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Clinical science

Macular displacement following rhegmatogenous


retinal detachment repair
Edward Lee,1 Tom H Williamson,1 Pirro Hysi,2 Manoharan Shunmugam,1
Mahmut Dogramaci,1 Roger Wong,1 D Alistair H Laidlaw1

▸ Additional material is ABSTRACT (FAF) imaging. Hyper-autofluorescent lines were


published online only. To view Aims To investigate the incidence of macula detected running parallel to selected retinal blood
please visit the journal online
(http://dx.doi.org/10.1136/ displacement and symptoms of distortion following vessels; it is hypothesised that the hyper-
bjophthalmol-2013-303637). rhegmatogenous retinal detachment (RRD) repair, autofluorescence is due to increased metabolic activity
1 quantify the displacement where seen and further of retinal pigment epithelium (RPE) that had previ-
Department of Ophthalmology,
St. Thomas’ Hospital, characterise the nature of the displacement. ously been located under major retinal blood vessels
London, UK Methods Consecutive patients undergoing primary and is postoperatively exposed to light. Comparison
2
Department of Twin Research RRD repair were assessed postoperatively with fundus of the retinal vasculature and the parallel hyper-
& Genetic Epidemiology, autofluorescence and optical coherence tomography autofluorescent ‘RPE vessel ghost’ lines thus gives a
St. Thomas’ Hospital,
London, UK imaging, and the extent of macula displacement indication of retinal displacement.
quantified using a novel means. Findings were examined The aims of this study were to determine the
Correspondence to for correlations with symptoms and pre-operative incidence of macula displacement and association
Edward Lee, Department of features. with symptoms of distortion following retinal
Ophthalmology, St. Thomas’
Results Macula displacement was evident detachment repair, to develop a means of quantify-
Hospital, Westminster Bridge
Road, London SE1 7EH, UK; postoperatively in 72% of 32 consecutive fovea-involving ing the displacement when seen, and to further
[email protected] detachments treated with vitrectomy and gas. It was also characterise the nature of the displacement.
evident in 5/17 foveal-sparing cases treated with
Received 28 April 2013 vitrectomy and gas and in two of two patients with METHODS
Revised 24 June 2013
Accepted 3 July 2013 fovea-involving detachments treated with vitrectomy and Over an 11-month period patients undergoing
Published Online First oil. There was a significant correlation between the RRD repair were routinely evaluated with FAF and
18 July 2013 presence of macula displacement and symptoms of optical coherence tomography (OCT) imaging and
distortion in the early postoperative period ( p=0.013). asked about symptoms of distortion of image size
Symptomatic patients described bending of lines with or or form on postoperative review. The findings of
