Eye (2015), 1–6

© 2015 Macmillan Publishers Limited All rights reserved 0950-222X/15

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Spectral domain ocular I Dooley, H Laviers, E Papavasileiou, C Mckechnie

CLINICAL STUDY
and H Zambarakji
coherence tomography
findings pre- and post
vitrectomy with
fibrovascular membrane
delamination for
proliferative diabetic
retinopathy

Abstract
Purpose To describe the intraretinal are useful prognostic indicators in fibrovascular
microstructure using serial spectral domain delamination surgery for patients with PDR.
optical coherence tomography (SD-OCT) Eye advance online publication, 25 September 2015;
preceding and following pars plana doi:10.1038/eye.2015.178
vitrectomy and delamination of fibrovascular
membranes in patients with proliferative
Introduction
diabetic retinopathy (PDR).
Methods This retrospective, interventional Optical coherence tomography (OCT) is a well-
case series includes 28 eyes. Outcome described method of viewing and measuring
measures included LogMAR distance best- various aspects of the retinal architecture in vivo.
corrected visual acuity (BCVA), SD-OCT The amount of detail and information that can
integrity of photoreceptor inner and outer be obtained from such images has already been
segments junction (IS/OS), and integrity of documented extensively.1 In particular, spectral
external limiting membrane (ELM). domain OCT (SD-OCT) delineates four highly
Results Pre-operative central macular reflective bands in the outer retina. These are
thickness (CMT) was significantly correlated from innermost to outermost: the external
with the final post-operative LogMAR BCVA limiting membrane (ELM), the photoreceptor Barts Health; Whipps Cross
(Pearson’s coefficient r = 0.89; P = 0.001). The inner and outer-segment (IS/OS) junction, the University Hospital, London,
eyes were categorised into three groups based outer-segment tips also referred to as Verhoeff’s UK
on post-operative IS/OS integrity (group 0: membrane and the retinal pigment epithelium
IS/OS intact; group 1: IS/OS irregular but not (RPE)/Bruch’s/choriocapillaris bands. Spaide Correspondence:
completely disrupted; group 2: IS/OS and Curcio2 have reviewed the current evidence H Zambarakji, Barts Health;
Whipps Cross University
completely disrupted). Mean BCVA improved and report that the anatomical attributions to the Hospital NHS Trust, London
significantly in group 0 (n = 9) from 1.13 ± 0.75 middle two hyper-reflective bands remain in E11 1NR, UK
preoperatively to 0.34 ± 0.21 (Student’s t-test: question. The innermost two bands, the ELM Tel: +44 208 539 5522
P = 0.06), in group 1 (n = 10) the BCVA and the IS/OS junction, are considered to ext. 5235;
Fax: +44 208 535 6466.
improved from 0.88 ± 0.56 to 0.58 ± 0.31 represent important hallmarks of photoreceptor
E-mail: hadi.zambarakji@
(Student’s t-test: P = 0.053) and in group 2 integrity and disruptions of these bands bartshealth.nhs.uk
(n = 9) the BCVA improved from 1.64 ± 0.53 to correlate with poor visual acuity in diabetic
1.53 ± 0.75 (Student’s t-test: P = 0.652). macular oedema (DMO), resolved central serous Received: 23 November
IS/OS integrity and ELM integrity at chorioretinopathy, branch retinal vein occlusion 2014
3 months post operatively, were significantly and post-retinal detachment repair.3–8 Accepted in revised form:
and positively correlated with final BCVA The concept of hierarchy of vulnerability among 9 July 2015
(Pearson’s coefficient: r = 0.83, Po0.001 and the ELM, IS/OS and cone outer-segment tips lines
Presentation: The paper was
r = 0.72, Po0.001, respectively). has been postulated.9 Thus diseases such as age- presented at the EVER
Conclusions Pre-operative CMT and post- related macular degeneration are more likely to meeting in Nice,
operative disruption of the IS/OS and ELM affect cone outer-segment tips, as well as the IS/OS October 2014
 Assessment of SD-OCT imaging in cases of vitrectomy and membrane delamination
I Dooley et al
2

