research article optical coherence tomography angiography...

Research ArticleOptical Coherence Tomography Angiography inCentral Serous Chorioretinopathy

Eliana Costanzo12 Salomon Yves Cohen1 Alexandra Miere1

Giuseppe Querques13 Vittorio Capuano1 Oudy Semoun1 Alarsquoa El Ameen1

Hassiba Oubraham1 and Eric H Souied1

1Department of Ophthalmology University Paris Est Creteil Intercity Hospital 94000 Creteil France2Department of Ophthalmology Second University of Naples Naples Italy3Department of Ophthalmology University Scientific Institute San Raffaele Milan Italy

Correspondence should be addressed to Eric H Souied esouiedhotmailcom

Received 7 August 2015 Revised 14 October 2015 Accepted 19 October 2015

Academic Editor Siamak Ansari-Shahrezaei

Copyright copy 2015 Eliana Costanzo et alThis is an open access article distributed under theCreativeCommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Purpose To analyze optical coherence tomography angiography (OCTA) findings in eyes with central serous chorioretinopathy(CSC) and to compare themwith those obtainedwithmultimodal imagingMethods A series of consecutive patients diagnosedwithCSC underwentOCTAandmultimodal imaging including spectral domainOCT fluorescein and indocyanine green angiographyOCTA images were performed at three main depth intervals automatically segmented outer retina manually adjusted outerretina and automatically segmented choriocapillaris Results Thirty-three eyes of 32 consecutive patients were analyzed OCTAshowed 3 main anomalies at the choriocapillaris the presence of dark areas (1933 eyes) which were frequently associated withserous retinal detachment presence of dark spots (733 eyes) which were frequently associated with retinal pigment epitheliumdetachment and presence of abnormal vessels (1233 eyes) which were frequently but not systematically associated with choroidalneovascularization as confirmed by multimodal imaging Conclusions OCTA revealed dark areas and dark spots which werecommonly observed An abnormal choroidal pattern was also observed in one-third of cases even when multimodal imagingdid not evidence any choroidal neovascularization Abnormal choroidal vessels should be interpreted with caution and we couldassume that this pathological choroidal vascular pattern observed in many CSC cases could be distinct from CNV

1 Introduction

Central serous chorioretinopathy (CSC) is a disorder char-acterized by episodes of macular serous retinal detachment(SRD) first described and characterized as a clinical entitywith fluorescein angiography (FA) [1ndash3] Several risk factorshave been identified such as glucocorticoid levels type Apersonality pregnancy uncontrolled systemic hypertensionuse of antibiotics bone marrow or organ transplantationinfection of the respiratory tract and infection by Heli-cobacter pylori [4ndash11] The disease may present with differentpatterns acute CSC ldquopersistingrdquo recurrent and chronic CSC[12] It usually occurs in young males but may be observedin older subjects of both genders CSC is characterized byretinal pigment epithelium (RPE) changes that are easily

observed on fundus autofluorescence (FAF) pictures serousretinal pigment epithelium detachment (PED) and episodesof SRD [12] FA usually shows areas of fluorescein leakageoften focal with a smokestack or inkblot pattern in acuteCSC [1ndash3] andmore widespread in chronic stages also calleddiffuse retinal pigment epitheliopathy [1 3] Indocyaninegreen angiography (ICGA) may show a hyperpermeabilityof the choroidal vessels and sometimes diffuse dye leakage[13] Optical coherence tomography (OCT) and especiallyenhanced-depth imaging (EDI) or swept source (SS) OCTshows a thick choroid and may allow better characterizingthe areas of PED and SRD [14 15] The disease may becomplicated by type 1 choroidal neovascularization (CNV)[16] However this complication may be difficult to diagnosebecause chronic CSC and type 1 CNV share many signs

Hindawi Publishing CorporationJournal of OphthalmologyVolume 2015 Article ID 134783 10 pageshttpdxdoiorg1011552015134783

2 Journal of Ophthalmology

on both FA and OCT CSC may also be associated withpolypoidal choroidal vasculopathy (PCV) and both entitiesmay be overlapped [12 17]

