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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 2  |  Issue : 1  |  Page : 40-46

Evaluation of fundus autofluorescence patterns in patients with central serous chorioretinopathy - A prospective, observational study


Department of Retina, Visakha Eye Hospital, Visakhapatnam, Andhra Pradesh, India

Date of Submission07-Jun-2022
Date of Decision26-Jul-2022
Date of Acceptance27-Jul-2022
Date of Web Publication05-Oct-2022

Correspondence Address:
Dr. Vasanthi Sannapuri
Department of Retina, Visakha Eye Hospital, Visakhapatnam, Andhra Pradesh - 530 017
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jocr.jocr_7_22

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  Abstract 


Aim: The aim of the study was to evaluate the patterns of fundus autofluorescence (FAF) and analyze the association between FAF and swept-source optical coherence tomography (SS-OCT) in idiopathic central serous chorioretinopathy (CSCR). Materials and Methods: 65 eyes of 65 patients were prospectively included in this study. Patients underwent a complete ophthalmologic examination. We classified patterns on FAF imaging into five types as blocked FAF, mottled FAF, hyper-FAF, hyper/hypo-FAF, and descending tract pattern. Each FAF pattern was then analyzed based on the SS-OCT findings. Results: Blocked FAF pattern was seen in 47.69% of patients, mottled in 7.69%, hyper in 23.07%, hyper/hypo in 18.46%, and descending tract in 3.07%. There is a significant difference between FAF patterns in all subjects (P < 0.0001). The blocked FAF pattern (mean [M] = 0.20, standard deviation [SD] = 0.14) showed the best visual acuity among all others. The descending tract FAF pattern group (M = 0.54, SD = 0.08) and hyper/hypo-FAF pattern group (M = 0.38, SD = 0.28) showed the least favorable visual prognosis in our study. The intact ellipsoid zone on the SS-OCT was mostly found in the blocked FAF group, and the disrupted ellipsoid zone was commonly exhibited in the hyper/hypo and descending tract groups. Disrupted external limiting membrane line on the SS-OCT was seen in one patient of the descending tract group only. Conclusions: The association between FAF and SS-OCT findings was analyzed in patients with idiopathic CSCR in our study. Detailed investigation using FAF could help estimate the duration of CSCR.

Keywords: Central serous chorioretinopathy, fundus autofluorescence, fundus fluorescence angiography, swept-source optical coherence tomography, visual acuity


How to cite this article:
Sannapuri V, Palimar V, Umamaheshwar V. Evaluation of fundus autofluorescence patterns in patients with central serous chorioretinopathy - A prospective, observational study. J Ophthalmol Clin Res 2022;2:40-6

How to cite this URL:
Sannapuri V, Palimar V, Umamaheshwar V. Evaluation of fundus autofluorescence patterns in patients with central serous chorioretinopathy - A prospective, observational study. J Ophthalmol Clin Res [serial online] 2022 [cited 2022 Nov 29];2:40-6. Available from: http://www.jocr.in/text.asp?2022/2/1/40/357896




  Introduction Top


Central serous chorioretinopathy (CSCR) is a multifactorial disease of eye with complex pathogenesis occurring in young- to middle-aged adults, characterized by serous detachment of the neurosensory retina at the posterior pole. It is associated with leakage of fluid at the level of retinal pigment epithelium (RPE).[1],[2],[3],[4],[5],[6],[7],[7],[8],[9] Patients with acute CSCR complain blurred vision, scotoma, and metamorphopsia. The acute form of CSCR generally resolves spontaneously in majority of cases, with a return to normal visual acuity.[10],[11],[12] However, the chronic form of this disease is often associated with visual acuity decline and atrophic and degenerative changes of the RPE.[6] Investigation tools such as fundus fluorescein angiography and indocyanine green angiography have provided insight about hemodynamics and fluid dynamics. Optical coherence tomography has provided additional clues about the size and elevation of detachments,[13] the development of retinal atrophy, and the correlates to visual acuity in resolved CSCR.[14]

