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Correlation Between Visual Functions and Retinal Morphology in Eyes with Early and Intermediate Age-Related Macular Degeneration

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Correlation Between Visual Functions and Retinal Morphology in Eyes with Early and Intermediate Age-Related Macular Degeneration International Journal of Environmental Research and Public Health Article Correlation between Visual Functions and Retinal Morphology in Eyes with Early and Intermediate Age-Related Macular Degeneration Rituparna Ghoshal 1,2, Sharanjeet Sharanjeet-Kaur 1,*, Norliza Mohamad Fadzil 1, Haliza Abdul Mutalib 1, Somnath Ghosh 3, Nor Fariza Ngah 4 and Roslin Azni Abd Aziz 4 1 Optometry and Vision Science Program, Faculty of Health Sciences, University Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, Kuala Lumpur 50300, Malaysia; [email protected] (R.G.); [email protected] (N.M.F.); [email protected] (H.A.M.) 2 Department of Optometry, Supreme Institute of Management and Technology, Mankundu Hooghly 712123, West Bengal, India 3 Department of Allied Health Sciences, Brainware University, Barasat, Kalkata 700125, West Bengal, India; [email protected] 4 Department of Ophthalmology, Hospital Shah Alam, Persiaran Kayangan, Seksyen 7, Shah Alam 40000, Selangor, Malaysia; [email protected] (N.F.N.); [email protected] (R.A.A.A.) * Correspondence: [email protected] Received: 10 May 2020; Accepted: 28 July 2020; Published: 2 September 2020 Abstract: In early and intermediate age related macular degeneration (ARMD), visual acuity alone has failed to explain the complete variation of vision. The aim of the present study was to determine correlation between different visual functions and retinal morphology in eyes with early and intermediate ARMD. In this single center cross sectional study, patients diagnosed as early or intermediate ARMD in at least one eye were recruited. Visual functions measured were best- corrected distance visual acuity (DVA),near vision acuity (NVA),reading speed (RS), and contrast sensitivity (CS). Parameters such as thickness (RT) and volume (RV) of the retina, outer retinal layer thickness (ORLT) and volume (ORLV), outer nuclear layer thickness (ONLT) and volume (ONLV), retinal pigment epithelium layer-Bruch’s membrane complex thickness (RPET) and volume (RPEV) were assessed employing semi-auto segmentation method of Spectralis optical coherence tomography (OCT). Twenty-six eyes were evaluated. DVA, CS, and RS showed significantly good correlation with RPET, ONLT, and ONLV, whereas NVA showed good correlation with ONLV and RPET. The present study concluded that RS, CS, NVA, and DVA represent the morphological alteration in early stages and should be tested in clinical settings. ONLT, ONLV, and RPET morphological parameters can be employed as important biomarkers in diagnosis of early to intermediate ARMD. Keywords: early and intermediate ARMD; retinal layers morphology; visual functions 1. Introduction Age related macular degeneration (ARMD) is a chronic degenerative condition of the retina that leads to significant visual impairment in elderly population. By 2020, the projected number of ARMD worldwide is 196 million [1]. Early and intermediate stages of ARMD are characterized by deposition of drusen between retinal pigment epithelium (RPE) and Bruch’s membrane (BM) and/or alteration of retinal pigment epithelium in the macular area, whereas in later stages, the disease may progress to either geographic atrophy (GA) or neovascular ARMD (n-ARMD) [2,3]. Although there are different treatment options available for n-ARMD, cure for ARMD continues to be elusive. Continuous research effort is made to prevent the further progression of early and intermediate ARMD to late ARMD [4]. Int. J. Environ. Res. Public Health 2020, 17, 6379; doi:10.3390/ijerph17176379 www.mdpi.com/journal/ijerph Int. J. Environ. Res. Public Health 2020, 17, 6379 2 of 14 Introduction of optical coherence tomography (OCT) has revolutionized the in-vivo cross sectional examination of retinal diseases including ARMD, which was previously only possible in histological studies. In recent years, alterations in retinal layers’ morphology in early ARMD has been studied in detail to investigate the disease pathology, which is yet to be fully implicit. While, retinal pigment epithelium-Bruch’s membrane (RPE-BM) complex is reported to be significantly thicker in early and intermediate ARMD compared to normal controls [5], significant thinning of RPE/photoreceptor (PR) and outer nuclear layer (ONL) over drusen was observed [6,7]. Inner retinal layers including the retinal nerve fiber layer (RNFL) and ganglion cell layers (GCLs) are reported to be well preserved in the central fovea and parafovea, despite some alteration in outer retinal layer in early to intermediate ARMD [8]. However, with the increased severity of the disease, the inner plexiform layer becomes thinned [8]. The OCT