Optical coherence tomography angiography (OCTA) is anew noninvasive nondye depth-resolved technique whichmay be used to investigate patients with CSC The conceptof OCTA is the detection of changes in blood flow in thevessels in a static eye without need for dye injection [18]The amplitude of the signal returning from nonstatic featuresvaries rapidly over time When calculating the decorrelationof signal amplitude from repeated consecutive B-scans at thesame cross section a contrast between static and nonstatictissues is created and generates a vascular decorrelationsignal that enables visualizing 3-dimensional retinal andchoroidal vasculature [19] OCTA images may be studiedby isolated segmentation in different vascular layers thusallowing analyzing the vascular structure in detail with nodarkening due to a staining or leakage [18ndash21]The aim of thisstudy was to analyze OCTA findings in eyes with CSC and tocompare themwith those obtainedwithmultimodal imaging

2 Methods

21 Study Population A series of consecutive patients diag-nosed with CSC at the University Eye Clinic of Creteil wasexamined All patients with CSC were included that ispatients with a clinical history of CSC and 6 months of visualimpairment patients previously treated or treatment-naiveand newly diagnosed treatment-naive CSC patients Patientswith any associated previous or concomitant ophthalmo-logical conditions that could confound the interpretationof clinical and imaging findings for the diagnosis of CSC(ie subretinal fibrosis age-related macular degenerationmacular or retinal vascular disease vitreoretinal diseaseor retinal surgery and hereditary retinal dystrophy) wereexcluded from the study This prospective clinical studywas conducted in accordance with the French bioethicallegislation and with the Declaration of Helsinki for researchinvolving human subjects It received the favorable opinionof the ethics committee of the France Macula Federation

22 Study Protocol Patients underwent a complete oph-thalmic examination including best-corrected visual acu-ity (BCVA) measurement with Early Treatment DiabeticRetinopathy Study (ETDRS) chart slit-lamp examinationdilated-fundus biomicroscopy and standardized imagingprotocol using Spectralis HRA + OCT (Heidelberg Engi-neering Heidelberg Germany) which included FAF FAand ICGA SD-OCT andor EDI-OCT All patients alsounderwent OCTA using a commercially available RTVueXR Avanti with AngioVue (Optovue Fremont CA USA)An incorporated software algorithm called Split-SpectrumAmplitude Decorrelation Angiography (SSADA) generates3-dimensional en face angiograms through decorrelationof two merged consecutive orthogonal registration volumesautomatically centered at the macula or manually centeredat the lesion Each acquired OCTA volume (3 times 3mm)consisted of 304 times 304 A-scan in 26 seconds The A-scan

rate is 70000 scans per second Each orthogonal volumeregistration is corrected to minimize motion artifacts Bothorthogonal volume scans are combined with a motion cor-rection technology (MCT) to create a 3-dimensional imageof retinal and choroidal blood flow A coregistered OCT B-scan allows the visualization of the retinal structure RTVueXR Avanti has an automated segmentation at the superficialretinal capillary plexus deep retinal capillary plexus outerretina and choriocapillaris [19ndash22] The OCTA software wasused to manually adjust the automated segmentation andits relative depth in the retina and choroid OCTA imageswere analyzed at three main depth intervals automaticallysegmented outer retina manually adjusted segmentationbetween the RPE and 30 120583m beneath it called manuallysegmented outer retina in order to detect a blood flowin the RPE-Bruch membrane-choriocapillaris complex andautomatically segmented choriocapillaris

Three trained OCTA users (Eliana Costanzo AlexandraMiere and Alarsquoa El Ameen) acquired the images and per-formed a qualitative analysis to determine CSC features Toassess the microvascular architecture three retina specialists(Salomon Yves Cohen Giuseppe Querques and Eric HSouied) analyzed a 3times 3 scanning area at the three depths pre-viously described Patients with poor quality OCTA images(ie due to eye movement) were not included in the analysisMoreover eyes previously treated were analyzed separatelyfrom treatment-naive eyes

Our analysis included descriptive statistics (using Mic-rosoft Office Excel software version 140 2010 RedmondUSA) for demographics and main clinical data as well asqualitative descriptions of the imaging findings

3 Results

Thirty-three eyes of 32 consecutive patients (21 males 11females mean age 548 plusmn 104 years) diagnosed with CSCwere enrolled in this study Mean BCVA was 023 plusmn 025logMAR (range 0ndash08 logMAR corresponding to 2020 to20125) Nine eyes (273) had newly diagnosed treatment-naive CSC while 24 eyes (727) had a history of at least6 months of visual symptoms in the affected eye In 8 eyes(242) CSC was associated with type 1 CNV Table 1 showspatient demographics and clinical characteristics

For clarity the whole population was analyzed firstwith description of images obtained at different levels In asecond time naive eyes were compared to previously treatedeyes In a third time eyes with abnormal choroidal vesselpatterns were described with more details with an attemptof classification according to the pattern