Fundus autofluorescence (FAF) is a noninvasive method that provides functional images of the fundus by employing stimulated emission of light from naturally occurring fluorophores, the most significant being lipofuscin. Lipofuscin is generated as a by-product of the retinoid cycle after the phagocytosis of photoreceptor outer segments by the RPE and demonstrates fluorescence between 500 nm and 750 nm with peak emission at 630 nm.[15] Since the accumulation of lipofuscin occurs in RPE cells because of their unique metabolic role,[16],[17],[18] FAF imaging may provide clues to the pathobiology of CSCR. FAF imaging was done using ZEISS CLARUS 700 WIDEFIELD FUNDUS CAMERA (Carl Zeiss Meditec AG, Germany), with a central 133° field. In this study, FAF using green light (FAF-GREEN-WIDEFIELD) was considered. Morphological retinal changes in the outer retinal layer also lead to abnormal FAF, resulting in abnormal retinol metabolism and lipofuscin accumulation. An abnormal FAF was defined as either an increased or decreased FAF signal when compared with the normal background FAF, outside of such lesions.[19] FAF imaging is classified into five patterns as blocked FAF, mottled FAF, hyper-FAF, hyper/hypo-FAF, and descending tract pattern. A pattern was defined as blocked FAF if there were no changes or uniform changes in decreased autofluorescence where subretinal fluids (SRFs) existed [Figure 1]; mottled FAF showed a grainy or coarse region of increased FAF when compared with the normal surrounding background fluorescence [Figure 2]; hyper-FAF showed an increased FAF signal when compared with that outside the lesion (referred to as normal FAF) [Figure 3]; hyper/hypo-FAF was characterized by a mixed form of hyperautofluorescence and hypoautofluorescence [Figure 4]; and descending tract exhibited a downward leading swathe of decreased autofluorescence originating from the posterior pole to extend below the level of the inferior arcade [Figure 5].[20]
Figure 1: FAF image shows a homogeneous background fluorescence and a uniform change from the FAF of the normal background (blocked FAF). FAF: Fundus autofluorescence

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Figure 2: FAF image shows a grainy or coarse region of increased FAF compared with the FAF of normal background depicting mottled FAF. FAF: Fundus autofluorescence

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Figure 3: FAF image shows an increase in FAF intensity around the macula and in the temporal area, compared with the FAF of normal background (hyper-FAF). FAF: Fundus autofluorescence

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Figure 4: FAF image with hyperautofluorescence and hypoautofluorescence (hyper/hypo-FAF). FAF: Fundus autofluorescence

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Figure 5: FAF image showing a downward leading swathe of decreased autofluorescence, originating from the posterior pole and extending below the level of the inferior arcade (descending tract). FAF: Fundus autofluorescence

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There is no major prospective study evaluating whether any particular FAF pattern is associated with better prognosis in terms of visual acuity. There is no study that correlated relation between swept source-optical coherence tomography (SS-OCT), optical coherence tomography angiography, and FAF patterns.


  Materials and Methods Top


Inclusion criteria

  1. Patients diagnosed as idiopathic CSCR.


Exclusion criteria

  1. Patients who have undergone laser photocoagulation or photodynamic therapy for CSCR
  2. History of usage of steroids
  3. History of any ocular surgery
  4. Patients with intraocular inflammation and optic disc pit.


The data required for sample size calculation were collected from the reference article.[21]

n = [Z1-α/2 × √P0 × (1 − P0) + Z1-β × √Pa (1 − Pa)]2/(P0 − Pa)2

= [1.96 × √0.58 × (1 − 0.58) + 0.84 × √0.389 × (1 − 0.389)]2/(0.58 − 0.389)2 = 52.

Sample size = 52

The number of patients/eyes included in our study is 65.

65 eyes of 65 patients from our institute were prospectively included in this study. Informed written consent was obtained from all the patients. Patients underwent a complete ophthalmologic examination including best-corrected visual acuity (BCVA), slit-lamp biomicroscopy, intraocular pressure measurement, color fundus photography, fundus fluorescence angiography, and posterior segment optical coherence tomography done using swept-source optical coherence tomography (DRI OCT Triton, Topcon Europe Medical BV Version 1.16). FAF was done using ZEISS CLARUS 700 WIDEFIELD FUNDUS CAMERA (Carl Zeiss Meditec AG, Germany), with a central 133° field. ZEISS CLARUS illuminates in two wavelength ranges, FAF-Blue (435–500 nm) and FAF-Green (500–585 nm). All fluorophores that absorb light within those ranges will be detected if the fluorophores emit light within the band pass filter range, which is 532–650 nm for FAF Blue and 630–750 nm for FAF-Green. In this study, FAF using green light (FAF-GREEN-WIDEFIELD) was considered.