without objects appearing smaller or narrower in the those undergoing primary surgery, with no history
operated eye. Quantifying the displacement of previous vitrectomy, RRD repair or macula
demonstrated that the extent of displacement was disease, were examined in this study. The study was
associated with distance from the optic disc ( p=0.005) approved by the local research and development
and the extent of retinal detachment. review board.
Conclusions Displacement of the macula is common FAF imaging was performed with the Topcon
following RRD repair and heterogeneous in nature. TRC-50IX fundus camera and Spaide autofluores-
Most affected patients are symptomatic in the early cence filters (Topcon, Tokyo, Japan) following
postoperative period. pupillary dilation.9 The excitation and emission
bandwidths of these filters are 500–610 and 675–
715 nm, respectively. In brief, 50° field images were
INTRODUCTION taken from both eyes centred on the fovea. Flash
Symptoms of distortion are prevalent among intensity, aperture and gain were adjusted to accom-
patients who have undergone anatomically success- modate differences in media clarity and pupil size.
ful retinal detachment repair, and may occur Cross-sectional macular images with a 6 mm width
despite good recovery of visual acuity.1–5 The were also acquired with spectral domain OCT
symptoms can be considered as distortion of image imaging (3D OCT-1000; Topcon) from both eyes
size (dysmetropsia) and/or form (metamorphopsia). and centred on the fovea at the same visit as the
In patients with good vision in the fellow eye, dys- FAF imaging was performed. At the same visit
metropsia and metamorphopsia in the operated eye patients were asked if they were aware of distortion
can impair fusion and compromise binocular single of straight lines when looking with just the oper-
vision.6 Unless one of the images is suppressed, the ated eye, or a difference in image size between the
patient is at risk of binocular diplopia, asthenopia two eyes. Visual acuities were tested using
or retinal rivalry, which may be poorly tolerated. In COMPlog, a validated, computerised and semi-
extreme cases, affected patients may choose to par- automated visual acuity measurement device, and
tially occlude the operated eye despite good post- measured in number of ETDRS letters.10
operative acuity. FAF images were further analysed using
It is likely that distortion following rhegmatogenous Photoshop CS4 (Adobe Systems, San José,
To cite: Lee E, retinal detachment (RRD) repair results from ectopic California, USA). ‘RPE vessel ghosts’ were defined
Williamson TH, Hysi P, et al. replacement of macula photoreceptors.7 Shiragami as hyper-autofluorescent lines running approxi-
Br J Ophthalmol et al8 described how displacement of the retina can be mately parallel to retinal blood vessels and with a
2013;97:1297–1302. detected post-operatively by fundus autofluorescence similar contour but separate from the blood vessel.