31 Systematic Analysis of Different Depth OCTA Images inthe Whole Population

311 Outer Retina Automatically segmented outer retinaOCTA images detected the presence of an abnormal flowin 6 eyes (182) and no remarkable findings in 27 eyes(818) The manually segmented area revealed the presenceof an abnormal flow in 9 eyes (273) while 24 eyes (727)presented no particular abnormality

Journal of Ophthalmology 3

Table 1Main demographical and clinical findings of study patients

Patient 119899 33Male 119899 21Female 119899 11

Age y (mean plusmn SD) 548 plusmn 104BCVA logMAR (mean plusmn SD) 023 plusmn 025Acute CSC (first diagnosis) 119899 of eyes 9 (273)Chronic CSC 119899 of eyes 24 (727)

Previous treatment in chronic CSCPDT 8 (333)IVT 6 (25)PDT + IVT 3 (125)No treatment 7 (292)

119899 numbers y years SD standard deviation CSC central serous chori-oretinopathy PDT photodynamic therapy and IVT intravitreal injection ofAntivascular Endothelial Growth Factor

312 Choriocapillaris The choriocapillaris segmentation(from 30 120583m to 60 120583m beneath the RPE) was obtained forall patients except 2 It revealed three types of findings darkareas dark spots and abnormal choroidal vessels The darkareas corresponded to diffuse or focal foggy ill-defined low-detectable flow areas in the choriocapillaris layer (Figures1 and 2) The dark spots corresponded to black single ormultiple well-delineated areas where no flow was detectableat the choriocapillaris Dark spots could be observed aloneor associated with dark areas (Figure 3) Abnormal choroidalvessels corresponded to distinct well-delineated high-flowtangled pattern areas in the choriocapillaris layer (Figure 4)as well as an abnormal dilation of choroidal vessels Resultsof OCTA were compared to those obtained with the coreg-istered OCT B-scan provided by the software Results of themorphological correlation between dark areas and dark spotswith OCT changes are shown in Table 2 There was a highcorrespondence between the presence of dark areas and SRDwhich was observed in 17 out of 19 eyes

32 Comparison of Naive and Previously Treated Eyes Eyeswere classified into two different groups Group A includedtreatment-naive eyes (16 eyes 485) and group B includedpreviously treated eyes (17 eyes 515) In group B 8eyes (47) were treated with photodynamic therapy (PDT)6 (354) with intravitreal injection of anti-VEGF and 3(176) with both therapies In group A the analysis ofthe automatically segmented outer retina did not find anyabnormality The analysis of the manually segmented outerretina found in one case (625) a hyperdense abnormalsignal The choriocapillaris analysis was normal in 2 cases(125) but showed the presence of dark areas in 13 eyes(812) More precisely dark areas were isolated in 5 eyes(312) associated with dark spots in 5 eyes (312) andassociated with abnormal choroidal vessels in 3 eyes (187)An abnormal choroidal vessel characterized by an abnormaldilation of choroidal vessels was observed in one eye (67)In group B the analysis of the automatically segmented outerretina revealed an abnormal flow in 5 eyes (294) and

Table 2 Automatic segmented choriocapillaris OCTA features inCSC patients

Dark area 119899 19SRD 119899 17Irregular flat 119899 7Hyperreflective deposit 119899 4OS elongation 11

Dark spot 119899 7PED (irregular flat) 119899 5Hyperreflective deposit 119899 2Pigment migration 119899 2

Abnormal vessels 119899 12Dilation 119899 1Indistinct tangled 119899 5Tangled ldquoball of woolrdquo 119899 5Pruned tree 119899 1

No abnormalities 119899 3119899 numbers of eyes dark area 19 dark spot 7 abnormal choroidal vessel 12and no abnormalities 3SRD serous retinal detachment PED pigment epithelial detachment OSphotoreceptor outer segments

was normal in the remaining cases (706) The manuallysegmented outer retina showed a hyperdense signal in 8 eyes(47) and was normal in the remaining cases (53) In thisgroup two patients were excluded from the analysis of thechoriocapillaris layer because of an incorrect segmented slabautomatically generated by the software In the remaining15 eyes the choriocapillaris layer appeared normal in 1 case(67) but showed a dark area in 4 eyes (267) dark spotsin 2 eyes (133) abnormal choroidal vessels in 6 eyes (40)and abnormal choroidal vessels with a dark area in 2 cases(133) Comparison of the two groups showed that thepresence of dark areas was significantly greater in group A(119901 = 0029) there was no significant difference betweengroups regarding dark spots or abnormal choroidal vessels