findings are consistent with histopathological findings in ARMD that reported Bruch’s membrane (BM), retinal pigment epithelium (RPE) and photoreceptors are the structures that are primarily affected [9,10]. However, association of these morphological changes with the visual functions of early and intermediate ARMD eyes is not yet well established. Relationship between morphological changes seen in OCT and visual functions in early and intermediate ARMD will guide the clinician in finding out the validated morphological and visual parameters that are mostly affected by the disease process endorsing surrogate endpoint for clinical trials seeking management for dry ARMD. Furthermore, suitable morphological and visual parameters will assist in the detection, treatment, and long-term monitoring of this chronic degenerative disease. While drawing this correlation in a retrospective study, Pappuru et al. reported inner segment-outer segment of photoreceptor (IS-OS), and ONL to be moderately associated with high contrast distance visual acuity [11]. Furthermore, Karampelas et al. reported a significantly thicker mean RPE-BM complex in early and intermediate ARMD [5]. In this retrospective research, distance visual acuity measured with Snellen’s chart did not achieve a good correlation with RPE-BM complex (r = 0.363 in − central early treatment diabetic retinopathy study (ETDRS) subfield). Thus, both the studies found moderate correlation of selected OCT parameters with high contrast visual acuity that failed to explain the complete variation of vision, making the parameters less suitable to use as biomarker in early and intermediate ARMD. However, neither of the two studies considered other visual functions such as contrast sensitivity, near acuity or reading speed while drawing these correlations. High contrast visual acuity alone may not always provide complete information of visual damage caused by the disease. High contrast visual acuity may often miss the visual damage in many instances that are picked by contrast sensitivity and reading speed measurements [12–15]. Therefore, the objective of the present study was to determine the correlation between different visual functions and outer retinal layers thickness in eyes with early and intermediate ARMD. The outcome of the study could identify visual functions other than visual acuity that can reflect macular integrity as a whole, as well as provide correlation between the visual functions and altered retinal morphological parameters. 2. Materials and Methods 2.1. Study Design and Participants A single center cross-sectional observational study was conducted in an Ophthalmology Clinic of a public hospital of Malaysia, which is also an ARMD referral center. Patients diagnosed as early or intermediate ARMD in at least one eye were recruited for the study between December 2016 and July 2017. Eyes with medium sized drusen of more than 63 microns was considered as early ARMD, whereas eyes with at least one large drusen of >125 micron and/or any pigmentary abnormalities of the retina was considered as intermediate ARMD [3]. Lesions were assessed in the two-disc diameter of fovea in the study eyes. Eyes with any other retinal pathology including GA, n-ARMD, media opacity such as significant cataract, corneal opacity, glaucoma, amblyopia, or any neurological disease that may affect the normal visual functions were excluded. Int. J. Environ. Res. Public Health 2020, 17, 6379 3 of 14 Sample size estimation for single proportion for large population formula was used to calculate the sample size [16]. The p value of 0.07 was taken from a study by Cheung et al. [17]. The 95% confidence level Z value used is 1.96 and precision, D2 is 10%. 2 2 (Zα/2) p(1 p) (1.96) 0.07 (1 0.07) n = − = × × − = 25.0086 = 25 D2 0.12 Therefore, the sample size for the study is 25 patients. Ethical approval was obtained from Medical Research and Ethics Committee of National Medical Research Register (NMRR-16-1965-31826 (IIR)) and Universiti Kebangsaan Malaysia Research and Ethics Committee (UKM 1.5.3.5/244/NN-186-2014), which follows the tenants of Helsinki. Written consent was obtained from all the participants. 2.2. Visual Functions A 4-m early treatment diabetic retinopathy study (ETDRS) chart was used to measure the best- corrected distance visual acuity (DVA). Pelli-Robson chart was used at 1 m to measure the contrast sensitivity (CS). CS was recorded based on the contrast of last triplet in which two or three letters were correctly read. A standard illumination of 85 candela per square meter (measured using ISO Tech Digital Luxmeter) was maintained during the CS assessment. Near visual acuity (NVA) and reading speed (RS) were recorded using a Universiti Teknologi MARA (UiTM) Malay related-word reading chart [18]. Subjects were instructed to read the sentences loudly from the first line as fast as possible. They were asked to continue reading
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