Publications by authors named "Ann E Elsner"

52 Publications

Imaging the Retinal Vasculature.

Annu Rev Vis Sci 2021 Sep 25;7:129-153. Epub 2021 Jun 25.

Indiana University School of Optometry, Bloomington, Indiana 47405, USA; email:

Advances in retinal imaging are enabling researchers and clinicians to make precise noninvasive measurements of the retinal vasculature in vivo. This includes measurements of capillary blood flow, the regulation of blood flow, and the delivery of oxygen, as well as mapping of perfused blood vessels. These advances promise to revolutionize our understanding of vascular regulation, as well as the management of retinal vascular diseases. This review provides an overview of imaging and optical measurements of the function and structure of the ocular vasculature. We include general characteristics of vascular systems with an emphasis on the eye and its unique status. The functions of vascular systems are discussed, along with physical principles governing flow and its regulation. Vascular measurement techniques based on reflectance and absorption are briefly introduced, emphasizing ways of generating contrast. One of the prime ways to enhance contrast within vessels is to use techniques sensitive to the motion of cells, allowing precise measurements of perfusion and blood velocity. Finally, we provide a brief introduction to retinal vascular diseases.
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http://dx.doi.org/10.1146/annurev-vision-093019-113719DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8446336PMC
September 2021

Quantifying frequency content in cross-sectional retinal scans of diabetics vs. controls.

PLoS One 2021 18;16(6):e0253091. Epub 2021 Jun 18.

School of Optometry, Indiana University, Bloomington, Indiana, United States of America.

Purpose: To examine subtle differences in the structure of diabetic vs. control retinas.

Methods: Spectral-domain optical coherence tomography (SD-OCT) images were compared for the retinas of 33 diabetic subjects who did not have clinical evidence of diabetic macular edema and age-matched controls, with central macular thicknesses of 275 and 276 microns, respectively. Cross-sectional retinal images through the fovea, called B-scans, were analyzed for spatial frequency content. The B-scans were processed to remove and smooth the portions of the retinal image not within regions of interest in the retina. The remaining retinal images were then quantified using a Fast Fourier Transform (FFT) approach that provided amplitude as a function of spatial frequency.

Results: The FFT analysis showed that diabetic retinas had spatial frequency content with significantly higher power compared to control retinas particularly for a deeper fundus layer at mid-range spatial frequencies, ranging from p = 0.0030 to 0.0497 at 16.8 to 18.2 microns/cycle. There was lower power at higher spatial frequencies, ranging from p = 0.0296 and 0.0482 at 27.4 and 29.0 microns/cycle. The range of mid-range frequencies corresponds to the sizes of small blood vessel abnormalities and hard exudates. Retinal thickness did not differ between the two groups.

Conclusions: Diabetic retinas, although not thicker than controls, had subtle but quantifiable pattern changes in SD-OCT images particularly in deeper fundus layers. The size range and distribution of this pattern in diabetic eyes were consistent with small blood vessel abnormalities and leakage of lipid and fluid. Feature-based biomarkers may augment retinal thickness criteria for management of diabetic eye complications, and may detect early changes.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0253091PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8213050PMC
June 2021

Cones in ageing and harsh environments: the neural economy hypothesis.

Ophthalmic Physiol Opt 2020 03 4;40(2):88-116. Epub 2020 Feb 4.

Indiana University, Bloomington, USA.

Purpose: Cones are at great risk in a wide variety of retinal diseases, especially when there is a harsh microenvironment and retinal pigment epithelium is damaged. We provide established and new methods for assessing cones and retinal pigment epithelium, together with new results. We investigated conditions under which cones can be imaged and could guide light, despite the proximity of less than ideal retinal pigment epithelium.

Recent Findings: We used a variety of imaging methods to detect and localise damage to the retinal pigment epithelium. As age-related macular degeneration is a particularly widespread disease, we imaged clinical hallmarks: drusen and hyperpigmentation. Using near infrared light provided improved imaging of the deeper fundus layers. We compared confocal and multiply scattered light images, using both the variation of detection apertures and polarisation analysis. We used optical coherence tomography to examine distances between structures and thickness of retinal layers, as well as identifying damage to the retinal pigment epithelium. We counted cones using adaptive optics scanning laser ophthalmoscopy. We compared the results of five subjects with geographic atrophy to data from a previous normative ageing study. Using near infrared imaging and layer analysis of optical coherence tomography, the widespread aspect of drusen became evident. Both multiply scattered light imaging and analysis of the volume in the retinal pigment epithelial layer from the optical coherence tomography were effective in localising drusen and hyperpigmentation beneath the photoreceptors. Cone photoreceptors in normal older eyes were shorter than in younger eyes. Cone photoreceptors survived in regions of atrophy, but with greatly reduced and highly variable density. Regular arrays of cones were found in some locations, despite abnormal retinal pigment epithelium. For some subjects, the cone density was significantly greater than normative values in some retinal locations outside the atrophy.

Summary: The survival of cones within atrophy is remarkable. The unusually dense packing of cones at some retinal locations outside the atrophy indicates more fluidity in cone distribution than typically thought. Together these findings suggest strategies for therapy that includes preserving cones.
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http://dx.doi.org/10.1111/opo.12670DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7155023PMC
March 2020

Distances From Capillaries to Arterioles or Venules Measured Using OCTA and AOSLO.

Invest Ophthalmol Vis Sci 2019 05;60(6):1833-1844

Indiana University School of Optometry, Bloomington, Indiana, United States.

Purpose: To investigate distances from retinal capillaries to arterioles or venules noninvasively.

Methods: An adaptive optics scanning laser ophthalmoscope (AOSLO) and optical coherence tomography angiography (OCTA) imager acquired detailed maps of retinal vasculature. Using OCTA, we quantified the distance from the edge of an arteriole or venule to the middle of the nearest capillaries (periarteriole or perivenule capillary-free zones, respectively) within the superficial vascular plexus of 20 young healthy subjects with normal axial lengths. These distances were compared to AOSLO images for three subjects. We tested the relation between the peripheral capillary-free zones and FAZ horizontal, vertical, effective diameters, and asymmetry indices in the deep vascular plexus. We examined enlargement with OCTA of capillary-free zones in a type 2 diabetic patient.