33 Description and Classification of Abnormal ChoroidalVessels Twelve eyes out of 33 showed an abnormal choroidalvessel pattern at the choriocapillaris (Table 3) In a recentstudy we described patterns of CNV inside fibrotic scarsas ldquopruned treerdquo defined as an irregular filamentous flowinside the neovascular network and ldquotangled patternrdquo as anabnormal high-flow frequently interlacing vascular network[23] One eye showed a pruned tree pattern One eye showedan abnormal diffuse dilation of choroidal vessels withoutdistinct pattern The most common finding was a tangledpattern observed in 1012 eyes Tangled pattern could bedivided in two kinds of lesions a ldquoball of wool-likerdquo patternor an indistinct tangled pattern Atypical ldquoball of wool-likerdquotangled pattern was observed in 510 eyes All these 5 eyesharboring a ldquoball of wool-likerdquo pattern had typical CNV onmultimodal imaging (Figure 4) In the other 510 eyes anindistinct tangled pattern with high-flow abnormal choroidalvessels was observed Multimodal imaging of these 5 eyeswith indistinct tangled pattern confirmed the presence of


(a)

(b)

(c) (d) (e)

AngioFlow

Figure 1 Acute central serous chorioretinopathy in a 48-year-old man Correlation between optical coherence tomography (OCT) OCTangiography (OCTA) fluorescein angiography (FA) and indocyanine green angiography (ICGA) (a) OCT B-scan the yellow vertical linesindicate the limits of the serous retinal detachment (SRD) (b) Detail of the OCT B-scan the dashed yellow line shows the transition betweenthe non-SRD and the SRD area the yellow arrow indicates the area of flow reduction (c) Late phase of FA hyperfluorescent leaking point(d) Early phase of ICGA abnormal dilation of choroidal vessels (e) OCTA at the choriocapillaris the dashed yellow circle delineates an areaof apparent blood flow reduction called dark area in this study

CNV in 25 eyes In the remaining 35 eyes with indistincttangled pattern multimodal imaging and follow-up of thepatient did not show evidence of CNV (Figure 5)

4 Discussion

This study described a series of consecutive patients withCSC whatever the stage of the disease analyzed by OCTAand aimed to compare the images obtained with thoseobtained with other imaging modalities Main findings werethe presence of dark areas which were frequently associatedwith SRD presence of dark spots which were frequently

associated with PED and presence of abnormal vessels at thechoriocapillaris whichwere frequently but not systematicallyassociated with CNV based on multimodal imaging

Three studies one case report and 2 case series havepreviously reported OCTA findings in CSC patients Allstudies have focused on the diagnosis of associated CNVThey demonstrated that OCTAwas able to detect the distinctneovascular network typical of CNV in 58 of eyes withchronic CSC [20] Another study has shown the very highsensitivity and specificity (100) of OCTA for the diagnosisof associated CNV [21] The case report has shown a focalchoriocapillaris defect related to the RPE focal loss [22]


(a) (b)

(c)

(d) (e)

AngioFlow

Figure 2 Chronic central serous chorioretinopathy in a 68-year-old woman Correlation between fluorescein angiography (FA) indocyaninegreen angiography (ICGA) optical coherence tomography (OCT) and OCT angiography (OCTA) (a) Late phase of FA showing a typicalleaking point the yellow dashed line corresponds to the OCT scan shown in (c) (b) ICGA showing an abnormal dilation of choroidal vessels(c) OCT B-scan showing a serous retinal detachment (SRD) (d) OCT B-scan showing the segmentation at the choriocapillaris shown in (e)(e) OCTA showing a dark area that corresponds to the SRD

In our series 8 CSC complicated by CNV were includedOur findings confirmed that in 100 of cases OCTA wasable to show an abnormal choroidal vessel pattern at thechoriocapillaris as well as detect an abnormal flow in themanual outer retina segmentation However interestinglythis study also revealed 3 cases of false positive that is whichhad an abnormal choroidal vessel pattern at the choriocap-illaris but no typical features of neovascular membrane on

multimodal imaging Thus this study suggests that inter-preting abnormal choroidal vessels at the choriocapillarisshould be made with caution in CSC patients and shouldnot systematically be considered as CNV In other words ourstudy compared OCTA and multimodal imaging findingsincluding FA ICGA and SD-OCT Due to our experiencein the field of CSC we could ascertain the absence of CNVin some cases based on multimodal imaging However we


