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ORIGINAL ARTICLE
Year : 2017  |  Volume : 4  |  Issue : 2  |  Page : 61-65

Correlation of fundus autofluorescence patterns in early dry age-related macular degeneration with best-corrected visual acuity


Department of Ophthalmology, Faculty of Medicine, Alexandria University, Alexandria, Egypt

Date of Web Publication17-Nov-2017

Correspondence Address:
Ahmed Mahmoud Ragab
309 Malak Hefney Street, Alexandria
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/erj.erj_7_17

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  Abstract 


Background: Correlation of abnormal fundus autofluorescence (FAF) patterns with best-corrected visual acuity (BCVA).Aim: This study aims to evaluate FAF patterns in eyes with early dry age-related macular degeneration (AMD) and correlate these patterns with logarithm of minimum angle of resolution (logMAR) BCVA. Settings and Design: Institutional, descriptive prospective cohort study. Subjects and Methods: One hundred fifty-nine eyes of 103 patients with early dry AMD were recruited. FAF imaging was done for all patients with the aid of confocal scanning laser ophthalmoscopy (cSLO). BCVA was recorded for all patients using logMAR BCVA. Statistical Analysis Used: Data were fed to the computer and analyzed using IBM SPSS software package Version 20.0 (Armonk, NY, USA: IBM Corp). Kruskal–Wallis test for abnormally quantitative variables, to compare between more than two studied groups and post hoc (Dunn's multiple comparisons test) for pairwise comparisons. The significance of the obtained results was judged at the 5% level. Results: Seven FAF patterns have been identified (normal, minimal change, focal increased, linear, patchy, reticular, and speckled pattern). The mean logMAR BCVA among eyes with different FAF patterns was significantly variable. Eyes with patchy FAF pattern had the best mean BCVA (0.15 ± 0.0), while eyes with linear FAF pattern had the worst mean BCVA (0.52). Conclusions: The mean logMAR BCVA was statistically significant variable among different FAF patterns in eyes with early AMD suggesting a possible link between each FAF pattern and the visual prognosis. This finding can aid in determining the visual potential of eyes with early AMD according to FAF pattern in large samples studies.

Keywords: Autofluorescence patterns in dry age-related macular degeneration, dry age-related macular degeneration, fundus autofluorescence


How to cite this article:
Shaarawy AS, Bessa AS, Lolah MA, Ragab AM. Correlation of fundus autofluorescence patterns in early dry age-related macular degeneration with best-corrected visual acuity. Egypt Retina J 2017;4:61-5

How to cite this URL:
Shaarawy AS, Bessa AS, Lolah MA, Ragab AM. Correlation of fundus autofluorescence patterns in early dry age-related macular degeneration with best-corrected visual acuity. Egypt Retina J [serial online] 2017 [cited 2018 May 26];4:61-5. Available from: http://www.egyptretinaj.com/text.asp?2017/4/2/61/218589




  Introduction Top


Age-related macular degeneration (AMD) is a disease of elderly individuals which usually leads to irreversible blindness.[1] Lipofuscin accumulation with age in retinal pigment epithelium (RPE) and sub-RPE drusen deposition is the hallmark of AMD which leads to oxidative stress and deterioration of RPE function and cell death.[2],[3]

Fundus autofluorescence (FAF) imaging is a noninvasive technique for fundus imaging which depends on autofluorescence property of lipofuscin.[4],[5] Increased RPE lipofuscin results in hyperfluorescence,[6.7] while atrophic areas with geographic atrophy (GA) exhibit hypofluorescence.[8],[9] FAF imaging may be superior to color fundus photography and angiography in patients with early AMD.[10],[11] Eight abnormal FAF patterns have been described by Bindewald that are associated with AMD; normal pattern characterized by the absence of abnormal autofluorescence on FAF images, even in the presence of drusen on color fundus photographs, minimal change pattern identified by a very limited irregular increase or decrease of background FAF without a characteristic topographic pattern, focal increased pattern defined by the presence of at least a well-defined one spot (200 μm diameter) of increased FAF much brighter than the surrounding background fluorescence, patchy pattern which demonstrates the presence of at least one ill-defined large area (200 μm diameter) of markedly increased FAF, linear pattern which shows at least one well-defined linear area of a markedly increased FAF, lace-like pattern is defined by multiple-branching linear structures of increased FAF that form a lace-like distribution, reticular pattern which is defined by the presence of ill-defined multiple small areas of decreased FAF and more typically located in a superotemporal location rather than the macular area, and speckled pattern which is characterized by simultaneous presence of multiple small areas of irregularly punctuate or linear increased and decreased FAF that extend beyond the macular area and may cover the entire posterior fundus.[10]

The aim of this study is to identify the distribution of different abnormal FAF patterns among early AMD patients and correlate these patterns to the logarithm of minimum angle of resolution (logMAR) best-corrected visual acuity (BCVA) to identify patterns which may be correlated to good visual prognosis and other ones that carry poor visual outcome. Accordingly, FAF imaging may be used as a prognostic test for classifying the patients according to each pattern.