Results: The periarteriole capillary-free zone (67.2 ± 25.3 μm) was readily visible and larger than the perivenule capillary-free zone (42.7 ± 14.4 μm), F(1, 998) = 771, P < 0.0001. The distance from foveal center (P = 0.003) and diameter (P = 0.048) were predictive of perivenule capillary-free zone values. OCTA and AOSLO corresponded for arterioles. FAZ effective diameter was positively associated with asymmetry indices, r = 0.49, P = 0.028, but not peripheral capillary-free zones, although focal enlargements were found in a diabetic patient.

Conclusions: For normal retinas, periarteriole and perivenule capillary-free zones are readily visible with OCTA and AOSLO. Periarteriole capillary-free zones were larger, consistent with arterioles carrying oxygen rich blood that diffuses to support the retina.
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http://dx.doi.org/10.1167/iovs.18-25294DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6892442PMC
May 2019

Central Macular Thickness in Diabetic Patients: A Sex-based Analysis.

Optom Vis Sci 2019 04;96(4):266-275

School of Optometry, University of California Berkeley, Berkeley, California.

Significance: The pathological changes in clinically significant diabetic macular edema lead to greater retinal thickening in men than in women. Therefore, male sex should be considered a potential risk factor for identifying individuals with the most severe pathological changes. Understanding this excessive retinal thickening in men may help preserve vision.

Purpose: The purpose of this study was to investigate the sex differences in retinal thickness in diabetic patients. We tested whether men with clinically significant macular edema had even greater central macular thickness than expected from sex differences without significant pathological changes. This study also aimed to determine which retinal layers contribute to abnormal retinal thickness.

Methods: From 2047 underserved adult diabetic patients from Alameda County, CA, 142 patients with clinically significant macular edema were identified by EyePACS-certified graders using color fundus images (Canon CR6-45NM). First, central macular thickness from spectral domain optical coherence tomography (iVue; Optovue Inc.) was compared in 21 men versus 21 women without clinically significant macular edema. Then, a planned comparison contrasted the greater values of central macular thickness in men versus women with clinically significant macular edema as compared with those without. Mean retinal thickness and variability of central macular layers were compared in men versus women.

Results: Men without clinically significant macular edema had a 12-μm greater central macular thickness than did women (245 ± 21.3 and 233 ± 13.4 μm, respectively; t40 = -2.18, P = .04). Men with clinically significant macular edema had a 67-μm greater central macular thickness than did women (383 ± 48.7 and 316 ± 60.4 μm, P < .001); that is, men had 55 μm or more than five times more (t20 = 2.35, P = .02). In men, the outer-nuclear-layer thickness was more variable, F10,10 = 9.34.

Conclusions: Underserved diabetic men had thicker retinas than did women, exacerbated by clinically significant macular edema.
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http://dx.doi.org/10.1097/OPX.0000000000001363DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6445750PMC
April 2019

Near-infrared polarimetric imaging and changes associated with normative aging.

J Opt Soc Am A Opt Image Sci Vis 2018 Sep;35(9):1487-1495

With aging, the human retina undergoes cell death and additional structural changes that can increase scattered light. We quantified the effect of normative aging on multiply scattered light returning from the human fundus. As expected, there was an increase of multiply scattered light associated with aging, and this is consistent with the histological changes that occur in the fundus of individuals before developing age-related macular degeneration. This increase in scattered light with aging cannot be attributed to retinal reflectivity, anterior segment scatter, or pupil diameter.
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http://dx.doi.org/10.1364/JOSAA.35.001487DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6640646PMC
September 2018

Adaptive optics imaging of the human retina.

Prog Retin Eye Res 2019 01 27;68:1-30. Epub 2018 Aug 27.

800E. Atwater S, School of Optometry, Indiana University, Bloomington, IN, United States.

Adaptive Optics (AO) retinal imaging has provided revolutionary tools to scientists and clinicians for studying retinal structure and function in the living eye. From animal models to clinical patients, AO imaging is changing the way scientists are approaching the study of the retina. By providing cellular and subcellular details without the need for histology, it is now possible to perform large scale studies as well as to understand how an individual retina changes over time. Because AO retinal imaging is non-invasive and when performed with near-IR wavelengths both safe and easily tolerated by patients, it holds promise for being incorporated into clinical trials providing cell specific approaches to monitoring diseases and therapeutic interventions. AO is being used to enhance the ability of OCT, fluorescence imaging, and reflectance imaging. By incorporating imaging that is sensitive to differences in the scattering properties of retinal tissue, it is especially sensitive to disease, which can drastically impact retinal tissue properties. This review examines human AO retinal imaging with a concentration on the use of the Adaptive Optics Scanning Laser Ophthalmoscope (AOSLO). It first covers the background and the overall approaches to human AO retinal imaging, and the technology involved, and then concentrates on using AO retinal imaging to study the structure and function of the retina.
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http://dx.doi.org/10.1016/j.preteyeres.2018.08.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6347528PMC
January 2019

Subtle changes in diabetic retinas localised in 3D using OCT.

Ophthalmic Physiol Opt 2018 09 26;38(5):477-491. Epub 2018 Jul 26.

Indiana University School of Optometry, Bloomington, USA.

Purpose: To detect and localise subtle changes in retinas of diabetic patients who clinically have no diabetic retinopathy (DR) or non-proliferative DR (NPDR) as compared to age- and sex- matched controls. Spectral Domain Optical Coherence Tomography (SD-OCT) and software to examine all retinal layers, including deeper layers, were used to quantify foveal avascular zone size and inner and outer retinal layer thicknesses, as well as to detect axial location of prominent lesions.