(a) (b) (c)

(d) (e)

(f)

(g) (h)

AngioFlow

Figure 3 Recurrent central serous chorioretinopathy in a 61-year-old man Multimodal imaging versus OCT angiography (OCTA)Multimodal imaging showing the correlation between color photography (a) fluorescein angiography (FA (b)) indocyanine greenangiography (ICGA (c)) optical coherence tomography (OCT (d)) fundus autofluorescence (FAF (e)) and OCT angiography (OCTA (h))with segmentation at the level shown on coregistered OCT B-scans ((f) and (g))The color fundus photography showed pigmentary changesthe yellow arrow indicates a hyperpigmentation dot Uneven leakage of dye ((b) and (c)) OCT B-scan showed a serous retinal detachment(SRD) Hyperautofluorescence with hyperautofluorescent parafoveal dots (arrow) Coregistered OCT B-scan showing the segmentationshown in (h) the yellow vertical lines indicate the limits of the SRD Coregistered OCT B-scan at the level of the yellow arrow shown in(h) the yellow arrow indicates the small area of retinal pigment epithelium detachment OCTA showed a moderately dark area delineated bya yellow dashed circle

could assume that the irregular choroidal pattern revealeda pathological choroidal vasculature that could correspondeither to abnormally dilated choroidal vessels or to CNV

This study disclosed two previously unreported findingsin CSC patients dark areas and dark spots at the chorio-capillaris The choriocapillaris has a fine densely packedhoneycomb-like microvasculature at the central fovea and

this aspect changes when moving toward the optic nerveor the periphery [24] In our series a rarefaction area wasobserved at the choriocapillaris and the term ldquodark areardquowas used to describe it These findings could however bean artifact due to a process of light attenuation or alteredsignal returned by the SRD flat irregular PED or outersegment photoreceptor elongation or a combination of all


Table 3 Comparison between abnormal choroidal vessel at the choriocapillaris level and multimodal imaging evidence of choroidalneovascularization (CNV)

Eye Abnormal choroidal vessel pattern Multimodal imaging features1 Typical tangled ldquoball of woolrdquo CNV2 Typical tangled ldquoball of woolrdquo CNV3 Indistinct tangled pattern CNV4 Typical tangled ldquoball of woolrdquo CNV5 Indistinct tangled pattern No CNV6 Indistinct tangled pattern No CNV7 Typical tangled ldquoball of woolrdquo CNV8 Pruned tree pattern CNV9 Indistinct tangled pattern CNV10 Indistinct tangled pattern No CNV11 Abnormal dilation No CNV12 Typical tangled ldquoball of woolrdquo CNV

(e998400) (f998400) (g998400)

(a) (b) (c) (d)

(e) (f) (g)

AngioFlowAngioFlowAngioFlow

Figure 4 Central serous chorioretinopathy (CSC) complicated by choroidal neovascularization (CNV) in a 59-year-old womanMultimodalimaging showing the correlation between fundus autofluorescence (FAF (a)) fluorescein angiography (FA (b)) indocyanine greenangiography (ICGA (c) and (d)) andOCT angiography (OCTA (e) (f) (g)) with coregisteredOCTB-scans showing the level of segmentation(e1015840 f1015840 g1015840) Chronic CSC with pigmentary changes and areas of hyperautofluorescence uneven leakage of fluorescein and dilated choroidalvessels ((a) to (c)) and presence of a choroidal neovascular membrane in the late phase of ICGA (d) Automatically segmented outer retinaOCTA showing a verymoderate hyperdense signal (e)Manually segmented outer retinaOCTA detecting a hyperdense signal correspondingto a discrete blood flow (f) Automatically segmented choriocapillaris OCTA showing a hyperdense signal that highlights a tangled lesionwith a typical neovascular network


Thic

knes

s(120583

m)

Position (mm)

1000

800

600

400

200

0

00

05

10

15

20

25

30

35

40

45

50

55

Follow-upReference

Follow-up thinnerFollow-up thicker

(a) (b) (c)

(d)

AngioFlow AngioFlow AngioFlow

(e) (f)

(g) (h) (i)

(d998400) (e998400) (f998400)