Data were analyzed by Microsoft Excel and GraphPad Prism software. Data were summarized by mean (M) ± standard deviation (SD) for continuous data and percentages for categorical data. The comparison between variables/follow-ups was done by Chi-square test/Fisher's exact test. The comparison between groups was done by one-way analysis of variance test for continuous normal data and Kruskal–Wallis test for continuous nonnormal data. The swept-source optical coherence tomography (SS-OCT) characteristics among FAF patterns were done by a single proportion test. All P < 0.05 was considered statistically significant.


  Results Top


During the study period from December 2019 to June 2021, data from a total of 75 patients were collected prospectively, out of which seven of them were excluded due to history of usage of steroids and three of them were excluded as they had already undergone laser photocoagulation for CSCR. A total of 65 patients were included in the analysis.

The mean age group in the study is 39.8 years and SD is 7.5 years, with the range 19–58 years. Only one patient is in the range of 19–26 years, 11 patients in the range of 27–34 years, 31 patients in the range of 35–42 years, 16 patients in the range of 43–50 years, and 6 patients in the range of 51–58 years. The maximum number of patients are in the range of 35–42 years [Table 1].
Table 1: The age (years) distribution of all subjects

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Among the study population, 58 (89.23%) were male and 7 (10.77%) were female [Table 2].
Table 2: The gender distribution of all subjects

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Right eye is affected in most of the patients (38, 58.46%) than the left eye (27, 41.54%) [Table 3].
Table 3: The distribution of all subjects of the affected eye

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Out of 65 patients, blocked FAF pattern is seen in 31 patients, mottled FAF pattern is seen in 5 patients, hyper-FAF pattern is seen in 15 patients, hyper/hypo-FAF pattern is seen in 12 patients, and descending tract FAF pattern is seen in 2 patients. Blocked FAF pattern is the most common pattern seen in 31 patients followed by hyper-FAF seen in 15 patients. Descending tract FAF is the least common FAF pattern. There is a significant difference between FAF patterns in all [P < 0.0001, [Table 4], and [Figure 6].
Figure 6: The cluster bar diagram for the comparison between FAF patterns in all subjects. FAF: Fundus autofluorescence

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Table 4: The comparison between fundus autofluorescence patterns in all subjects

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The mean LogMAR BCVA value of the blocked FAF pattern is 0.20. The mean LogMAR BCVA value of the mottled FAF pattern is 0.29. The mean LogMAR BCVA value of the hyper-FAF pattern is 0.32. The mean LogMAR value of the hyper/hypo-FAF pattern is 0.38 and the descending tract FAF pattern is 0.54. Blocked FAF showed the best visual acuity among all others. Hyper/hypo-FAF and descending tract FAF patterns showed the least favorable visual prognosis. The difference between FAF patterns and baseline BCVA of the affected eye-logMAR values of all subjects is statistically significant. P = 0.022, [Table 5], and [Figure 7].
Figure 7: The simple mean bar diagram for the comparison between FAF patterns and baseline best-corrected visual acuity of affected eye-logMAR values of all subjects. FAF: Fundus autofluorescence

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Table 5: The comparison between fundus autofluorescence patterns and baseline best-corrected visual acuity of affected eye (LogMAR) of all subjects

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Disruption of external limiting membrane (ELM) is seen in only 1 subject in descending tract group [Table 6] and [Figure 8]. The intact ellipsoid zone on the SS-OCT was mostly found in the blocked FAF group which also shows sub retinal fluid in the region where the fundus auto-fluorescence intensity decreases [Figure 9] and the disrupted ellipsoid zone was commonly exhibited in the hyper/hypo and descending tract groups. Pigment epithelial detachment is seen in only 2 subjects of blocked FAF pattern and hyper FAF pattern groups.
Figure 8: The clustered bar showing swept-source optical coherence tomography characteristics among FAF patterns. FAF: Fundus autofluorescence, PED: Pigment epithelial detachment, EZ: Ellipsoid zone, ELM: External limiting membrane, OS: Outer segment