Methods: Diabetic subjects, 19 total with 16 having no DR and three having non-proliferative retinopathy, were matched with 19 controls with respect to age and sex. Macular-centred SD-OCT grids of 20 × 15° were taken with the Spectralis. En face or transverse images were generated from the SD-OCT data by automatically segmenting all retinal layers. The transverse images were investigated for foveal avascular zone (FAZ) size, retinal vessel calibre, and structural changes. The size of the FAZ was compared for diabetics vs controls using vendor software and manual marking in Photoshop. Inner retinal layer (IRL ) and outer nuclear layer (ONL ) thicknesses at the margins of the FAZ were measured using vendor software.

Results: The FAZ area was larger for diabetics (mean ± S.D. = 0.388 ± 0.074 mm ) than controls (0.243 ± 0.113 mm ), t = 5.27, p < 0.0001, using vendor software. The mean IRL was thicker for the diabetics (86.8 ± 14.5 μm) than controls (65.2 ± 16.3 μm), t = 4.59, p = 0.00023, despite lack of exudation by clinical exam. There was no significant association between FAZ area and mean IRL for the diabetics, r = 0.099, p = 0.69. Vessels not clinically detected were visible in the NFL transverse image of most diabetics, especially for a mild NPDR patient. A prominent lesion found in the en face infra-red image of a mild NPDR subject was localised in the photoreceptor layer by SD-OCT, as well as additional outer retinal changes in other subjects.

Conclusions: Our results demonstrate changes in inner and outer diabetic retinas not readily detectable by clinical exam. IRL had not thinned at the margins of the large FAZs, indicating neural mass did not yet decrease despite potential ischemia.
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http://dx.doi.org/10.1111/opo.12578DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6202252PMC
September 2018

Confocal Retinal Imaging Using a Digital Light Projector with a Near Infrared VCSEL Source.

Proc SPIE Int Soc Opt Eng 2018 Feb;10546

Aeon Imaging, LLC, 501 S Madison St., Ste. 103, Bloomington, IN, USA 47403-2452.

A custom near infrared VCSEL source has been implemented in a confocal non-mydriatic retinal camera, the Digital Light Ophthalmoscope (DLO). The use of near infrared light improves patient comfort, avoids pupil constriction, penetrates the deeper retina, and does not mask visual stimuli. The DLO performs confocal imaging by synchronizing a sequence of lines displayed with a digital micromirror device to the rolling shutter exposure of a 2D CMOS camera. Real-time software adjustments enable multiply scattered light imaging, which rapidly and cost-effectively emphasizes drusen and other scattering disruptions in the deeper retina. A separate 5.1″ LCD display provides customizable visible stimuli for vision experiments with simultaneous near infrared imaging.
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http://dx.doi.org/10.1117/12.2290286DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5995569PMC
February 2018

Polarization Variability in Age-related Macular Degeneration.

Optom Vis Sci 2018 04;95(4):277-291

Indiana University School of Optometry, Bloomington,

Significance: Age-related macular degeneration (AMD) is a leading cause of irreversible vision loss. Complementary imaging techniques can be used to better characterize and quantify pathological changes associated with AMD. By assessing specific light-tissue interactions, polarization-sensitive imaging can be used to detect tissue disruption early in the disease process.

Purpose: The aim of this study was to compare variability in central macular polarization properties in patients with nonexudative AMD and age-matched control subjects.

Methods: A scanning laser polarimeter (GDx, LDT/CZM) was used to acquire 15 × 15-degree macular images in 10 subjects diagnosed with nonexudative AMD and 10 age-matched control subjects. The coefficient of variation (COV, SD/mean) was used to quantify variability in pixel intensity in the central 3.3° of the macula for custom images emphasizing multiply scattered light (the depolarized light image) and polarization-retaining light (the maximum of the parallel detector image). The intensity COV was compared across subject categories using paired t tests for each image type.

Results: The COV in the central macula was significantly higher in the AMD subject group (average, 0.221; 95% confidence interval [CI], 0.157 to 0.265) when compared with matched control subjects (average 0.120; 95% CI, 0.107 to 0.133) in the depolarized light image (P = .01). The COV in the maximum of the parallel detector image was not statistically different between the two subject groups (AMD average, 0.162 [95% CI, 0.138 to 0.185]; control average, 0.137 [95% CI, 0.115 to 0.158]; P = .21).

Conclusions: Variability in multiply scattered light is higher than that of light that is more polarization preserving in patients with nonexudative AMD. Multiple scattering may act as an early indicator representing disruption to the macula in early AMD.
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http://dx.doi.org/10.1097/OPX.0000000000001197DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6688506PMC
April 2018

Measuring polarization changes in the human outer retina with polarization-sensitive optical coherence tomography.

J Biophotonics 2018 05 26;11(5):e201700134. Epub 2018 Feb 26.

School of Optometry, Indiana University, Bloomington, Indiana.

Morphological changes in the outer retina such as drusen are established biomarkers to diagnose age-related macular degeneration. However, earlier diagnosis might be possible by taking advantage of more subtle changes that accompany tissues that bear polarization-altering properties. To test this hypothesis, we developed a method based on polarization-sensitive optical coherence tomography with which volumetric data sets of the macula were obtained from 10 young (<25 years) and 10 older (>54 years) subjects. All young subjects and 5 of the older subjects had retardance values induced by the retinal pigment epithelium and Bruch's membrane (RPE-BM) complex that were just above the noise floor measurement (5°-13° at 840 nm). In contrast, elevated retardance, up to 180°, was observed in the other 5 older subjects. Analysis of the degree of polarization uniformity (DOPU) demonstrates that reduced DOPU (<0.4) in the RPE is associated with elevated double pass phase retardation (DPPR) below the RPE-BM complex, suggesting that the observed elevated DPPR in older subjects is the result of increased scattering or polarization scrambling. Collectively, our measurements show that the outer retina can undergo dramatic change in its polarization properties with age, and in some cases still retain its clinically normal appearance.
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http://dx.doi.org/10.1002/jbio.201700134DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6596294PMC
May 2018

Alterations to the Foveal Cone Mosaic of Diabetic Patients.