Figure 5 Central serous chorioretinopathy in a 52-year-old man with abnormal choroidal vessels on OCTA but no evidence of CNV onmultimodal imaging Late phase of fluorescein angiography (FA (a)) early and late phase of indocyanine green angiography (ICGA (b) and(c)) OCTA (d e f) and coregistered OCT B-scan (d1015840 e1015840 f1015840) Late phase of ICG revealed faint hyperfluorescent points which are usualfeatures of CSR [13] but no clear evidence of neovascular choroidal membrane Automatically segmented outer retina OCTA image didnot show any evidence of hyperdense abnormal signal (d) Manually segmented outer retina OCTA image showing a moderate abnormalhyperdense signal (e) Automatically segmented choriocapillaris OCTA image showing an abnormal choroidal vessel (arrow) with a tangledpattern lesion OCT revealed mild flat irregular PED and SRD (d1015840 e1015840 f1015840 g)This patient was not treated After one-month follow-up the SRDspontaneously decreased (38 microns) arguing in favor of absence of neovascular lesion (h i)


these features But dark areas could also correspond to a flowvoid due to a focal atrophy of the choriocapillaris secondaryto compression by the enlarged vessels from the outer cho-roid as previously suggested in CSC [25] InterestinglyOCTA also showed areas without detectable flow that werecalled dark spots in our study Focal flow reductions in thechoriocapillaris layer could be one of the causes of darkareas

In conclusion OCTA appears to be a promising tech-nique because it avoids the burden of intravenous injectionsof dye that may sometimes be complicated by serious sideeffects However interpreting images needs a learning curveof knowledge This report aimed to describe OCTA findingsobserved in CSC and to correlate them with other imagingmodality findings It showed dark areas and dark spots ascommon findings observed at the choriocapillaris in eyeswith CSC It also revealed the presence of abnormal dilatedchoroidal vessels at the same level that were frequently but notsystematically associated with CNV raising the question ofOCTA imaging interpretation and specificity Further studiesare needed to confirm these preliminary results and assessthe usefulness of this noninvasive tool in the diagnosis andmanagement of CSC

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

References

[1] D Bujarborua P N Nagpal and M Deka ldquoSmokestack leak incentral serous chorioretinopathyrdquo Graefersquos Archive for Clinicaland Experimental Ophthalmology vol 248 no 3 pp 339ndash3512010

[2] A E Maumenee ldquoMacular diseases clinical manifestationsrdquoTransactions of the American Academy of Ophthalmology andOtolaryngology vol 69 pp 605ndash613 1965

[3] J D Gass ldquoPathogenesis of disciform detachment of theneuroepitheliumrdquo American Journal of Ophthalmology vol 63no 3 supplement pp 1ndash139 1967

[4] R F Spaide L Campeas A Haas et al ldquoCentral serouschorioretinopathy in younger and older adultsrdquoOphthalmologyvol 103 no 12 pp 2070ndash2080 1996

[5] L A Yannuzzi ldquoType-A behavior and central serous chori-oretinopathyrdquo Retina vol 7 no 2 pp 111ndash131 1987

[6] S P Garg T Dada D Talwar and N R Biswas ldquoEndogenouscortisol profile in patients with central serous chorioretinopa-thyrdquo British Journal of Ophthalmology vol 81 no 11 pp 962ndash964 1997

[7] B Nicholson J Noble F Forooghian and C Meyerle ldquoCen-tral serous chorioretinopathy update on pathophysiology andtreatmentrdquo Survey of Ophthalmology vol 58 no 2 pp 103ndash1262013

[8] M-H Errera R P Kohly and L da Cruz ldquoPregnancy-associated retinal diseases and their managementrdquo Survey ofOphthalmology vol 58 no 2 pp 127ndash142 2013

[9] Y Eom J Oh S-W Kim and K Huh ldquoSystemic factorsassociated with central serous chorioretinopathy in KoreansrdquoKorean Journal of Ophthalmology vol 26 no 4 pp 260ndash2642012

[10] A A Fawzi G N Holland A E Kreiger J R HeckenlivelyJ G Arroyo and E T Cunningham Jr ldquoCentral serous chori-oretinopathy after solid organ transplantationrdquoOphthalmologyvol 113 no 5 pp 805ndash813e5 2006

[11] AM B Casella R F Berbel G L BressanimM RMalaguidoand J A Cardillo ldquoHelicobacter pylori as a potential target forthe treatment of central serous chorioretinopathyrdquo Clinics vol67 no 9 pp 1047ndash1052 2012