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Figure 9: Swept-source optical coherence tomography image showing subretinal fluid in the region where the fundus autofluorescence intensity decreased. This optical coherence tomography pattern is seen in the blocked fundus autofluorescence pattern group

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Table 6: Swept-source optical coherence tomography characteristics among fundus autofluorescence patterns

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  Discussion Top


In our study, FAF patterns were grouped as blocked (47.69%), mottled (7.69%), hyper (23.07%), hyper/hypo (18.46%), and descending tract (3.07%). There is a significant difference between FAF patterns in all patients (P < 0.0001).

Outer segment elongation and sub retinal deposits seen in 2 subjects in the mottled group [Figure 10]. Outer segment elongation and loss of photoreceptors results in increased transmission of retinal pigment epithelium fluorescence seen in 6 subjects in the hyper-FAF pattern group [Figure 11]. Outer segment elongation is seen in the maximum number of subjects in the hyper-FAF pattern group [P < 0.0001]. Outer segment elongation is not seen in the blocked FAF group. Pigment epithelial detachment is seen in only blocked FAF and hyper/hypo FAF groups [P < 0.0001]. Disruption of ellipsoid zone is seen in 9 subjects in the hyper/hypo-FAF pattern group [Figure 12]. Disruption of external limiting membrane (ELM) is seen in only descending tract FAF group [P < 0.0001] [Figure 13].
Figure 10: Optical coherence tomography image showing subretinal fluid and shows outer segment elongation and subretinal deposit. This pattern is seen in the mottled fundus autofluorescence pattern group

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Figure 11: Optical coherence tomography image showing elongation of the photoreceptor's outer segments around the macula and loss of photoreceptor of the temporal area that results in increased transmission of retinal pigment epithelium fluorescence. This pattern of optical coherence tomography is seen in the hyperfundus autofluorescence pattern group

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Figure 12: Optical coherence tomography showing intact external limiting membrane and disruption of the ellipsoid zone. This pattern of optical coherence tomography is seen in the hyper/hypo-fundus autofluorescence pattern group

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Figure 13: Optical coherence tomography images showing the disruption of the external limiting membrane and the ellipsoid zone. This type of optical coherence tomography is seen in descending tract pattern

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In our study, the blocked FAF pattern (M = 0.20, SD = 0.14) showed the best visual acuity among all others. The descending tract FAF pattern group (M = 0.54, SD = 0.08) and hyper/hypo-FAF pattern group (M = 0.38, SD = 0.28) showed the least favorable visual prognosis.

There is a significant association between FAF patterns and duration of symptoms (in days) in our study (P < 0.0001). The mean duration of symptoms is shortest in the blocked FAF pattern (8.97 days) and symptom duration was longer in descending tract FAF (56 days) and hyper/hypo-FAF patterns (51.83 days).

Han et al.[21] conducted a retrospective study to evaluate the FAF patterns in patients with CSCR. FAF patterns were grouped as blocked, mottled, hyper, hyper/hypo, and descending tract patterns. The blocked FAF pattern is the most common pattern and descending tract FAF is the least common pattern in this study, which is similar to our study. SD OCT was used in their study. The limitation of their study was that it was a retrospective study. The advantages of our study are that it is a prospective observational study and SS OCT was used.

Lee et al.[5] reported FAF patterns in CSCR according to the course of the disease. They analyzed the FAF findings by dividing the patients with CSCR into acute, chronic, and sequelae. They observed hyper-FAF, hypo-FAF, or minimal changes at acute CSCR and discrete hyper-FAF dots or descending tract at chronic CSCR. They reported that these FAF findings helped with the more accurate assessment of the disease status and prognosis and helped with the proper treatment modality used in the clinic.

Zola et al.[22] reported FAF pattern changes over time in patients with chronic CSCR. The most common baseline pattern in their study was granular hypo-FAF. Subsequently, the earliest change in chronic CSCR was a diffuse hyper-FAF followed by the formation of hypo-FAF spots with time.