Invest Ophthalmol Vis Sci 2017 07;58(9):3395-3403

School of Optometry, Indiana University, Bloomington, Indiana, United States.

Purpose: We measured localized changes occurring in the foveal cone photoreceptors and related defects in the cone mosaic to alterations in the nearby retinal vasculature.

Methods: The central 4° of the retina of 54 diabetic (53.7 ± 12.5 years) and 85 control (35.8 ± 15.2 years) participants were imaged with the Indiana adaptive optics scanning laser ophthalmoscope. Foveal cones and overlying retinal capillaries were imaged and infrared scanning laser ophthalmoscopy (IR SLO) images and optical coherence tomography (OCT) B-scans were obtained. Follow-up imaging sessions were performed with intervals from 4 to 50 months for 22 of the 54 diabetic participants.

Results: The foveal cone mosaics of 49 of 54 diabetic participants were of sufficient quality to assess the absence or presence of small localized defects in the cone mosaic. In 13 of these 49 diabetic participants we found localized defects, visualized as sharp-edged areas of cones with diminished reflectivity. These small, localized areas ranged in size from 10 × 10 μm to 75 × 30 μm. Of these 13 participants with cone defects, 11 were imaged over periods from 4 to 50 months and the defects remained relatively stable. These dark regions were not shadows of overlying retinal vessels, but all participants with these localized defects had alterations in the juxtafoveal capillary network.

Conclusions: The foveal cone mosaic can show localized areas of dark cones that persist over time, that apparently correspond to either missing or nonreflecting cones, and may be related to local retinal ischemia.
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http://dx.doi.org/10.1167/iovs.17-21793DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5501497PMC
July 2017

Evaluation of intraretinal migration of retinal pigment epithelial cells in age-related macular degeneration using polarimetric imaging.

Sci Rep 2017 06 9;7(1):3150. Epub 2017 Jun 9.

Department of Ophthalmology, Tokyo Medical University, Tokyo, Japan.

The purpose of the present study was to evaluate the intraretinal migration of the retinal pigment epithelium (RPE) cells in age-related macular degeneration (AMD) using polarimetry. We evaluated 155 eyes at various AMD stages. Depolarized light images were computed using a polarization-sensitive scanning laser ophthalmoscope (PS-SLO), and the degree of polarization uniformity was calculated using polarization-sensitive optical coherence tomography (OCT). Each polarimetry image was compared with the corresponding autofluorescence (AF) images at 488 nm (SW-AF) and at 787 nm (NIR-AF). Intraretinal RPE migration was defined by the presence of depolarization at intraretinal hyperreflective foci on PS-SLO and PS-OCT images, and by the presence of hyper-AF on both NIR-AF and SW-AF images. RPE migration was detected in 52 of 155 eyes (33.5%) and was observed in drusenoid pigment epithelial detachment (PED) and serous PED with significantly higher frequencies than in other groups (P = 0.015). The volume of the migrated RPE cluster in serous PED was significantly correlated with the volume of the PED (R = 0.26; P = 0.011). Overall, our results showed that intraretinal RPE migrations occurred in various AMD stages, and that they occurred more commonly in eyes with serous and drusenoid PED.
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http://dx.doi.org/10.1038/s41598-017-03529-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5466639PMC
June 2017

SD-OCT and Adaptive Optics Imaging of Outer Retinal Tubulation.

Optom Vis Sci 2017 03;94(3):411-422

*OD, FAAO †OD ‡PhD, FAAO §MD, PhD ∥BS **OD, PhD School of Optometry, Indiana University, Bloomington, Indiana (all authors).

Purpose: To investigate outer retinal tubulation (ORT) using spectral domain optical coherence tomography (SD-OCT) and an adaptive optics scanning laser ophthalmoscope (AOSLO). To document the frequency of ORT in atrophic retinal conditions and quantify ORT dimensions versus adjacent retinal layers.

Methods: SD-OCT images were reviewed for the presence of retinal atrophy, scarring, and/or exudation. The greatest width of each ORT was quantified. Inner and outer retinal thicknesses adjacent to and within the area of ORT were measured for 18 patients. AOSLO imaged ORTs in five subjects with direct and scattered light imaging.

Results: ORT was identified in 47 of 76 subjects (61.8%) and in 65 eyes via SD-OCT in a wide range of conditions and ages, and in peripapillary atrophy. ORTs appeared as finger-like projections in atrophy, seen in the en face images. AOSLO showed some ORTs with bright cones that guide light within atrophic areas. Multiply scattered light mode AOSLO visualized variegated lines (18-35 μm) radiating from ORTs. The ORTs' width on OCT b-scan images varied from 70 to 509 μm. The inner retina at the ORT was significantly thinner than the adjacent retina, 135 vs.170 μm (P = .004), whereas the outer retina was significantly thicker, 115 vs. 80 μm (P = .03).

Conclusions: ORTs are quite common in eyes with retinal atrophy in various disorders. ORTs demonstrate surviving photoreceptors in tubular structures found within otherwise nonsupportive atrophic areas that lack retinal pigment epithelium and choriocapillaris.
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http://dx.doi.org/10.1097/OPX.0000000000001031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5321857PMC
March 2017

Comparison of Cysts in Red and Green Images for Diabetic Macular Edema.

Optom Vis Sci 2017 02;94(2):137-149

*MS, PhD †PhD, FAAO ‡OD, FAAO §OD, PhD ∥AA **OD ††OD, PhD, FAAO ‡‡PhD §§MD, PhD ∥∥MS, MBA Indiana University School of Optometry, Bloomington, Indiana (MAA, VEM, AEE, BPH, KB, TJG, SGB, SBY); University of California, Berkeley School of Optometry, Berkeley, California (TVL, GYO, JAC); Aeon Imaging, LLC, Bloomington, Indiana (MSM, AEE, TJG); EyePACS, LLC, San Jose, California (JAC); and Department of Ophthalmology, Tokyo Medical University Ibaraki Medical Center, Inashiki, Ibaraki, Japan (MM).