Lee E, et al. Br J Ophthalmol 2013;97:1297–1302. doi:10.1136/bjophthalmol-2013-303637 1297


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Clinical science

The presence of RPE vessel ghosts was taken as evidence of


retinal displacement only in the absence of confluent subretinal
fluid (SRF) on the corresponding OCT scan (to exclude potential
artefact from a parallax effect). Affected images were overlaid
with concentric measuring circles, centred on the midpoint
of the optic disc, with diameters of 1.0–10.0 disc diameters
(figure 1). RPE vessel ghosts were highlighted, and where these
crossed one of the concentric measuring circles, the distance
was measured from that intersection to the intersection of the
same measuring circle and the corresponding blood vessel.
Measurements were expressed as a percentage of disc diameter in
the same eye. For each sample point the distance from the
current vessel position to the centre of the optic disc (r) was mea-
sured, along with the angle of the interconnecting line. The x
and y co-ordinates of each sample point could then be calculated
using trigonometry (figure 1). Positive x and y co-ordinates cor-
responded to retina temporal and superior to the optic disc,
respectively. The number of sample points identified in each
image using this standardised approach was used as an indicator
of how widespread the displacement of blood vessels was in that
subject’s macula, and used to test for an association with the pres-
ence or absence of postoperative symptoms of distortion.
Patient characteristics and outcomes were obtained by a
review of the case notes and a prospectively completed elec-
tronic database used to record operation findings and proce-
dures at the time of surgery (VITREOR, Microsoft Access,
available with the book on vitreoretinal surgery published by
Springer).11 The operation note was used to determine whether
the detachment was fovea-involving or fovea-sparing at the time
of surgery. Operation drawings were analysed in Photoshop to
measure the maximal extent of the detachment, in the temporal
half of the retina, above and below the fovea (0–90°).
Fisher’s exact test was used to examine for associations
between the presence or absence of displacement on FAF
imaging and lens status at the time of imaging ( phakia or pseu- Figure 1 Example fundus autofluorescence (FAF) image following
dophakia) and recorded symptoms of distortion. A t test was vitrectomy and gas surgery for a rhegmatogenous fovea-involving retinal
used to test for differences in visual acuity between patients detachment. Postoperatively this patient complained of distorted vision
with and without displacement. The relationship between the in the operated eye with lines appearing ‘wiggly’. He also described
amplitude of post-operative retinal vessel displacement and pos- horizontal and vertical double vision, and on testing with the prism
ition within the macula was studied using a multi-level mixed cover test the operated eye rotated downwards to take up fixation. In
effects linear regression model which accommodates different the uppermost image, white hyper-autofluorescent lines can be seen
measurements taken from individual patients and adjusts for adjacent to retinal blood vessels. These retinal pigment epithelium (RPE)
vessel ghosts run approximately parallel to neighbouring retinal vessels
potential confounding variables. The Stata V.12.1 (College
and have a similar contour. The RPE vessel ghosts are highlighted in blue
Station, Texas, USA) xtmixed module was used for this. For out- in the lowermost image, and concentric circles with fixed disc diameters
comes that were not normally distributed we used a normal have been overlaid in red. These concentric circles were used to measure
logarithmic transformation prior to analysis. The level of prob- the extent of displacement in each FAF image. Where the concentric
ability taken as significant was p=0.05 or less. sampling circles overlay a ghost vessel, the linear distance between the
‘sampling circle-ghost vessel’ intersection and ‘sampling circle-retinal
RESULTS vessel’ intersection was measured as a fraction of optic disc diameter.
Demographics and clinical characteristics The x and y co-ordinates for the sample point were calculated using
of the patient sample trigonometry (measurement lines in yellow). It is evident from the RPE
There were 87 eligible patients during the study period of vessel ghosts in this example image that the macula has been shifted
predominantly downwards, but to a variable extent depending on
whom 27 were excluded from further analysis due to incom-
position within the macula. It is therefore likely that the downwards
plete follow-up data. Specifically, 10 patients were transferred movement of the cornea on taking up fixation with the prism cover test
back early to referring units, did not attend follow-up appoint- is due to rotation of the eye on a horizontal axis such that the inferiorly
ments or had investigations inadvertently missed, seven patients displaced fovea will be rotated upwards in order to take up fixation,
had media opacities preventing adequate postoperative imaging, while the cornea will be rotated downwards.
and 10 patients had intra-operative or early postoperative com-
plications such as retinal re-detachment. Of the 60 patients
whose follow-up data were further analysed, 49 were treated cryo-buckle non-drain procedures (of whom three had
with vitrectomy, retinopexy and gas tamponade (of whom 32/ fovea-involving detachments). FAF and OCT imaging, and
49 had fovea-involving detachments at the time of surgery), two symptom evaluation, were typically performed at the first post-
were treated with vitrectomy, retinopexy and oil tamponade operative visit following absorption of intraocular gas when
(both fovea-involving detachments), and nine were treated with used; the median interval between surgery and imaging in these

