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Fundus autofluorescence (FAF) imaging is a admired apparatus for imaging eyes with retinal diseases1 and serves as a assessable endpoint in analytic trials accompanying to age-related macular abatement (AMD).2 The autofluorescence adjustment takes advantage of the built-in backdrop of lipofuscin that is commonly present in the animal retinal colorant epithelium (RPE) cells.3 Lipofuscin consists of lipid-containing granules with beaming properties, which accrue in the RPE as a metabolic by-product of the beheld cycle,4 added specifically, from the assimilation of photoreceptor alien segments. Thus, FAF abstinent noninvasively is bedeviled by the autofluorescence of lipofuscin.5



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Lipofuscin accumulates as the RPE ages, about these deposits are additionally begin anyhow broadcast in patients with retinal disease, such as AMD. One of the ancient apparent ache markers in AMD is an aberrant arrangement of FAF. These imaging changes are attributed to differences in the bulk or administration of bisretinoid fluorophores in the RPE lipofuscin. In vitro class observations accept appropriate that lipofuscin and one of its aloft components, the fluorophore A2E, may apply baneful furnishings on the RPE6,7; however, in vivo affirmation is adjoin a aerial lipofuscin accession in patients with aboriginal or average stages of AMD,8 and the agitation is ongoing.9,10

Numerous studies accept appropriate that FAF imaging could abetment in the apprehension and/or ecology of, for example, geographic abatement (GA)11 or choroidal neovascularization12 in AMD. However, it is cryptic how abundant able-bodied quantitative affirmation exists to abutment the accurateness of FAF imaging.13 Quantitative fundus autofluorescence (qAF), alien in 2011,14 is performed by calibrating the FAF angel to an anchored advertence of accustomed fluorescence efficiency, authoritative it accessible to reproducibly quantify and analyze the FAF acuteness amid patients and beyond time.

Gliem et al. arise the aboriginal appliance of qAF to abstraction non-neovascular AMD.8 Nevertheless, the authors accustomed several limitations of their study. For example, abstracts were not performed in patients earlier than 65 years, and patients with backward AMD were not advised either.



The aim of this abstraction was to use qAF to considerately admeasurement FAF intensities and analyze them with accustomed age-matched controls. By analytical FAF differences in a quantitative manner, via qAF imaging, the present abstraction may afford ablaze on the role of lipofuscin fluorophores in assorted AMD phenotypes and to check the accord of lipofuscin to accelerating AMD in vivo.

The abstraction agreement adhered to the credo of animal assay as presented in the Declaration of Helsinki and was accustomed by both the Institutional Review Board (IRB) at New York University (NYU) School of Medicine, Department of Ophthalmology and Western IRB (Puyallup, WA) at the Vitreous-Retina-Macula Consultants of New York, a clandestine convenance associated with NYU. Abstracts were collected, stored, and managed in acquiescence with the Bloom Insurance Portability and Accountability Act of 1996. From October 2016 to October 2017, patients with AMD were prospectively enrolled at the Brooklyn and Manhattan offices of the Vitreous-Retina-Macula Consultants of New York. A multicenter accord with NYU and Bellevue Hospital additionally accustomed us to recruit controls. A accounting abreast accord was acquired from anniversary accommodating afore the admission of any abstraction accompanying activities.

Participants included pseudophakic patients age-old 60 to 90 years and diagnosed with non-neovascular AMD in at atomic one eye, forth with accustomed age-matched controls. The admittance belief for patients and controls were the analytic assay of non-neovascular AMD based on the Beckman Initiative for Macular Assay (renamed the Stephen J. Ryan Initiative for Macular Research) Classification Committee system.15 Back available, eyes underwent added multimodal imaging, including blush fundus photography (Topcon TRC 50IX fundus camera; Topcon Medical Systems, Tokyo, Japan), ultra-widefield fundus photography (Optos 200Tx, Optos, Dunfermline, United Kingdom), accustomed FAF application the scanning laser ophthalmoscope short-wave dejected autofluorescence (Spectralis HRA OCT; Heidelberg Engineering, Heidelberg, Germany) and/or blooming ultra-widefield autofluorescence (Optos 200Tx), fluorescein and/or indocyanine-green angiography (Optos 200Tx and/or Topcon TRC 50IX and/or Spectralis HRA OCT), and imaging with optical adherence tomography angiography (RTVue XR Avanti; Optovue, Fremont, CA or Plex Elite 9000; Carl Zeiss Meditec, Dublin, CA) to characterize drusen phenotype.16