[12] A Daruich A Matet A Dirani et al ldquoCentral serouschorioretinopathy recent findings and new physiopathologyhypothesisrdquo Progress in Retinal and Eye Research vol 48 pp82ndash118 2015

[13] M Uyama H Matsunaga T Matsubara I Fukushima KTakahashi and T Nishimura ldquoIndocyanine green angiographyand pathophysiology of multifocal posterior pigment epithe-liopathyrdquo Retina vol 19 no 1 pp 12ndash21 1999

[14] Y Imamura T Fujiwara R Margolis and R F SpaideldquoEnhanced depth imaging optical coherence tomography of thechoroid in central serous chorioretinopathyrdquo Retina vol 29 no10 pp 1469ndash1473 2009

[15] D Ferrara K J Mohler N Waheed et al ldquoEn face enhanced-depth swept-source optical coherence tomography features ofchronic central serous chorioretinopathyrdquo Ophthalmology vol121 no 3 pp 719ndash726 2014

[16] A T Fung L A Yannuzzi and K Bailey Freund ldquoType 1(Sub-retinal pigment epithelial) neovascularization in centralserous chorioretinopathy masquerading as neovascular age-related macular degenerationrdquo Retina vol 32 no 9 pp 1829ndash1837 2012

[17] T Toyama K Ohtomo Y Noda and T Ueta ldquoPolypoidalchoroidal vasculopathy and history of central serous chori-oretinopathyrdquo Eye vol 28 no 8 pp 992ndash997 2014

[18] R F Spaide J M Klancnik andM J Cooney ldquoRetinal vascularlayers imaged by fluorescein angiography and optical coherencetomography angiographyrdquo The JAMA Ophthalmology vol 133no 1 pp 45ndash50 2015

[19] Y Jia S T Bailey D JWilson et al ldquoQuantitative optical coher-ence tomography angiography of choroidal neovascularizationin age-related macular degenerationrdquo Ophthalmology vol 121no 7 pp 1435ndash1444 2014

[20] M Quaranta-El Maftouhi A El Maftouhi and C M EandildquoChronic central serous chorioretinopathy imaged by opticalcoherence tomographic angiographyrdquoAmerican Journal ofOph-thalmology vol 160 no 3 pp 581e1ndash587e1 2015

[21] M A Bonini Filho T E de Carlo D Ferrara et al ldquoAssocia-tion of choroidal neovascularization and central serous chori-oretinopathy with optical coherence tomography angiographyrdquoJAMA Ophthalmology vol 133 no 8 pp 899ndash906 2015

[22] S M McClintic Y Jia D Huang and S T Bailey ldquoOpticalcoherence tomographic angiography of choroidal neovascular-ization associatedwith central serous chorioretinopathyrdquo JAMAOphthalmology vol 133 no 10 pp 1212ndash1214 2015

[23] A Miere O Semoun S Y Cohen et al ldquoOptical coherencetomography angiography features of subretinal fibrosis in age-related macular degenerationrdquo Retina vol 35 no 11 pp 2275ndash2284 2015


[24] W Choi K J Mohler B Potsaid et al ldquoChoriocapillaris andchoroidal microvasculature imaging with ultrahigh speed OCTangiographyrdquo PLoS ONE vol 8 no 12 Article ID e81499 2013

[25] L Yang J B Jonas and W Wei ldquoOptical coherence tomog-raphy-assisted enhanced depth imaging of central serous chori-oretinopathyrdquo Investigative Ophthalmology amp Visual Sciencevol 54 no 7 pp 4659ndash4665 2013

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Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


on both FA and OCT CSC may also be associated withpolypoidal choroidal vasculopathy (PCV) and both entitiesmay be overlapped [12 17]

Optical coherence tomography angiography (OCTA) is anew noninvasive nondye depth-resolved technique whichmay be used to investigate patients with CSC The conceptof OCTA is the detection of changes in blood flow in thevessels in a static eye without need for dye injection [18]The amplitude of the signal returning from nonstatic featuresvaries rapidly over time When calculating the decorrelationof signal amplitude from repeated consecutive B-scans at thesame cross section a contrast between static and nonstatictissues is created and generates a vascular decorrelationsignal that enables visualizing 3-dimensional retinal andchoroidal vasculature [19] OCTA images may be studiedby isolated segmentation in different vascular layers thusallowing analyzing the vascular structure in detail with nodarkening due to a staining or leakage [18ndash21]The aim of thisstudy was to analyze OCTA findings in eyes with CSC and tocompare themwith those obtainedwithmultimodal imaging