junction and in advanced cases the ELM, in contrast to patients with significant cataracts or other media opacities
idiopathic epiretinal membrane (ERM) where traction results reducing the ability to image the retina were excluded.
in disruption further towards the inner retina, leaving the All eyes underwent logMAR distance visual acuity
ELM intact and the IS/OS largely unaffected except in testing using Thompson’s visual acuity chart (Thompson
advanced cases.9,10 Thus, despite the fact that diabetic software solutions, Herts, UK). SD-OCT imaging was
retinopathy (DR) is considered to be an inner retinal disease obtained at each clinic visit by an OCT-trained technician.
because of retinal non-perfusion, structural change in the SD-OCT scans were performed for each eye using the
outer retina is observed as epiretinal fibrosis and traction Cirrus OCT instrument (Carl Zeiss Meditec, Dublin, CA,
develop. Although the strength and adhesion of the epiretinal USA). Visual acuity measurements were recorded at the
membranes is not measurable, surgical experience shows that time of corresponding OCT scans.
the strength of the adhesions in proliferative diabetic Three vitreoretinal-trained masked observers (HZ, ID
retinopathy (PDR) membranes is greater than that observed and LP) agreed on a grading system before the start of the
in ERM and also that, subretinal fluid (SRF) may be an study, which was applied for the analysis of all scans. SD-
important prognostic factor in traction retinal detachment OCT scans were graded independently. Central macular
(TRD) secondary to PDR.11–13 Interestingly, reduced thickness (CMT) was measured using the automated
photoreceptor outer-segment thickness also correlates with central 1 mm subfield thickness of the macular cube
poor visual function in DMO, indicating that outer retinal 512/128 function in which a 6 × 6 mm area is scanned
structural changes in the absence of traction may be observed with 128 horizontal lines each consisting of 512 scans per
in diabetic eyes.14 In one recent study, the integrity of the IS/ line. If the automatic plane recognition software failed to
OS and ELM bands were shown to correlate well with visual appropriately identifying the ILM and RPE, then the in-
acuity following pars plana vitrectomy (PPV) for PDR.15 built calliper was utilised. The high definition 5-line raster
The study included a significant number of eyes with scans were used for the purpose of identifying the
non-clearing vitreous haemorrhage and pre-macular presence of ERM, cystoid macular oedema (CMO),
haemorrhage that may have contributed to worse mean vitreomacular traction (VMT) and integrity of the IS/OS
visual acuity levels preoperatively and significantly and ELM hyper-reflective bands. CMO, ERM and VMT
improved mean levels of vision at last follow-up.15 were graded as present (grade 1) or absent (grade 0). The
There is limited pre-operative SD-OCT data in PDR and photoreceptor layer was imaged as a hyper-reflective line
post-operative SD-OCT data following PPV for showing the IS/OS junction above the retinal pigment
complications of PDR. In the present study, we limited epithelium and the next hyper-reflective line on the inner
our entry criteria to eyes with severe pre-retinal fibrosis, aspect of the IS/OS line being the ELM line.2 The integrity
as well as TRD involving or threatening the macula. We of the IS/OS and ELM were graded as follows: grade 0
described serial SD-OCT scans preceeding and following was given when an intact hyper-reflective line was found,
PPV with pre-retinal membrane delamination and report grade 1 was assigned for any focal disruption of the
on the value of imaging the ELM and IS/OS junction respective line, and grade 2 was assigned for total
in relation to visual recovery. We postulated that the disruption of the respective line. The scores and OCT
integrity of the IS/OS and ELM post-operatively would assessments for each grader were recorded
correlate with visual outcomes. independently. OCT scans of poor quality were excluded
from the analysis. Where a patient had bilateral
delamination surgery, one eye was randomly chosen to
Materials and methods
remain in the study and the other eye was excluded.
This is a retrospective, consecutive interventional non- All procedures were performed by two surgeons (HZ
comparative case series for patients who underwent PPV and CM) using the Bausch and Lomb Stellaris Vision
and delamination of fibrovascular membranes secondary Enhancement System (Bausch and Lomb, Rochester, NY,
to PDR between 1st August 2012 and 31st March 2014. All USA). No triamcinolone or per-operative dyes were used
cases were identified through a search of the surgical as part of vitrectomy surgery. Membrane removal was
records database at Whipps Cross University Hospital performed using curved and/or vertical vitreoretinal
NHS Trust (Medisoft Ophthalmology, Medisoft Limited, scissors as completely as possible. In no patient, ILM peel
Leeds, UK). We recorded patients demographics, history was attempted. Panretinal endolaser photocoagulation
and clinical examination findings, and reviewed details of was performed when this was considered clinically
the surgical records including per-operative and post- indicated in particular, if insufficient laser had been
operative complications. The study did not require IRB applied preoperatively or for the management of retinal
approval and complied with the tenets of the Declaration breaks. This study followed the Tenets of the Declaration
of Helsinki. Patients with concurrent macular diseases or of Helsinki. We certify that all applicable institutional and