Exclusion belief were advised if any of the afterward allegation were present: diabetes mellitus, choroidal neovascularization in both eyes, antecedent articulation anatomy or any added action that would decidedly baffle with ocular imaging, and assay of any accessory retinopathy added than AMD such as retinal dystrophies, attitude occlusions, astigmatic degeneration, or axial aqueous chorioretinopathy.

Referencing a normative dataset,17,18 we abstinent qAF levels in three non-neovascular AMD phenotypes: bendable drusen (SD)/cuticular drusen (CD), which are amid amid the RPE and Bruch membrane,16 baffling macular ache (RMD)-subretinal drusenoid deposits (SDDs) centralized to the RPE,16 and GA. Participants with accustomed crumbling and advantageous maculas were additionally recruited and abstinent during this study.

According to accustomed of care, patients had a absolute aggrandized eye exam, which included imaging of the afterwards articulation of the eye. The patient’s medical, family, and amusing history were advised application a absolute medical questionnaire. In particular, the afterward elements were included: age, race, iris color, history of avalanche surgery, any history of abiding sun acknowledgment to the eyes, smoker history (including continuance and frequency), claimed history of diabetes or branch disease, claimed history of any added medical conditions, and any ancestors history of macular degeneration, any added retinal degeneration, or cardiac ache (Table).

Table:

Demographic and Analytic Overview of the Abstraction Population

A connected protocol, consisting of a near-infrared reflectance, spectral-domain optical adherence tomography (SD-OCT) images and qAF, was performed simultaneously, and in allotment for accumulated analysis, with the Spectralis HRA OCT, a qAF-ready scanning laser ophthalmoscope. Because the accustomed lens absorbs the dejected autofluorescence action ablaze and crumbling changes of the lens (such as avalanche development) can baffle with quantitative measurements, alone pseudophakic eyes with accustomed intraocular lens absorbance spectrum and bright afterwards abridged were advised in this study. The action of converting a qualitative angel into a quantitative angel is performed by amalgam an centralized fluorescence advertence in the Spectralis, which is additionally scanned at the time of imaging. This allows alone images to be normalized for variations in laser ability or detector acuteness amid patients. Details of the qAF address are in Delori et al.14 For assay purposes, qAF images were taken on the patient’s acceptable eye.

For qAF imaging, the camera was positioned centered on the fovea of the accommodating by application the near-infrared reflectance access and the centralized fixation light. Afterwards switching to the qAF access (488-nm action and 500-nm to 680-nm detection), focus and alignment were readjusted according to refraction and to access a accordant signal. For optical acerbic of photopigment, the retina was apparent to dejected action ablaze for at atomic 25 to 30 seconds. For anniversary participant, 12 qAF images were acquired in sequence, and a beggarly angel was computed application customized software developed by Heidelberg Engineering for recording qAF images (30° acreage of appearance and 768 pixels × 768 pixels). Up to three of the 12 images could be afar to access the clearest blended possible.

After the recording of anniversary series, the affection of the acquired images was thoroughly evaluated for angel artifacts. Exclusion belief mainly included bereft optical acerbic or aphotic images, shadows, or ambiguous fixation. The qAF ethics were affected by barometer the beggarly gray levels aural eight concentric segments (qAF-8) for the pericentral mid-ring of the Delori arrangement (Figure 1).

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Figure 1.

The quantitative fundus autofluorescence (qAF)-8 pattern. The qAF-8 is the beggarly of the qAF ethics aural the eight numbered zones. This bury apparatus should be in the centermost of the fovea and the bound on the banausic bend of the optic disc.

Retina argosy and GA itself (in the patients with GA) were afar from analysis. The qAF-gray ethics were automatically exported to a spreadsheet assay affairs (Microsoft Excel 2016 for Windows, adaptation 15.14; Microsoft Corporation, Redmond, WA) Finally, the qAF-8 ethics were statistically compared with those ascendancy individuals afterwards eye disease, for anniversary AMD phenotype.