2 Methods

21 Study Population A series of consecutive patients diag-nosed with CSC at the University Eye Clinic of Creteil wasexamined All patients with CSC were included that ispatients with a clinical history of CSC and 6 months of visualimpairment patients previously treated or treatment-naiveand newly diagnosed treatment-naive CSC patients Patientswith any associated previous or concomitant ophthalmo-logical conditions that could confound the interpretationof clinical and imaging findings for the diagnosis of CSC(ie subretinal fibrosis age-related macular degenerationmacular or retinal vascular disease vitreoretinal diseaseor retinal surgery and hereditary retinal dystrophy) wereexcluded from the study This prospective clinical studywas conducted in accordance with the French bioethicallegislation and with the Declaration of Helsinki for researchinvolving human subjects It received the favorable opinionof the ethics committee of the France Macula Federation

22 Study Protocol Patients underwent a complete oph-thalmic examination including best-corrected visual acu-ity (BCVA) measurement with Early Treatment DiabeticRetinopathy Study (ETDRS) chart slit-lamp examinationdilated-fundus biomicroscopy and standardized imagingprotocol using Spectralis HRA + OCT (Heidelberg Engi-neering Heidelberg Germany) which included FAF FAand ICGA SD-OCT andor EDI-OCT All patients alsounderwent OCTA using a commercially available RTVueXR Avanti with AngioVue (Optovue Fremont CA USA)An incorporated software algorithm called Split-SpectrumAmplitude Decorrelation Angiography (SSADA) generates3-dimensional en face angiograms through decorrelationof two merged consecutive orthogonal registration volumesautomatically centered at the macula or manually centeredat the lesion Each acquired OCTA volume (3 times 3mm)consisted of 304 times 304 A-scan in 26 seconds The A-scan

rate is 70000 scans per second Each orthogonal volumeregistration is corrected to minimize motion artifacts Bothorthogonal volume scans are combined with a motion cor-rection technology (MCT) to create a 3-dimensional imageof retinal and choroidal blood flow A coregistered OCT B-scan allows the visualization of the retinal structure RTVueXR Avanti has an automated segmentation at the superficialretinal capillary plexus deep retinal capillary plexus outerretina and choriocapillaris [19ndash22] The OCTA software wasused to manually adjust the automated segmentation andits relative depth in the retina and choroid OCTA imageswere analyzed at three main depth intervals automaticallysegmented outer retina manually adjusted segmentationbetween the RPE and 30 120583m beneath it called manuallysegmented outer retina in order to detect a blood flowin the RPE-Bruch membrane-choriocapillaris complex andautomatically segmented choriocapillaris

Three trained OCTA users (Eliana Costanzo AlexandraMiere and Alarsquoa El Ameen) acquired the images and per-formed a qualitative analysis to determine CSC features Toassess the microvascular architecture three retina specialists(Salomon Yves Cohen Giuseppe Querques and Eric HSouied) analyzed a 3times 3 scanning area at the three depths pre-viously described Patients with poor quality OCTA images(ie due to eye movement) were not included in the analysisMoreover eyes previously treated were analyzed separatelyfrom treatment-naive eyes

Our analysis included descriptive statistics (using Mic-rosoft Office Excel software version 140 2010 RedmondUSA) for demographics and main clinical data as well asqualitative descriptions of the imaging findings

3 Results

Thirty-three eyes of 32 consecutive patients (21 males 11females mean age 548 plusmn 104 years) diagnosed with CSCwere enrolled in this study Mean BCVA was 023 plusmn 025logMAR (range 0ndash08 logMAR corresponding to 2020 to20125) Nine eyes (273) had newly diagnosed treatment-naive CSC while 24 eyes (727) had a history of at least6 months of visual symptoms in the affected eye In 8 eyes(242) CSC was associated with type 1 CNV Table 1 showspatient demographics and clinical characteristics

For clarity the whole population was analyzed firstwith description of images obtained at different levels In asecond time naive eyes were compared to previously treatedeyes In a third time eyes with abnormal choroidal vesselpatterns were described with more details with an attemptof classification according to the pattern

31 Systematic Analysis of Different Depth OCTA Images inthe Whole Population

311 Outer Retina Automatically segmented outer retinaOCTA images detected the presence of an abnormal flowin 6 eyes (182) and no remarkable findings in 27 eyes(818) The manually segmented area revealed the presenceof an abnormal flow in 9 eyes (273) while 24 eyes (727)presented no particular abnormality

















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