Purpose: To investigate whether cysts in diabetic macular edema are better visualized in the red channel of color fundus camera images, as compared with the green channel, because color fundus camera screening methods that emphasize short-wavelength light may miss cysts in patients with dark fundi or changes to outer blood retinal barrier.

Methods: Fundus images for diabetic retinopathy photoscreening were acquired for a study with Aeon Imaging, EyePACS, University of California Berkeley, and Indiana University. There were 2047 underserved, adult diabetic patients, of whom over 90% self-identified as a racial/ethnic identify other than non-Hispanic white. Color fundus images at nominally 45 degrees were acquired with a Canon Cr-DGi non-mydriatic camera (Tokyo, Japan) then graded by an EyePACS certified grader. From the 148 patients graded to have clinically significant macular edema by the presence of hard exudates in the central 1500 μm of the fovea, we evaluated macular cysts in 13 patients with cystoid macular edema. Age ranged from 33 to 68 years. Color fundus images were split into red, green, and blue channels with custom Matlab software (Mathworks, Natick, MA). The diameter of a cyst or confluent cysts was quantified in the red-channel and green-channel images separately.

Results: Cyst identification gave complete agreement between red-channel images and the standard full-color images. This was not the case for green-channel images, which did not expose cysts visible with standard full-color images in five cases, who had dark fundi. Cysts appeared more numerous and covered a larger area in the red channel (733 ± 604 μm) than in the green channel (349 ± 433 μm, P < .006).

Conclusions: Cysts may be underdetected with the present fundus camera methods, particularly when short-wavelength light is emphasized or in patients with dark fundi. Longer wavelength techniques may improve the detection of cysts and provide more information concerning the early stages of diabetic macular edema or the outer blood retinal barrier.
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http://dx.doi.org/10.1097/OPX.0000000000001010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5266646PMC
February 2017

Distribution differences of macular cones measured by AOSLO: Variation in slope from fovea to periphery more pronounced than differences in total cones.

Vision Res 2017 03 3;132:62-68. Epub 2016 Nov 3.

Indiana University School of Optometry, 800 E. Atwater Ave, Bloomington, IN 47405, United States. Electronic address:

Large individual differences in cone densities occur even in healthy, young adults with low refractive error. We investigated whether cone density follows a simple model that some individuals have more cones, or whether individuals differ in both number and distribution of cones. We quantified cones in the eyes of 36 healthy young adults with low refractive error using a custom adaptive optics scanning laser ophthalmoscope. The average cone density in the temporal meridian was, for the mean±SD, 43,216±6039, 27,466±3496, 14,996±1563, and 12,207±1278cones/mm for 270, 630, 1480, and 2070μm from the foveal center. Cone densities at 630μm retinal eccentricity were uncorrelated to those at 2070μm, ruling out models with a constant or proportional relation of cone density to eccentricity. Subjects with high central macula cone densities had low peripheral cone densities. The cone density ratio (2070:630μm) was negatively correlated with cone density at 630μm, consistent with variations in the proportion of peripheral cones migrating towards the center. We modelled the total cones within a central radius of 7deg, using the temporal data and our published cone densities for temporal, nasal, superior, and inferior meridians. We computed an average of 221,000 cones. The coefficient of variation was 0.0767 for total cones, but higher for samples near the fovea. Individual differences occur both in total cones and other developmental factors related to cone distribution.
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http://dx.doi.org/10.1016/j.visres.2016.06.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5346455PMC
March 2017

Imaging the visual system: from the eye to the brain.

Ophthalmic Physiol Opt 2016 05;36(3):213-7

School of Optometry, University of California, Berkeley, USA.

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http://dx.doi.org/10.1111/opo.12298DOI Listing
May 2016

Non-mydriatic confocal retinal imaging using a digital light projector.

Proc SPIE Int Soc Opt Eng 2015 Feb 10;9376. Epub 2015 Mar 10.

Aeon Imaging, LLC, 501 S Madison St., Ste. 103, Bloomington, IN, USA 47403-2452; School of Optometry, Indiana University, 800 E Atwater Ave., Bloomington, IN, USA 47405-3680.

A digital light projector is implemented as an integrated illumination source and scanning element in a confocal non-mydriatic retinal camera, the Digital Light Ophthalmoscope (DLO). To simulate scanning, a series of illumination lines are rapidly projected on the retina. The backscattered light is imaged onto a 2-dimensional rolling shutter CMOS sensor. By temporally and spatially overlapping the illumination lines with the rolling shutter, confocal imaging is achieved. This approach enables a low cost, flexible, and robust design with a small footprint. The 3 generation DLO technical design is presented, using a DLP LightCrafter 4500 and USB3.0 CMOS sensor. Specific improvements over previous work include the use of yellow illumination, filtered from the broad green LED spectrum, to obtain strong blood absorption and high contrast images while reducing pupil constriction and patient discomfort.
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http://dx.doi.org/10.1117/12.2077704DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4749182PMC
February 2015

Henle fiber layer phase retardation changes associated with age-related macular degeneration.

Invest Ophthalmol Vis Sci 2014 Dec 18;56(1):284-90. Epub 2014 Dec 18.

Indiana University School of Optometry, Bloomington, Indiana, United States.

Purpose: To quantify and compare phase retardation amplitude and regularity associated with the Henle fiber layer (HFL) between nonexudative AMD patients and age-matched controls using scanning laser polarimetry (SLP) imaging.

Methods: A scanning laser polarimeter was used to collect 15 × 15° macular-centered images in 25 patients with nonexudative AMD and 25 age-matched controls. Raw image data were used to compute macular phase retardation maps associated with the HFL. Consecutive, annular regions of interest from 0.5 to 3.0° eccentricity, centered on the fovea, were used to generate intensity profiles from phase retardation data and analyzed with two complementary techniques: a normalized second harmonic frequency (2f) of the fast Fourier Transform (FFT) analysis and a curve fitting analysis using a 2f sine function. Paired t-tests were used to compare the normalized 2f FFT magnitude at each eccentricity between the two groups, the eccentricity that yielded the maximum normalized 2f FFT between paired individuals across the two groups, and curve fitting RMS error at each eccentricity between the two groups.