Eye
 Assessment of SD-OCT imaging in cases of vitrectomy and membrane delamination
I Dooley et al
3

governmental regulations concerning the ethical use of traction rhegmatogenous retinal detachment, and 7% had
human subjects were followed during this research taught thickened posterior hyaloid.
In the 16 patients with pre-operative scans, the pre-
operative CMT was shown to be significantly correlated
Statistical analysis
with the final post-operative logMAR BCVA (Pearson’s
Interobserver agreement was obtained for grading of correlation r = 0.89; P = 0.001; Table 1 and Figure 1). Two
OCT scans using the kappa test. Pairs of means were other pre-operative factors that were moderately
compared using Student’s t-test and groups of means correlated with final logMAR BCVA, SRF, and pre-
were compared using ANOVA. Correlations were operative logMAR BCVA, had correlation coefficients of
examined using Pearson’s product-moment coefficient (r). 0.69 (P = 0.03) and 0.50 (P = 0.49), respectively (Table 1).
A P-value of o0.05 was taken as statistically significant. For all 28 eyes, the mean pre-operative logMAR
BCVA improved significantly from 1.24 (±0.64) to 0.81
(±0.77, P = 0.006) at last post-operative visit. Fifty-four
Results percent (n = 15) of patients experienced a final post-
Twenty-eight eyes of 28 patients were included in the operative improvement in BCVA equivalent to ≥ 3 lines on
study. Mean (± SD) duration of follow-up was 11.4 ( ±5.7) the ETDRS (Early Treatment of Diabetic Retinopathy Study)
months. Twelve eyes were excluded due to ungradable or chart, whereas 14% of patients (n = 4) experienced a
unobtainable OCT images, 4 eyes were excluded by deterioration of ≥ 3 ETDRS lines. Three of these four
random selection in patients with bilateral surgery. patients had pre-operative OCT scans and all (3/3) had
ELM and ISOS grades of 2, which was a significantly worse
Fifteen eyes (54%) had pre-operative OCT scans, 14 eyes
mean grade than the other 13 patients with pre-operative
had OCT scans at 1–3 months and 27 eyes had OCT scans
scans (unpaired Student’s t-test: P = 0.003 and P = 0.006,
43 months post operatively.
respectively). All four patients with loss of ≥ 3 ETDRS lines
OCT results are summarised in Table 1. Of the 28
had post-operative ELM and ISOS grades of 2.
patients 64% were male, the mean age was 54 (±13) years.
In Table 2 and Figure 2, the eyes were divided into three
The right eye was the study eye in 58% of cases. Age was
groups based on post-operative IS/OS integrity. Mean
not significantly correlated with final best-corrected
BCVA improved significantly in group 0 (n = 9) from
visual acuity (BCVA) (Pearson’s coefficient: r = 0.077,
1.13 ± 0.75 preoperatively to 0.34 ± 0.21 (P = 0.06; Figure 3),
P = 0.346). The overall inter-observer agreement for the in group 1 (n = 10) the BCVA improved from 0.88 ± 0.56 to
grading of IS/OS and ELM status was 89% (Kappa 0.58 ± 0.31 (P = 0.053) and in group 2 (n = 9) the BCVA
statistic: 0.709; Po0.01). At final visit 43% (n = 12) of improved from 1.64 ± 0.53 to 1.53 ± 0.75 (P = 0.652).
patients were pseudophakic and 56% (n = 15) were using Eyes were also categorised in three subgroups based on
anti-glaucoma medication in the study eye. Sixty-eight the integrity of the ELM. The mean BCVA improved
percent of eyes (n = 19) had gaseous intraocular significantly in group 0 (from 1.10 ± 0.71 to 0.36 ± 0.22;
tamponade, 18% of cases (n = 5) used silicone oil, and 7% P = 0.008; Figure 3b) and group 1 (from 1.03 ± 0.56 to
(n = 2) had silicone oil tamponade at last visit. In addition 0.54 ± 0.23; P = 0.016). Group 2 remained unchanged with
to PDR, 57% had TRD, 25% had non-clearing vitreous a mean pre-operative BCVA of 1.71 ± 0.51 and a mean
haemorrhage with pre-retinal fibrosis, 11% had combined post-operative BCVA of 1.70 ± 0.88 (P = 0.974).