  Subjects and Methods Top


The study was conducted at Alexandria faculty of medicine, main university hospital between January 2015 and December 2015, Alexandria, Egypt. The study adhered to the tenets of the Declaration of Helsinki. Institutional Review Board/Ethics Committee approval for human studies has been obtained. Patients with early dry AMD were eligible for enrollment. The inclusion criteria were patients with clinically documented dry AMD. Exclusion criteria were patients with choroidal neovascularization membrane (CNV) from any cause, patients with any retinal pathology other than dry AMD, patients with previous retinal intervention, myopic patients more than −6 D, also patients with visually significant cataract or media opacity that can affect imaging quality. Patients who had other ocular pathologies, such as uveitis, previous trauma, patients with compromised retinal or optic nerve function as a result of glaucoma, current use of oral or topical anti-inflammatory agents (steroidal or nonsteroidal) for intraocular inflammatory diseases, history of steroid responsiveness, were also excluded from the study.

One hundred fifty-nine eyes of 103 patients with early AMD were enrolled in this observational cross sectional study. All patients were informed about the design of the study and the procedure involved, and all gave written informed consent. A complete patient's evaluation was performed, which included the patient's age, medical, and ocular history. A detailed preoperative ophthalmic evaluation including slit-lamp examination, intraocular pressure measurement with Goldman applanation tonometry, and dilated fundus examination was performed. In addition, BCVA using Snellen acuity chart was examined then converted to logMAR BCVA for statistical analysis. Color fundus photography (Topcon Retinal Camera, TRC50X, Japan) and SD-OCT (Spectralis OCT; Heidelberg Engineering, Germany) were performed for all patients. FAF images were obtained with confocal scanning laser ophthalmoscopy (cSLO) (Heidelberg Retina Angiograph, HRA classic, Heidelberg Engineering, Germany). For excitation 488 nm argon blue laser was used and emission is recorded above 500 nm with a barrier filter. For acquisition of FAF images, the best 100 single images were aligned, and a mean image was generated. Images of FAF of early AMD eyes were assessed and classified according to the classification of FAF patterns in early age-related macular disease study as described by Bindewald et al.[10] In Bindewald et al. study normal FAF pattern was identified by the absence of abnormal alterations on FAF images, even in the presence of soft or hard drusen. Eyes that named with minimal change pattern showed very limited irregular increase or decrease of background FAF without an obvious topographic pattern. Bindewald and his colleagues described the focal increased pattern if there was at least a well-defined one spot (200 μm diameter) of markedly increased FAF much brighter than the surrounding background fluorescence, while they described eyes with at least one ill-defined large area (200 μm diameter) of markedly increased FAF that is brighter than the surrounding background fluorescence as eyes with patchy pattern. The borders of the areas of abnormal hyperautofluorescence in this type are typically less well defined than the previous pattern. The linear pattern was defined by the presence of at least one well-demarcated linear area of marked hyperautofluorescence. The reticular pattern was identified by the presence of multiple small areas of decreased FAF that is usually ill defined. They described the speckled FAF pattern as the simultaneous presence of a variety of FAF abnormalities in a larger area of the FAF image that often extend outside the macular area and even the posterior pole. Lace-like pattern was seen as multiple-branching linear structures of increased FAF that form a lace-like structure.

Data were fed to the computer and analyzed using IBM SPSS software package Version 20.0 (Armonk, NY, USA: IBM Corp). Kruskal–Wallis test for abnormally quantitative variables, to compare between more than two studied groups and post hoc (Dunn's multiple comparisons test) for pairwise comparisons. The significance of the obtained results was judged at the 5% level.


  Results Top


In all 103 patients of them, 78 were females (75.72%) and 25 were males (24.27%) with mean age 63.35 ± 4.8. In the studied patients, 159 eyes showed signs of early dry AMD.