Results: Normalized 2f FFT components were lower in the AMD group at each eccentricity, with no difference between the two groups in the maximum normalized 2f FFT component eccentricity. The root-mean-square (RMS) error from curve fitting was significantly higher in the AMD group.

Conclusions: Phase retardation changes in the central macula indicate loss and/or structural alterations to central cone photoreceptors in nonexudative AMD patients. Scanning laser polarimetry imaging is a noninvasive method for quantifying cone photoreceptor changes associated with central macular disease.
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http://dx.doi.org/10.1167/iovs.14-14459DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4294289PMC
December 2014

Eye shape using partial coherence interferometry, autorefraction, and SD-OCT.

Optom Vis Sci 2015 Jan;92(1):115-22

*OD †PhD, FAAO ‡BS Indiana University School of Optometry, Bloomington, Indiana (all authors).

Purpose: Peripheral refraction and retinal shape may influence refractive development. Peripheral refraction has been shown to have a high degree of variability and can take considerable time to perform. Spectral domain optical coherence tomography (SD-OCT) and peripheral axial length measures may be more reliable, assuming that the retinal position is more important than the peripheral optics of the lens/cornea.

Methods: Seventy-nine subjects' right eyes were imaged for this study (age range, 22 to 34 years; refractive error, -10 to +5.00). Thirty-degree SD-OCT (Spectralis, Heidelberg Engineering, Heidelberg, Germany) images were collected in a radial pattern along with peripheral refraction with an autorefractor (Shin-Nippon Autorefractor) and peripheral axial length measurements with partial coherence interferometry (IOLMaster, Zeiss). Statistics were performed using repeated-measures analysis of variance in SPSS (IBM, Armonk, NY), Bland-Altman analyses, and regression. All measures were converted to diopters to allow direct comparison.

Results: Spectral domain OCT showed a retinal shape with an increased curvature for myopes compared with emmetropes/hyperopes. This retinal shape change became significant around 5 degrees. The SD-OCT analysis for retinal shape provides a resolution of 0.026 diopters, which is about 10 times more accurate than using autorefraction (AR) or clinical refractive techniques. Bland-Altman analyses suggest that retinal shape measured by SD-OCT and the partial coherence interferometry method were more consistent with one another than either was with AR.

Conclusions: With more accurate measures of retinal shape using SD-OCT, consistent differences between emmetropes/hyperopes and myopes were found nearer to the fovea than previously reported. Retinal shape may be influenced by central refractive error, and not merely peripheral optics. Partial coherence interferometry and SD-OCT appear to be more accurate than AR, which may be influenced by other factors such as fixation and accommodation. Autorefraction does measure the optics directly, which may be a strength of that method.
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http://dx.doi.org/10.1097/OPX.0000000000000453DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4516166PMC
January 2015

The association between the foveal avascular zone and retinal thickness.

Invest Ophthalmol Vis Sci 2014 Sep 30;55(10):6870-7. Epub 2014 Sep 30.

School of Optometry, Indiana University, Bloomington, Indiana, United States.

Purpose: To investigate the association between the size and shape of the foveal avascular zone and retinal thickness in healthy subjects.

Methods: In vivo imaging of the foveal microvasculature was performed on 32 subjects by using an adaptive optics scanning laser ophthalmoscope (AOSLO). Motion contrast maps of the AOSLO images were used to generate a montage revealing the foveal capillary network. Foveal avascular zone (FAZ) diameters along the horizontal (FAZH) and vertical (FAZV) meridians were measured on the montages. An asymmetry index (AI) of the FAZ was then computed as the ratio of the FAZH to FAZV. Retinal thickness was investigated by using spectral-domain optical coherence tomography (SDOCT). Inner retinal layer (INLFAZ) thickness and outer nuclear layer (ONLFAZ) thickness were measured at the edges of the FAZ on the horizontal and vertical SDOCT scans on the same eye.

Results: The foveal capillary network was readily visualized in all subjects. As expected there was individual variation in the size and shape of the FAZ. Along the horizontal and vertical meridians, the mean±SD (μm) of the FAZ diameter was 607±217 and 574±155, respectively. The INLFAZ thickness was 68±9 and 66±9, and the ONLFAZ thickness was 103±13 and 105±11, respectively. The mean±SD of the AI was 1.03±0.27. The difference between FAZH and FAZV decreases with increasing FAZ area (P=0.004). Mean ONLFAZ was negatively correlated with FAZ effective diameter (P<0.0001). No significant correlation was found between mean INLFAZ and FAZ effective diameter (P=0.16).

Conclusions: Despite large individual variations in size and shape of the FAZ, the INLFAZ has a relatively constant thickness at the margins of the FAZ, suggesting the presence of retinal capillaries is needed to sustain an INLFAZ thickness greater than 60 μm. A smaller FAZ area is associated with a vertically elongated FAZ.
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http://dx.doi.org/10.1167/iovs.14-15446DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4214206PMC
September 2014

In vivo adaptive optics microvascular imaging in diabetic patients without clinically severe diabetic retinopathy.

Biomed Opt Express 2014 Mar 27;5(3):961-74. Epub 2014 Feb 27.

Eugene and Marilyn Glick Eye Institute, Department of Ophthalmology, Indiana University School of Medicine, 1160 West Michigan Street, Indianapolis, IN 46202, USA.

We used a confocal adaptive optics scanning laser ophthalmoscope (AOSLO) to image the retina of subjects with non-proliferative diabetic retinopathy (NPDR). To improve visualization of different retinal features, the size and alignment of the confocal aperture were varied. The inner retinal layers contained clearly visualized retinal vessels. In diabetic subjects there was extensive capillary remodeling despite the subjects having only mild or moderate NPDR. Details of the retinal microvasculature were readily imaged with a larger confocal aperture. Hard exudates were observed with the AOSLO in all imaging modes. Photoreceptor layer images showed regions of bright cones and dark areas, corresponding in location to overlying vascular abnormalities and retinal edema. Clinically undetected intraretinal vessel remodeling and varying blood flow patterns were found. Perifoveal capillary diameters were larger in the diabetic subjects (p<0.01), and small arteriolar walls were thickened, based on wall to lumen measurements (p<.05). The results suggest that existing clinical classifications based on lower magnification clinical assessment may not adequately measure key vascular differences among individuals with NPDR.
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http://dx.doi.org/10.1364/BOE.5.000961DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3959854PMC
March 2014

Utility of hard exudates for the screening of macular edema.