Dysli et al.[2] demonstrated shorter fluorescence lifetimes in acute CSCR and prolonged fluorescence lifetimes in chronic CSCR, due to increased accumulation of lipofuscin. In this study, they concluded that FAF change was associated with worse visual acuity.

Matsumoto et al.[23] reported that the increased mottled FAF seemed to originate from the elongated photoreceptor Outer Segment in the detached retina. We confirmed that this pattern is probably associated with the longer duration accumulation of SRF when compared with the blocked FAF. The hyperfluorescence FAF represents patchy accumulation in the subretinal space distributed generally and uniformly within the subretinal space i.e., increased diffused FAF is demonstrated. Symptom duration was longer in patients with hyper-FAF in comparison with the mottled FAF. The hypo-FAF was seen in damaged RPE due to the mechanical damages due to SRF and the accumulated autofluorescent materials. It was proposed that as hypo-FAF occurred in the hyper-FAF area, hyper-FAF and hypo-FAF coexist, so this pattern is demonstrated as hyper/hypo-FAF in our study. Fundus autofluorescence imaging in which downward leading area of decreased autofluorescence which originates from the posterior pole and extends below the level of inferior arcaded is termed as descending tract FAF pattern.

Limitations

  1. In our study, the sample size is less
  2. It is a single-centered study
  3. Follow-up was not done to detect the different the phases of CSCR.



  Conclusions Top


The association between FAF and SS-OCT findings was analyzed in patients with idiopathic CSCR in our study. Detailed investigation using FAF could help estimate the duration of CSCR.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Spaide RF, Campeas L, Haas A, Yannuzzi LA, Fisher YL, Guyer DR, et al. Central serous chorioretinopathy in younger and older adults. Ophthalmology 1996;103:2070-9.  Back to cited text no. 6
    
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Liegl R, Ulbig MW. Central serous chorioretinopathy. Ophthalmologica 2014;232:65-76.  Back to cited text no. 12
    
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Eandi CM, Chung JE, Cardillo-Piccolino F, Spaide RF. Optical coherence tomography in unilateral resolved central serous chorioretinopathy. Retina 2005;25:417-21.  Back to cited text no. 14
    
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Weinberger AW, Lappas A, Kirschkamp T, Mazinani BA, Huth JK, Mohammadi B, et al. Fundus near infrared fluorescence correlates with fundus near infrared reflectance. Invest Ophthalmol Vis Sci 2006;47:3098-108.  Back to cited text no. 15
    
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von Rückmann A, Fitzke FW, Bird AC. Distribution of fundus autofluorescence with a scanning laser ophthalmoscope. Br J Ophthalmol 1995;79:407-12.  Back to cited text no. 17
    
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Roisman L, Lavinsky D, Magalhaes F, Aggio FB, Moraes N, Cardillo JA, et al. Fundus autofluorescence and spectral domain OCT in central serous chorioretinopathy. J Ophthalmol 2011;2011:706849.  Back to cited text no. 19
    
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Imamura Y, Fujiwara T, Spaide RF. Fundus autofluorescence and visual acuity in central serous chorioretinopathy. Ophthalmology 2011;118:700-5.  Back to cited text no. 20
    
21.
Han J, Cho NS, Kim K, Kim ES, Kim DG, Kim JM, et al. Fundus Autofluorescence Patterns in Central Serous Chorioretinopathy. RETINA 9000; Publish Ah. Available from: https://journals.lww.com/retinajournal/Fulltext/publishahead/FUNDUS_AUTOFLUORESCENCE_PATTERNS_IN_CENTRAL_SEROUS.96116.aspx. [last accessed on 2020 Nov 12].  Back to cited text no. 21
    
22.
Zola M, Chatziralli I, Menon D, Schwartz R, Hykin P, Sivaprasad S. Evolution of fundus autofluorescence patterns over time in patients with chronic central serous chorioretinopathy. Acta Ophthalmol 2018;96:e835-9.  Back to cited text no. 22
    
23.
Matsumoto H, Kishi S, Sato T, Mukai R. Fundus autofluorescence of elongated photoreceptor outer segments in central serous chorioretinopathy. Am J Ophthalmol 2011;151:617-23.e1.  Back to cited text no. 23
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12], [Figure 13]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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