Table 1 Correlation with final LogMAR BCVA

Preop mean Corr (r) P-value 3-Month mean Corr (r) P-value Final mean Corr (r) P-value
n = 16 n = 16 n = 27

CMT (SD) 694 (623) 0.89 0.001 391 (165) 0.17 0.528 300 (89) − 0.08 0.7
ELM (SD) 1.3 (0.8) 0.40 0.128 1.2 (0.8) 0.77 0.001 0.9 (0.8) 0.70 0.001
IS/OS (SD) 1.4 (0.8) 0.47 0.064 1.2 (0.7) 0.87 0.001 1.0 (0.8) 0.64 0.001
SRF 19% 0.69 0.003 19% 0.25 0.360 7% 0.22 0.270
CMO 88% 0.25 0.354 44% 0.08 0.766 44% 0.01 0.988
ERM 75% − 0.03 0.908 56% 0.53 0.033 52% − 0.16 0.449
BCVA (SD) 1.43 (0.81) 0.50 0.049 1.06 (0.9) 0.74 0.002 0.81 (0.77) NA NA
VMT 44% 0.05 0.848 0% NA NA 0% NA NA
Abbreviations: 3-Month mean, mean post-operative level at 3 months; corr, Pearson correlation coefficient (r); CMO, cystoid macular oedema; CMT, central
macular thickness; ELM, external limiting membrane integrity; ERM, epiretinal membrane; Final mean, mean post-operative level at final visit (11.3 months);
IS/OS: inner-segment outer-segment junction integrity; preop mean, mean pre-operative level; SRF, subretinal fluid; VMT, vitreomacular traction.
Final visit was at a mean of 11.3 months post operatively. ELM integrity and IS/OS integrity are graded on a 3 point qualitative scale, where 0 = continuous,
1 = irregular, but not completely disrupted, 2 = complete disruption of membrane.

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 Assessment of SD-OCT imaging in cases of vitrectomy and membrane delamination
I Dooley et al
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Discussion 3-month and final visits. The presence of ERM at