Optom Vis Sci 2014 Apr;91(4):370-5

*OD †MD, MPA ‡OD, PhD §MS ∥PhD **MD, PhD University of California, Berkeley School of Optometry, Berkeley, California (TVL, GYO, GHB, JAC); Aeon Imaging, LLC, Bloomington, Indiana (MSM, AEE, TJG); Indiana University School of Optometry, Bloomington, Indiana (AEE, TJG); and EyePACS, LLC, San Jose, California (GHB, JAC).

Purpose: The purpose of this study was to determine whether hard exudates (HEs) within one disc diameter of the foveola is an acceptable criterion for the referral of diabetic patients suspected of clinically significant macular edema (CSME) in a screening setting.

Methods: One hundred forty-three adults diagnosed as having diabetes mellitus were imaged using a nonmydriatic digital fundus camera at the Alameda County Medical Center in Oakland, CA. Nonstereo fundus images were graded independently for the presence of HE near the center of the macula by two graders according to the EyePACS grading protocol. The patients also received a dilated fundus examination on a separate visit. Clinically significant macular edema was determined during the dilated fundus examination using the criteria set forth by the Early Treatment Diabetic Retinopathy Study. Subsequently, the sensitivity and specificity of HEs within one disc diameter of the foveola in nonstereo digital images used as a surrogate for the detection of CSME diagnosed by live fundus examination were calculated.

Results: The mean (±SD) age of 103 patients included in the analysis was 56 ± 17 years. Clinically significant macular edema was diagnosed in 15.5% of eyes during the dilated examination. For the right eyes, the sensitivity of HEs within one disc diameter from the foveola as a surrogate for detecting CSME was 93.8% for each of the graders; the specificity values were 88.5 and 85.1%. For the left eyes, the sensitivity values were 93.8 and 75% for each of the two graders, respectively; the specificity was 87.4% for both graders.

Conclusions: This study supports the use of HE within a disc diameter of the center of the macula in nonstereo digital images for CSME detection in a screening setting.
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http://dx.doi.org/10.1097/OPX.0000000000000205DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3969389PMC
April 2014

Henle fiber layer phase retardation measured with polarization-sensitive optical coherence tomography.

Biomed Opt Express 2013 1;4(11):2296-306. Epub 2013 Oct 1.

Center for Optical Research and Education, Utsunomiya University, Utsunomiya, Tochigi, 321-8585 Japan.

We developed a method based on polarization-sensitive optical coherence tomography (PS-OCT) to quantify the double pass phase retardation (DPPR) induced by Henle fiber layer in three subjects. Measurements of the retina were performed at a mean wavelength of 840 nm using two polarization states that were perpendicular in a Poincaré sphere representation and phase retardation contributions from tissue layers above and below the Henle fiber layer were excluded using appropriately placed reference and measurement points. These points were semi-automatically segmented from intensity data. Using a new algorithm to determine DPPR, the Henle fiber layer in three healthy subjects aged 50-60 years showed elevated DPPR in a concentric ring about the fovea, with an average maximum DPPR for the three subjects of 22.0° (range: 20.4° to 23.0°) occurring at an average retinal eccentricity of 1.8° (range: 1.5° to 2.25°). Outside the ring, a floor of approximately 6.8° was measured, which we show can mainly be attributed to phase noise that is induced in the polarization states. We also demonstrate the method can determine fast axis orientation of the retardation, which is found consistent with the known radial pattern of Henle fibers.
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http://dx.doi.org/10.1364/BOE.4.002296DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3829392PMC
December 2013

Non-Mydriatic Confocal Retinal Imaging Using a Digital Light Projector.

Proc SPIE Int Soc Opt Eng 2013 Mar;8567

Aeon Imaging, LLC, 501 S Madison St., Ste. 103, Bloomington, IN, USA 47403-2452.

A digital light projector is implemented as an integrated illumination source and scanning element in a confocal non-mydriatic retinal camera, the DLP-Cam. To simulate scanning, a series of illumination lines are rapidly projected on the retina. The backscattered light is imaged onto a 2-dimensional rolling shutter CMOS sensor. By temporally and spatially overlapping the illumination lines with the rolling shutter, confocal imaging is achieved. This approach enables a low cost, flexible, and robust design with a small footprint. Qualitative image comparison with commercial non-mydriatic SLOs and fundus cameras shows comparable fine vessel visibility and contrast.
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http://dx.doi.org/10.1117/12.2001305DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3824258PMC
March 2013

Clinical applications of high resolution in-vivo retinal imaging.

J Ophthalmol 2013 27;2013:312974. Epub 2013 Feb 27.

Department of Vision Science, New England College of Optometry, Boston, MA 02115, USA.

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http://dx.doi.org/10.1155/2013/312974DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3600202PMC
March 2013

Fixation stability and scotoma mapping for patients with low vision.

Optom Vis Sci 2013 Feb;90(2):164-73

Indiana University School of Optometry, Bloomington, Indiana 47405, USA.

Purpose: To develop a simplified device that performs fundus perimetry techniques such as fixation mapping and kinetic perimetry.

Methods: We added visual stimulation to a near-infrared retinal imager, the laser scanning digital camera (LSDC). This device uses slit scanning illumination combined with a two-dimensional CMOS (complementary metal oxide semiconductor) detector, with continuous viewing of the retina. The CMOS readout was synchronized with the slit scanning, thereby serving as a confocal aperture to reduce stray light in retinal images. A series of retinal images of 36 degrees was automatically aligned to provide data for fixation maps and quantification of fixation stability. The LSDC and alignment techniques also provided fundus viewing with retinal location correction for scotoma mapping.