Statistical assay was performed application IBM SPSS software for Windows adaptation 20.0.0 (IBM Corporation, Armonk, NY).

An absolute samples Welch t assay was run to actuate whether there were differences in qAF-8 amid AMD and ascendancy participants. There were no outliers in the data, as adjourned by assay of a box plot. The qAF-8 for anniversary accession was commonly distributed, as adjourned by the Shapiro-Wilk assay (P > .05). The acceptance of accord of variances was violated, as adjourned by Levene’s assay for adequation of variances (P = .035).

The Mann-Whitney U assay and Kruskal-Wallis assay were acclimated to analyze connected variables amid and/or amid groups.

A Kruskal-Wallis H assay was run to actuate whether there were differences in qAF-8 amid three groups of participants: controls, those with SD/CD or drusen phenotypes, and those with a predominantly SDD phenotype, which we advised as RMD. Distributions of qAF-8 were not agnate for all groups, as adjourned by beheld assay of a box plot.

Subsequently, pairwise comparisons were performed application Dunn’s action with a Bonferroni alteration for assorted comparisons.

In accession to the pairwise comparison, a abstracted allegory of qAF-8 in SDD and drusen phenotypes was performed. Because of the attendance of outliers in the abstracts as adjourned by assay of a box plot, a Mann-Whitney U assay was run to actuate whether there were differences in qAF-8 amid drusen and SDD phenotypes. Distributions of qAF-8 were similar, as adjourned by beheld inspection. A P bulk of .05 or beneath was accustomed as significant.

The patients included in this abstraction had a beggarly (standard aberration [SD]) age of 83.1 (5.39) years, and 19.35% of patients were men. Analytic and demographic characteristics are abbreviated in the Table.

Cigarette smoking, hypertension, hypercholesterolemia were some adjustable accident factors for AMD, which we begin in our cohort. Controls had a beggarly (SD) age of 74.4 (7.97) years, and 27.77% of participants were men.

Of the 38 AMD patients recruited, 7 were afar from assay because of angel defects. The beggarly qAF-8 was college in ascendancy participants (132.2 ± 42.8) than in AMD patients (75.9 ± 23.3, P < .003), a statistically cogent aberration (Figure 2). We additionally empiric that qAF levels were decidedly lower in patients with SDD/RMD (95.5 ± 47.2) than in participants afterwards AMD (131.2 ± 38.7, P = .0162) (Figure 3). Patients with SD/CD had average qAF ethics (97.2 ± 35.9 au), but were not statistically decidedly altered from either advantageous eyes (131.2 au ± 38.7 au, P = .0684) or SDD/RMD eyes at this sample admeasurement (Figure 4).

Figure 2.

Quantitative fundus autofluorescence (qAF)-8 for ascendancy against patients with age-related macular abatement (without geographic atrophy). Lower qAF-8 ethics were decidedly altered (P = .0026).

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Figure 3.

Quantitative fundus autofluorescence (qAF)-8 for ascendancy against patients with baffling macular ache / subretinal drusenoid deposits (without geographic atrophy). Lower qAF-8 ethics were decidedly altered (P = .0162).

Figure 4.

Quantitative fundus autofluorescence (qAF)-8 for ascendancy against patients with bendable drusen/cuticular drusen (without geographic atrophy). Lower qAF-8 ethics were not decidedly altered (P = .0684)

A added assay arise statistically cogent differences in beggarly qAF-8 amid the SDD eyes (95.5 au ± 47.2 au) and ascendancy eyes (131.2 au ± 38.7 au) for a P bulk of .0279, but not amid the SD/CD eyes (97.2 au ± 35.9 au) and ascendancy eyes, nor amid the SD/CD eyes and the SDD/RMD eyes (Figure 5).

Figure 5.

Quantitative fundus autofluorescence (qAF)-8 for ascendancy against non-neovascular age-related macular abatement phenotypes (without geographic atrophy). A statistically cogent aberration was alone begin for allegory amid ascendancy against patients with baffling macular disease/subretinal drusenoid deposits (P = .0279).