1298 Lee E, et al. Br J Ophthalmol 2013;97:1297–1302. doi:10.1136/bjophthalmol-2013-303637


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Clinical science

60 patients was 29 days. Subsequent follow-up images and func-


tional data were not included in this study. Postoperative find-
ings are further evaluated in relation to the type of operative
procedure performed and foveal status recorded at the time of
surgery.

Macula displacement
Following vitrectomy and gas, RPE vessel ghosts indicating dis-
placement were seen in 23 of 32 eyes with fovea-involving
detachments (72%). The detachment and surgical details for
these patients are shown in the online supplementary data table.
Analysis of the fovea-involving detachments treated with vitrec-
tomy and gas (n=32) found no association between the presence
or absence of distortion and lens status ( phakia or pseudophakia)
or post-operative visual acuity ( p=0.648 and p = 0.678, respect-
ively). However, the presence of postoperative symptoms of dis-
tortion did correlate with number of displaced blood vessel
sampling points identified in each autofluorescence image (an
indicator of how widespread the displacement of vessels was in
that subject’s macula) (r=0.565, p<0.001).
Of the 17 eyes with fovea-sparing retina detachments treated
with vitrectomy and gas, five had detached retina confined to
the superonasal quadrant only. None of these showed evidence
of macula displacement following surgery. The remaining 12
fovea-sparing detachments treated with vitrectomy and gas had
detached retina directly superior or superotemporal to the
macula. Five of these had postoperative shift evident within the
macular arcades and in three this was confined to the area of
detachment seen clinically, but in two cases there was a shift of
blood vessels directly above and below the fovea suggesting that
the previously uninvolved fovea had become involved. Both
these patients experienced symptoms of distortion postopera-
tively. In all cases with vitrectomy and gas where macular dis-
placement was present, the vertical component of movement
was in a superior to inferior direction with RPE vessel ghosts
lying superior to the postoperative position of the correspond- Figure 2 Examples of less common forms of displacement (RPE
ing retinal blood vessels (figure 1). vessel ghosts and corresponding displaced blood vessels are
Two fovea-involving detachments were treated with vitrec- highlighted with pairs of arrows). Fundus autofluorescence (FAF) image
tomy and 1300 cs silicone oil as a primary procedure. Both had A is from patient no. 30 in the supplementary data table. Within the
near total (>270°) retinal detachments. In one patient this was macula it is evident the retina has been displaced inferiorly. However,
secondary to a giant retinal tear and the other patient had mul- by looking at vessels above and below the disc, it is evident that there
tiple tears in the inferior, temporal and superior quadrants. has been temporal displacement as well. FAF image B is from a patient
with a temporal giant retinal tear and near total (>270°) detachment,
Neither patient was advised to adopt a specific posture post-
treated with vitrectomy and oil. Postoperatively the retina has been
operatively and both had evidence of macula displacement. In displaced superiorly.
the patient with a temporal giant retinal tear, the direction of
shift was upwards with RPE vessel ghosts lying inferior to the
corresponding retinal blood vessel (figure 2); in the other the
observed shift was downwards. Of the nine patients treated with macula, namely outer-retinal folds (n=2), cystoid macula
cryo-buckle procedures, none had RPE vessel ghosts evident on oedema (n=1) and epiretinal membrane (n=1). The two eyes
imaging. with outer-retinal folds both had superotemporal detachments
that were recorded as being fovea-sparing. Postoperatively, one
Ultrastructure had evidence of a single outer-retinal fold passing through the
OCT images were reviewed for evidence of disrupted retinal fovea; it is likely the fluid had either extended further pre- or
structure postoperatively. Of the 32 eyes treated with vitrectomy peri-operatively than had been detected clinically, or that the
and gas for fovea-off detachments, 47% (15/32) had an OCT extent of fluid had progressed further at the end of surgery or
abnormality at this early time point of imaging. The abnormal- postoperatively. The patient had 6/6 vision but was aware of a
ities detected were outer-retinal folds (n=6), multiple blebs of kink in horizontal lines when imaged 48 days following
SRF (n=3), a single bleb of SRF (n=1, with the bleb being sub- surgery. The FAF image had evidence of displaced retina super-
foveal), outer-retinal photoreceptor layer defects (n=3), an epir- ior and temporal to the fovea. The other eye with outer-retinal
etinal membrane (n=1), a full thickness macular fold (n=1) and folds had presented with an acute-on-chronic round-hole
a full thickness macular hole (n=1, this same eye also had outer- superotemporal RRD. The postoperative OCT showed multiple
retinal folds). diffusely distributed outer-retinal folds affecting the macula
Of the 17 eyes with fovea-on detachments treated with when imaged 17 days following surgery. At this time point,
vitrectomy and gas, four had OCT abnormalities within the vision was limited to 6/36.