Results: First, fixation mapping was readily performed in patients with central scotoma or amblyopia. The automatic alignment algorithm allowed quantification of fixation stability in patients with macular pathologies that did not cause scotoma. Second, fixation stability was rapidly and quantitatively assessed by the automatic registration of the series of retina images. There was no significant difference in the fixation stability with automatic versus manual alignment. Kinetic perimetry demonstrated that fundus imaging helped reduce the variability of perimetric data by identifying and preventing false-positives caused by eye motion. We found that the size of the blind spot was significantly larger for dark targets on brighter backgrounds than when the contrast was reversed (p < 0.045). This is consistent with incremental targets being detected partially or wholly because of scattered light falling on more sensitive retinal locations.

Conclusions: Fundus perimetry with the LSDC allows for a wide range of fixation and perimetry tasks.
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http://dx.doi.org/10.1097/OPX.0b013e31827cda72DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3560296PMC
February 2013

Cone photoreceptor packing density and the outer nuclear layer thickness in healthy subjects.

Invest Ophthalmol Vis Sci 2012 Jun 14;53(7):3545-53. Epub 2012 Jun 14.

School of Optometry, Indiana University, Bloomington, Indiana 47405-3860, USA.

Purpose: We evaluated the relationship between cone photoreceptor packing density and outer nuclear layer (ONL) thickness within the central 15 degrees.

Methods: Individual differences for healthy subjects in cone packing density and ONL thickness were examined in 8 younger and 8 older subjects, mean age 27.2 versus 56.2 years. Cone packing density was obtained using an adaptive optics scanning laser ophthalmoscope (AOSLO). The ONL thickness measurements included the ONL and the Henle fiber layer (ONL + HFL), and were obtained using spectral domain optical coherence tomography (SDOCT) and custom segmentation software.

Results: There were sizeable individual differences in cone packing density and ONL + HFL thickness. Older subjects had on average lower cone packing densities, but thicker ONL + HFL measurements. Cone packing density and ONL + HFL thickness decreased with increasing retinal eccentricity. The ratio of the cone packing density-to-ONL2 was larger for the younger subjects group, and decreased with retinal eccentricity.

Conclusions: The individual differences in cone packing density and ONL + HFL thickness are consistent with aging changes, indicating that normative aging data are necessary for fine comparisons in the early stages of disease or response to treatment. Our finding of ONL + HFL thickness increasing with aging is inconsistent with the hypothesis that ONL measurements with SDOCT depend only on the number of functioning cones, since in our older group cones were fewer, but thickness was greater.
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http://dx.doi.org/10.1167/iovs.11-8694DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3406883PMC
June 2012

Foveal localization in non-exudative AMD using scanning laser polarimetry.

Optom Vis Sci 2012 May;89(5):667-77

Indiana University School of Optometry, Bloomington, Indiana 47405, USA.

Purpose: To determine whether custom scanning laser polarimetry (SLP) images, differing in polarization content, can be used to accurately localize the fovea in the presence of non-exudative age-related macular degeneration (AMD). To determine whether alterations to the foveal structure in non-exudative AMD significantly disrupts the birefringent Henle fiber layer, responsible for the macular cross pattern in some SLP images. To determine whether phase retardation information, specifically color-coded information representing its magnitude and axis, allow better foveal localization than images including retardation amplitude only.

Methods: SLP images were acquired in 25 AMD subjects and 25 age-matched controls. Raw data were used to generate five custom image types differing in polarization content. The foveal location was marked by three graders in each image type for each subject. The difference in variability was compared between the AMD subjects and matched controls. We further determined whether the orientation of Henle fiber layer phase retardation improved localization in 10 subjects with the highest variability in images including only phase retardation amplitude.

Results: Images that differed in polarization content led to strikingly different visualizations of AMD pathology. The Henle fiber layer remained sufficiently intact to assist in fovea localization in all subjects but with more variability in the AMD group. For both the AMD and matched control group, images containing birefringence amplitude and orientation information reduced the amount of intragrader, intergrader, and interimage variability for estimating foveal location.

Conclusions: The disruption in Henle fiber birefringence was evident in the eyes with AMD but nevertheless was sufficient to help in foveal localization despite macular pathology. Phase retardation amplitude and axis of orientation can be a useful tool in foveal localization in patients with AMD.
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http://dx.doi.org/10.1097/OPX.0b013e31824eeb25DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3348428PMC
May 2012

Foveal phase retardation changes associated with normal aging.

Vision Res 2011 Nov 27;51(21-22):2263-72. Epub 2011 Aug 27.

Indiana University, School of Optometry, Bloomington 47405,USA.

This study quantified normal age-related changes to the photoreceptor axons in the central macula using the birefringent properties of the Henle fiber layer. A scanning laser polarimeter was used to acquire 15° × 15° macular images in 120 clinically normal subjects, ranging in age from the third decade to the eighth. Raw image data of the macular cross were used to compute phase retardation maps associated with Henle fiber layer. Annular regions of interest ranging from 0.25° to 3° eccentricity and centered on the fovea were used to generate intensity profiles from the phase retardation data, which were then analyzed using sine curve fitting and Fast Fourier Transform (FFT). The amplitude of a 2f sine curve was used as a measure of macular phase retardation magnitude. For FFT analysis, the 2f amplitude, as well as the 4f, were normalized by the remaining FFT components. The amplitude component of the 2f curve fit and the normalized 2f FFT component decreased as a function of age, while the eccentricity of the maximum value for the normalized 2f FFT component increased. The phase retardation changes in the central macula indicate structural alterations in the cone photoreceptor axons near the fovea as a function of age. These changes result in either fewer cone photoreceptors in the central macula, or a change in the orientation of their axons. This large sample size demonstrates systematic changes to the central cone photoreceptor morphology using scanning laser polarimetry.
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http://dx.doi.org/10.1016/j.visres.2011.08.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3319026PMC
November 2011
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