The everyman qAF-8 au ethics were in the patients with GA, abnormally those associated with RMD/SDD. The beggarly qAF-8 in nine participants was 80 au ± 48.6 au, with a cogent statistical aberration (P = .0112).

In 2015, Armenti et al. advised 31 eyes in 27 advantageous pseudophakic patients. They assured that qAF displays a beeline all-embracing access until age 75 to 80 years, as ahead suggested,19,20 but again appears to abatement thereafter. It was accepted that abbreviating qAF afterwards age 75 may be due to changes in lipofuscin turnover. We begin commensurable after-effects in both pseudophakic eyes with AMD and accustomed crumbling femal controls (Figure 6). Our abstraction participants additionally approved an advancement trend of qAF-8 up to 75 years of age, but there was additionally a abatement in qAF-8 with abbreviating RPE bloom and accretion severity of non-neovascular AMD date (soft drusen to RMD to GA) in this sample.

Figure 6.

Quantitative fundus autofluorescence (qAF)-8 for ascendancy against patients with age-related macular abatement (AMD). A bottomward trend is additionally apparent afterwards the age of 80 in patients with AMD (red arrow).

Gliem et al. did not address the lens cachet of their abstraction patients,8 so it ability accept afflicted their results. It is additionally alien how abundant qAF ethics ability alter afterwards a avalanche abstraction in alone patients. We adduce to abstraction this further.

Reports of quantitative abstracts from FAF imaging are sparse. Frampton et al. articular alone eight primary assay studies, from 2,240 altered references, which address FAF imaging accuracy, for assay and ecology disease, quantitatively.13 Furthermore, amid three studies for accepting FAF images in baffling pseudodrusen in AMD,21–23 alone one of these studies arise an cold (quantitative) access for free how aberrant (hypo or hyper) autofluorescence was defined.23

Although the agreement of SD, CD, and SDD may allotment similarities, they are differentiable by multimodal imaging back the RPE’s position and ablaze assimilation characteristics are taken into account.16

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Both bendable drusen and cuticular drusen are accountable to capricious bulk of ablaze abrasion because of their breadth beneath the RPE. In contrast, SDDs are centralized to the RPE. Moreover, the accustomed history and sequelae of CD and SD display characteristics of coalescence, resorption, and RPE disturbances that advance us to accede them aural the aforementioned AMD phenotype for our study.24

The qAF-8 in SD/CD eyes presented lower levels than age-matched ascendancy eyes. The FAF patterns of SD themselves ranged from bang to hyperautofluorescent. Accessible explanations for an added drusen-associated autofluorescence compared with accomplishments beset greater accession of fluorophores aural the aloft RPE or built-in fluorescence of drusen.8

Reduced qAF-8 ethics additionally acquired in CD were in band with a antecedent address application accustomed FAF imaging and accordant with a proposed abrasion of the aloft RPE.25 Balaratnasingam et al. additionally declared the CD phenotype on FAF, characterized by a hypofluorescent centermost with a hyperfluorescent margin, afterwards quantification.24 We begin capricious qAF levels in eyes with CD phenotypes, alignment from near-normal for age (Figure 7) to the everyman levels associated with GA (Figure 8).

Figure 7.

An allegorical case of the appropriate eye of an 81-year-old man with cuticular drusen (CD) phenotype as apparent on (A) blush photography, (B) fluorescein angiography, (C) indocyanine blooming angiography, and (D) accustomed fundus autofluorescence. Large drusen interspersed with CD. (F) A cross-sectional added abyss imaging optical adherence tomography (OCT) B-scan enables a accumulated assay with quantitative fundus autofluorescence (qAF)-8 ethics acquired or (G) a region-of-interest (ROI)-qAF in CD cluster. (H) The OCT aggregate and (I) abstract inset of the breadth of the band browse were registered to the ROI-qAF to admittance absolute spatial alternation amid the two methods.

Figure 8.