3 months was significantly correlated with a worse final
Conventional theory explains that poor visual outcomes
BCVA, but this association was lost at final visit.
following surgical treatment of PDR are the result of
Furthermore, post-operative CMT is not significantly
macular ischaemia or long standing TRD of the macula.
correlated with final BCVA, whereas it was strongly and
Our data support the importance of intraretinal structural
changes at the level of the ELM and IS/OS junction in significantly correlated when measured preoperatively.
eyes with severe PDR. As far as we know, this is the first Our results show that BCVA and SD-OCT parameters
study to examine pre-operative as well as post-operative assessed at 3 months post operatively were most strongly
SD-OCT images in the context of PPV for PDR. correlated with the final BCVA, indicating that good
The ELM and IS/OS junction findings at 3 months were surgical outcomes at 3 months were usually maintained at
the most strongly correlated findings with final logMAR last follow-up.
BCVA, better than the ELM and IS/OS junction findings We speculate that the photoreceptor injury was beyond
at final visit. We postulate that this effect of falling repair in eyes with disrupted IS/OS junction and/or ELM,
correlation may be due to other confounding issues such leading to poor visual outcomes. We believe that the
as cataract formation. It is noteworthy that ERM was IS/OS and the ELM integrity may act as a surrogate of
present post-operatively in the majority of patients at the photoreceptor integrity and function in the present setting.
The IS/OS group 0 (based on final OCT scans) showed
a significant final post-operative improvement in mean
BCVA, which was also the case for the ELM groups 0 and 1.
This finding supports the hypothesis that IS/OS and
ELM integrity have an important role in maintaining
macular function and that the disruption of these
structures is associated with poorer post-operative
outcomes. It would seem that minimal disruption of the
IS/OS and ELM are desirable for a favourable BCVA post
membrane delamination for PDR. A poor ELM and IS/OS
grade preoperatively confers a greater likelihood of a
poorer post-operative BCVA.
Shah et al examined post-operative outer-segment OCT
changes in PDR. They reported a correlation with post-
operative ELM, IS/OS integrity and final BCVA (52 and
55%, respectively), which is less than that of our study.
Figure 1 Scatter plot of pre-operative CMT (in microns; x axis) This difference may be attributed to differing patient
against final post-operative logMAR BCVA (y axis). The best-fit
baseline characteristics as 17 of 36 (47%) patients in Shah’s
line and Pearson correlation coefficient (r = 0.89) are depicted,
along with the 95% confidence belt (broken lines, shaded area). paper had tractional macular detachments and cases with
This strong correlation was positive and significant (P = 0.001). persistent ERM were excluded.15 All our patients had

Table 2 Eyes are grouped by IS/OS or ELM status into: group 0 (no disruption), group 1 (irregular but not broken), and group 2
(complete interruption)

Group 0 Group 1 Group 2 P P P

0 vs 1 0 vs 2 1 vs 2

IS/OS
Preop BCVA (n = 27) 1.13 ± 0.75 (9) 0.88 ± 0.56 (9) 1.64 ± 0.53 (9)
IS/OS group at 3 months and post op BCVA (n = 16) 0.2 ± 0.14 (2) 0.59 ± 0.22 (9) 2.18 ± 0.54 (5) 0.355 0.001 0.001
IS/OS group last visit and post op BCVA (n = 27) 0.34 ± 0.21 (9) 0.58 ± 0.31 (9) 1.52 ± 0.95 (9) 40.5 0.001 0.007

ELM
Preop BCVA (n = 27) 1.10 ± 0.71 (10) 0.91 ± 0.58 (9) 1.71 ± 0.51 (8)
ELM group at 3 months and post op BCVA (n = 16) 0.39 ± 0.34 (3) 0.52 ± 0.20 (7) 1.90 ± 0.71 (6) 40.5 0.001 0.001
ELM group last visit and post op BCVA (n = 27) 0.36 ± 0.21 (10) 0.52 ± 0.24 (9) 1.70 ±0.88 (8) 40.5 0.001 0.001
Abbreviations: BCVA, best-corrected visual acuity in LogMAR; ELM, external limiting membrane integrity; IS/OS, inner-segment outer-segment junction integrity.
Numbers of eyes (n) are shown in bracket where relevant. P refers to P-value for ANOVA, a Po0.05 was taken as statistically significant. 0 vs 1, group 0 compared
with group 1; 0 vs 2, group 0 compared with group 2; 1 vs 2, group 1 compared with group 2.