All studied eyes showed different forms of drusen as a sign of dry AMD with and without pigmentary changes. These drusen were not always associated with a change in autofluorescence signal. Seven patterns of FAF have been identified in this study with a wide variation in their prevalence; normal pattern, minimal change pattern, focal increased pattern, patchy pattern, reticular pattern, linear pattern, and speckled pattern. Focal increased pattern was the most prevalent pattern in the 159 eyes as it was demonstrated in 54 eyes (34%) followed by the normal pattern in 48 eyes (30.2%) followed by the minimal change pattern which was present in 30 eyes (18.9%). On the other hand, the least common type was the speckled pattern as only three eyes depicted this pattern (1.9%). The remaining patterns were distributed in the following descending frequency: Patchy pattern in 12 eyes (7.5%), reticular and linear patterns were equally prevalent in 6 eyes for each pattern (3.8% each). Interestingly, lace-like pattern which has been described in Bindewald et al., the study could not be identified in this study. The distribution of FAF patterns was variable in the studied eyes [Table 1].
Table 1: Distribution of the studied cases according to fundus autofluorescence phenotypes in early dry age-related macular degeneration and its correlation with visual acuity

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The mean logMAR BCVA was 0.31 ± 0.23 among studied eyes. The difference in mean logMAR BCVA among different patterns was statistically significant [Table 1] and [Figure 1], [Figure 2].
Figure 1: Distribution of the studied cases according to fundus autofluorescence phenotypes in early dry age-related macular degeneration and its correlation with visual acuity.

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Figure 2: Distribution of the studied cases according to fundus autofluorescence phenotypes in early dry age-related macular degeneration and its correlation with visual acuity.

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Eyes with patchy pattern showed the best mean logMAR BCVA (0.15 ± 0.002), followed by eyes which demonstrated normal FAF pattern (0.24 ± 0.16), whereas eyes with linear pattern were linked to the worst visual potential (0.52 ± 0.001). Other patterns: minimal change pattern, focal increased pattern, reticular pattern, and speckled pattern were associated with modest decrease in visual acuity as compared to eyes with patchy pattern or normal pattern or linear pattern [Table 1] and [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9].
Figure 3: Normal pattern. A 58-year-old female patient fundus picture and fundus autofluorescence image. The color fundus picture shows multiple drusen. On the other hand, no abnormal fundus autofluorescence pattern could be identified.

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Figure 4: Minimal change pattern. A 62-year-old female patient fundus picture and fundus autofluorescence image. The color fundus picture shows different drusen types at the macular area, while fundus autofluorescence image shows minimal alternations in the fundus autofluorescence signal.

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Figure 5: Focal increase pattern. A 71-year-old female patient fundus picture and fundus autofluorescence image. The color fundus picture shows multiple drusen mainly large soft type. Fundus autofluorescence image shows small focal hyperautofluorescence spots.

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Figure 6: Reticular pattern. A 60-year-old male patient fundus picture and fundus autofluorescence image. The color fundus picture shows multiple hard drusen along the superotemporal arcade. Fundus autofluorescence image shows reticular hypofluorescence corresponding to the site of the lesions.

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Figure 7: Linear pattern. A 74-year-old female patient fundus picture and fundus autofluorescence image. The color fundus picture shows multiple soft drusen deposition. Fundus autofluorescence image showed vertical linear hyperfluorescence at the medial macula with some spots of hyperfluorescence spots temporal to the macula.

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Figure 8: Patchy pattern. A 75-year-old female patient fundus picture and fundus autofluorescence image. The color fundus picture shows soft macular drusen deposition. Fundus autofluorescence image of the same patient depicts a large area of hyperautofluorescence.

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Figure 9: Speckled pattern. A 57-year-old male patient fundus picture and fundus autofluorescence image. The color fundus picture shows multiple mixed drusen deposition with pigmentary changes. Fundus autofluorescence image demonstrates alternating spots of hypo- and hyper-autofluorescence.