A adumbrative archetype of geographic abatement (GA) in a cuticular drusen (CD) phenotype in a 77-year-old woman as apparent on (A) blush photography, and (B) an ultra-widefield fluorescein angiography with agnate patterns of borderline drusen and macular CD. (C) Accustomed fundus autofluorescence did not admittance to quantify low quantitative fundus autofluorescence (qAF) levels in (D) articulation of Delori arrangement or in (E) a region-of-interest. (F) Near-infrared reflectance in aggregate with (G) an added abyss imaging optical adherence tomography B-scan and (H) abstract inset of the breadth of the band browse showed greater qAF ethics in GA lobules associated with focal retinal colorant epithelium preservation.

The everyman qAF-8 levels were acquired for the RMD/SDD phenotype, possibly because of appearance of autofluorescence by SDD aloft the RPE. It has additionally been appropriate for RMD that its associated choroidal dearth and attendance of SDD ability be affiliated with a slowing of the beheld cycle,26 bargain rod and cone densities due to alien retinal atrophy,27 or a altered agreement of lipofuscin, constant in bargain lipofuscin accession and/or lower qAF measures.8

One of the strengths of this abstraction was our accomplice of participants earlier than 60 years of age, in allegory to the adolescent accomplice advised by Gliem et al.8 This affection accustomed us to use qAF in patients best acceptable to accept backward stages in AMD. For instance, macular complications of RPE-related changes, such as GA, generally arise added frequently in patients with AMD who are earlier than 60 years.

We additionally evaluated thoroughly the non-neovascular AMD date application advanced multimodal imaging techniques for absolute drusen phenotyping, abnormally backward non-neovascular AMD patients who accept added progressed fundus changes acute altered assay strategies to access reliable data. For instance, the use of optical adherence tomography angiography can acknowledge whether choroid capillaries are present, acceptance bright adverse amid GA and abatement accessory to addition ache or for the apprehension of subclinical choroidal neovascularization.28

Finally, we alone advised pseudophakic patients with bright afterwards abridged to abstain the accretion airheadedness of lens opacities with age, which makes the constant qAF ethics added inaccurate. Likewise, a baby capsulotomy in an opacified abridged ability be visually able for the patient, but not for the qAF method.

Also, the abstraction had several limitations. The sample admeasurement was baby partly because of our austere admittance belief aiming to accommodate alone patients with aerial angel affection and assertive audible phenotypes. There were additionally periods of time at which the centralized advertence bare recalibration in both facilities. The ambition was to accumulate the abstracts as constant as possible, but baby errors may accept accumulated amid calibrations. Some patients beneath to be adjourned by this investigational device, possibly biasing the results.

The qAF imaging address itself has built-in biologic limitations to its accommodation for anon barometer lipofuscin absorption in the RPE. Differential administration of lipofuscin aural RPE cells29 or agreement of lipofuscin fluorophores30 could affect acuteness of autofluorescence; therefore, these phenomena charge to be addressed in approaching studies. However, the FAF spectra of macular fluorophores additionally accept aerial abeyant for noninvasive anatomization into spatially and molecularly absolute identification through hyperspectral imaging.31,32 Finally, the qAF measures may be bargain by absorbers of the action or emitted fluorescence ablaze such as melanin granules30 or subretinal drusenoid deposits.33

In summary, our abstraction complemented that of Gliem et al.,8with agnate allegation on an earlier cohort. We concluded, for our baby abstraction groups, that qAF-8 is college in advantageous eyes than in eyes with AMD, suggesting that the antecedent of autofluorescence, lipofuscin, may not be as adverse as it was thought. This is constant with alternating theories that lipofuscin sequesters oxidative articles to anticipate damage, or that it is a aloof bystander.34 Thus, qAF may be a advantageous absolute aftereffect capricious for analysis trials of AMD. Prospective studies with beyond groups of patients are adumbrated to validate these conclusions.

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It would be advantageous to appraise qAF in the junctional zone35 and/or lobules of GA36 to chase recommendations from the Classification of Abatement Consensus Meetings37 with commendations to qAF levels alfresco atrophic areas38 and aural the grayish rather than atramentous lobules of abatement in some GA subtypes.39 We will present our allegation application qAF in GA due to RMD.40 Since the Spectralis combines qAF and SD-OCT in absolute registration, enabling a spatiotemporal illustration of RPE bloom and retinal anatomy in combination, the qAF adjustment provides a advantageous apparatus to abstraction this non-neovascular backward AMD date further.

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