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 Assessment of SD-OCT imaging in cases of vitrectomy and membrane delamination
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Figure 2 (a) A high definition pre-operative macular OCT scan

and (b) the same patient 12 months following PPV and
delamination surgery. The patient was a 55-year old with type
2 diabetes managed with insulin. The pre-operative OCT (a)
displays a thickened taut posterior hyaloid, with cystoid macular
oedema, a focally disrupted IS/OS = 1 and ELM = 1. The BCVA
was 0.8 and the CMT was 450 microns. The post-operative scan
(b) 10-months post PPV and delamination surgery. The BCVA
improved to 0.54 and the CMT has reduced to 271 microns, the
ELM was complete (ELM = 0) and the IS/OS was focally
disrupted but not completely disrupted (IS/OS = 1). Figure 3 Box-whisker plot depicting the BCVA for patients
grouped by (a) IS/OS and (b) external limiting membrane
integrity (group 0: IS/OS or ELM intact; group 1: IS/OS or ELM
irregular but not completely disrupted; group 2: IS/OS or ELM
pre-retinal fibrosis with an element of traction requiring completely disrupted), before (pre-operative) and after (post-
membrane delamination, furthermore eyes with operative) delamination of fibrovascular membranes in prolif-
erative diabetic retinopathy.
post-operative ERM were not excluded. Baseline
demographics were also slightly different as 85% of our Pre-operative and post-operative CMO, defined in this
patients suffered from type 2 DM and 70% were on study as any cystoid spaces seen on the high definition
insulin, compared with 89% (31/36) on insulin in the SD-OCT images, does not correlate with final BCVA and
study reported by Shah et al.15 neither does pre-operative VMT correlate with final
In only 15 of the 28 eyes were pre-operative scans BCVA. Our findings would suggest that intraretinal
available for analysis. This is due to the presence of structural changes are the predominant predictive
concomitant VH and advanced macular detachment, parameter of post-operative visual function and that the
which prevented quality scanning in the remaining 13 relative contribution of other findings such as VMT and
patients. Despite this limitation we have found three CMO to have less relative contribution to final visual
pre-operative factors (pre-operative BCVA, pre-operative function. Eyes with PDR undergoing PPV for TRD have
CMT and presence of SRF preoperatively) that are usually suffered from significant intraretinal structural
significantly correlated with final BCVA. change and have reduced visual potential, unlike those

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 Assessment of SD-OCT imaging in cases of vitrectomy and membrane delamination
I Dooley et al
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with DMO where a reduction in macular thickness and 2 Spaide RF, Curcio CA. Anatomical correlates to the
oedema may be more likely to result in a significant bands seen in the outer retina by optical coherence
tomography: literature review and model. Retina 2011;
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Study limitations include its retrospective design, small 3 Otani T, Yamaguchi Y, Kishi S. Correlation between visual
numbers, lack of randomisation, and the absence of a acuity and foveal microstructural changes in diabetic
control group. Some of these limitations may be difficult macular edema. Retina 2010; 30: 774–780.
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Freeman WR. The association between percent disruption of
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Developments such as intraoperative OCT may yield 6 Murakami T, Tsujikawa A, Ohta M, Miyamoto K, Kita M,
further insight into the contribution of the IS/OS and Watanabe D et al. Photoreceptor status after resolved
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follow-up, this may have altered their BCVA, however we
7 Schocket LS, Witkin AJ, Fujimoto JG, Ko TH, Schuman JS,
felt their inclusion caused less bias than their exclusion. Rogers AH et al. Ultrahigh-resolution optical coherence
In summary, we report a significant correlation between tomography in patients with decreased visual acuity
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8 Sakamoto A, Nishijima K, Kita M, Oh H, Tsujikawa A,
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Yoshimura N. Association between foveal photoreceptor
prognostic factors following diabetic vitrectomy for status and visual acuity after resolution of diabetic macular
complications of PDR. Ocular findings at 3 months appear edema by pars plana vitrectomy. Graefes Arch Clin Exp
to remain relatively stable at final follow-up. High- Ophthalmol 2009; 247: 1325–1330.
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membrane and inner segment and outer-segment Flynn HW Jr. Composite spectral domain optical coherence
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12 Iwasaki T, Miura M, Matsushima C, Yamanari M, Makita S,
for proliferative diabetic retinopathy surgery if: the pre- Yasuno Y. Three-dimensional optical coherence tomography
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14 Forooghian F, Stetson PF, Meyer SA, Chew EY, Wong WT,
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Conflict of interest segment length and visual acuity in diabetic macular edema.
Retina 2010; 30: 63–70.
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retinal microstucture and foveal thickness with visual acuity
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