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  Discussion Top


cSLO has been documented as an effective tool in demonstrating autofluorescence property of lipofuscin in vivo. FAF was found to be superior in detecting alternations that take place in RPE due to drusen deposition and lipofuscin accumulation with age to color fundus imaging and fundus fluorescein angiography.[12] Several studies have been conducted to set a classification system for eyes with early AMD depending on either color fundus pictures or angiography.[13] However, many eyes with early AMD may show no abnormality with these imaging modalities.[12] Accordingly, a new classification of early AMD has been described depending on the noninvasive FAF imaging.[10]

Changes seen on color fundus photography in studied eyes were not always associated with changes in FAF images. This agrees with FAM (FAF in AMD) study in which visible changes on color fundus images were associated with no FAF alternations.[10]

Recently, Bindewald et al., have described eight patterns of early AMD according to FAF imaging with the aid of cSLO. Alterations in FAF in eyes with early AMD were classified into eight phenotypic patterns including normal, minimal change, focal increased, patchy, linear, lace-like, reticular, and speckled.[10] In this study, it was found that there is a correlation between each FAF phenotype in early AMD and the BCVA. In addition, distribution of the FAF patterns among studied eyes was variable with focal increased pattern being the most common pattern followed by the normal pattern in contrast to Bindewald et al., study where speckled pattern was the most common pattern. Conversely, the speckled pattern was the least prevalent pattern in the studied sample while lace-like pattern failed to be demonstrated, interestingly, lace-like pattern was the least common in Bindewald et al., a study which is comparable to the current study findings as it failed to be demonstrated in the studied sample. Similarly, the prevalence of FAF patterns was different in Batioǧlu et al., study where the most frequent pattern was the reticular pattern followed by the minimal change pattern, while speckled pattern was the least common type which agrees with the present study followed by lace-like pattern and linear pattern.[14] The variations among other studies and the current study regarding FAF patterns distribution among studied eyes may be linked to the difference in characteristics of the patient cohort.

The current study revealed that the mean logMAR BCVA was variable among different FAF patterns with a mean BCVA of 0.31 ± 0.23 among the studied eyes. This was worse than the mean logMAR in eyes recruited for Batioǧlu et al., study where it was 0.17 at the baseline. Eyes with patchy pattern demonstrated better BCVA compared to other types, while eyes with focal increased pattern showed the worst BCVA. This may be linked to more damage caused by this distribution to RPE and consequently the photoreceptors. Although patchy pattern has been linked to a better visual acuity in this study, it has been demonstrated that eyes with this type were more likely to develop choroidal neovascularization (CNV) on follow-up as demonstrated by Batioǧlu et al.[14]

The current study has several limitations. Although FAF imaging is a noninvasive tool to demonstrate lipofuscin, it is difficult to obtain a good quality signal in the presence of a cataract. In addition, the description of FAF patterns may be difficult to be reproducible as it is usually affected by intra- and inter-observer variability in describing each pattern. Furthermore, some eyes with early AMD may show mixed patterns of FAF. Another point to be considered is that approximately 30% of early dry AMD eyes showed normal FAF scan in this study, this might make the use of FAF imaging as a sole tool for diagnosis or follow-up of early dry AMD patients inappropriate. Thus, FAF imaging could be used as a complementary tool in the assessment of early AMD eyes with other imaging modalities.


  Conclusions Top


FAF is a rapid, noninvasive tool in evaluating patients with dry AMD. Fundus autofluorescence imaging for patients with early AMD could be used as an effective tool with other imaging modalities to identify visual potential and visual prognosis in those patients guided by their FAF pattern. Further studies with the development of new software to assess the described patterns more precisely might provide reproducible patterns to diagnose eyes with early AMD. Follow-up of these patterns may help predict each pattern behavior and determine patterns that carry the highest risk for progression to GA or wet AMD.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Friedman DS, O'Colmain BJ, Muñoz B, Tomany SC, McCarty C, de Jong PT, et al. Prevalence of age-related macular degeneration in the United States. Arch Ophthalmol 2004;122:564-72.  Back to cited text no. 1
    
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Dorey CK, Wu G, Ebenstein D, Garsd A, Weiter JJ. Cell loss in the aging retina. Relationship to lipofuscin accumulation and macular degeneration. Invest Ophthalmol Vis Sci 1989;30:1691-9.  Back to cited text no. 7
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Lois N, Owens SL, Coco R, Hopkins J, Fitzke FW, Bird AC, et al. Fundus autofluorescence in patients with age-related macular degeneration and high risk of visual loss. Am J Ophthalmol 2002;133:341-9.  Back to cited text no. 11
    
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Arnold JJ, Quaranta M, Soubrane G, Sarks SH, Coscas G. Indocyanine green angiography of drusen. Am J Ophthalmol 1997;124:344-56.  Back to cited text no. 13
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