Beaver Dam Eye Study (BDES), an ongoing population-based cohort study initiated in 1987. Individual arterioles and venules were measured using semi-automated computer software from which summary measures were calculated. Results. Correlation coefficients between the Parr-Hubbard and revised formulas were high (Pearson correlation coefficients ranging from 0.94 to 0.98). Both arteriolar and venular caliber significantly increased with an increasing number of vessels measured using the Parr-Hubbard formulas (p 0.50). Conclusions. We describe revised formulas for summarizing retinal vessel diameters measured from fundus photographs to be used in future studies and analyses. The revised formulas correlate highly with the previously used Parr-Hubbard formulas, but offer the advantages of being more robust against variability in the number of vessels observed, being independent of image scale, and being easier to implement.
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                Author and article information

                Journal
                Transl Vis Sci Technol
                Transl Vis Sci Technol
                TVST
                Translational Vision Science & Technology
                The Association for Research in Vision and Ophthalmology
                2164-2591
                14 July 2023
                July 2023
                : 12
                : 7
                : 16
                Affiliations
                [1 ]Department of Ophthalmology, University of Groningen, University Medical Center Groningen, Groningen, the Netherlands
                [2 ]Graduate School of Medical Sciences, Research School of Behavioural and Cognitive Neurosciences, University of Groningen, Groningen, the Netherlands
                Author notes
                [* ] Correspondence: K. Pappelis, Department of Ophthalmology, University Medical Center Groningen, PO Box 30.001, 9700 RB, Groningen, the Netherlands. e-mail: k.pappelis@ 123456rug.nl
                Article
                TVST-23-5455
                10.1167/tvst.12.7.16
                10353742
                37450282
                5c550e50-b1ad-4beb-9e7b-9faea03372c0
                Copyright 2023 The Authors

                This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

                History
                : 16 June 2023
                : 17 January 2023
                Page count
                Pages: 11
                Categories
                Retina
                Retina

                fundus imaging,scanning laser ophthalmoscope,retinal vessel caliber,central light reflex,hypertension

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