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Clinical science

Metamorphopsia Quantitative analysis


Postoperative distortion was reported in 69% (22/32) of those Further analysis of the FAF images was performed for the
patients with foveal-off detachments treated with vitrectomy largest single group of patients, fovea-involving detachments
and gas. Of those with evidence of macular shift, symptoms treated with vitrectomy and gas. The single patient with a full-
were present in 83% (19/23), and conversely, in those with thickness macular fold was excluded from this analysis as the
symptoms there was evidence of shift in 86% (19/22), indicating gross distortion of normal anatomy prevented accurate quantifi-
a high level of concordance between FAF evidence of shift and cation of displacement. In the remaining 22 patients with
postoperative symptoms of distortion (Fisher’s exact p=0.0126; fovea-involving detachments treated with vitrectomy and gas
figure 3). Some 45% of patients who were aware of bending of and with postoperative retinal displacement evident, mixed
straight lines also responded positively when asked if there was model statistical analysis was used to test for associations
a difference in image size between the eyes; this was variably between the amplitude of displacement and each of x, y and r
described as objects appearing smaller or narrower in the oper- (distance of the sample point from the optic disc). A significant
ated eye as compared to the unoperated eye. No patients association was found with r ( p=0.005) but not x or y
reported images appearing larger in the operated eye. (p=0.156 and p=0.711, respectively). However, it was evident
Of the patients treated with vitrectomy and gas for that the displacement is typically heterogeneous within the
fovea-sparing detachments, two reported postoperative distor- macula, or along the course of individual blood vessels, as
tion. These patients accounted for two of the five with evidence demonstrated in the inferior vessel displayed in figure 1. These
of macula shift postoperatively. One had an acuity of 78 ETDRS findings indicate that rather than there having been a uniform
letters (UK Snellen equivalent 6/8) and a normal OCT but FAF shift of the retina, there has instead been variable distortion or
evidence of shift above and below the fovea suggestive of foveal stretch which is only partly determined by position within the
involvement. The other was described previously with OCT evi- macula.
dence of a single outer-retinal fold passing through the fovea, In the 22 patients with quantitative analysis, the extent of
symptoms of distortion and evidence of displaced blood vessels retinal detachment in the temporal retina was measured in
superior and temporal to the fovea. degrees of involvement above and below the fovea. In our
regression model, we found significant associations between the
magnitude of displacement and the above ( p=0.0003) and
below ( p=0.02) angles of detachment (table 1). The regression
model we applied takes into account the non-independence of
multiple observations from the retina of individual subjects, and
the results therefore suggest that when present, the displacement
was more marked in eyes with larger extents of detached retina
at the time of surgery.

DISCUSSION
This study demonstrates that displacement of the retina is both
common following vitrectomy surgery for retinal detachment
and has functional significance. Furthermore, we have devel-
oped a means of quantifying the displacement and further char-
acterised the changes seen. The ability to quantify displacement
permits comparisons between patients and between different
techniques and allows measurement of change during longitu-
dinal follow-up; it is therefore likely to facilitate further under-
standing of the aetiology and steps that can be taken to
minimise its occurrence.
The finding that the extent of retinal displacement within the
macula of individuals is heterogeneous is of functional and
prognostic significance. These results indicate that the retina has
not been purely rotated around the disc, or shifted downwards,
but instead there is a more complex movement with some
regions within the macula being displaced more than others
(heterogeneous shift). We propose this is because the retina has

Table 1 Analysis of association between extent of retinal


detachment and amplitude of displacement
95% CI
Coefficient SE p Value Lower Upper

Angle above fovea 0.0142 0.0039 0.0003 0.0066 0.0219


Figure 3 Concordance between fundus autofluorescence (FAF) Angle below fovea 0.0088 0.0038 0.0213 0.0013 0.0162
evidence of macula displacement (shift) and symptoms of distortion.
The regression coefficient is the logarithmic value of displacement (in disc diameters)
The 32 rows indicated on the y axis correspond to individual patients. with a 1° change in angle.
Numbers are shown in brackets.

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Clinical science

been variably stretched rather than there being a uniform displace- reported here with silicone oil tamponade and upwards dis-
ment. This explanation is consistent with the symptoms of distor- placement confirms a previous findings by Codenotti et al19
tion and change in image size, rather than double vision alone, in who had two patients with silicone oil tamponade in which
patients following retinal detachment surgery.1 Furthermore, all upwards displacement was seen. The numbers are not sufficient to
patients who had dysmetropia in this series and that of Ugarte and justify a definite conclusion, but the most likely explanation for the
Williamson,1 had micropsia and not macropsia; this would be direction of displacement in the patient we report relates to their
explained by the fixation target stimulating a smaller number of presentation with a giant retinal tear; the tear extended from 1 to
foveal photoreceptors than in the fellow eye and so further sup- 5 o’clock temporally, resulting in a very mobile retina. If drainage
ports the theory that at least some of the displacement seen is due was performed from the superior extent of this tear during silicone
to retinal stretch and hence greater separation between foveal oil exchange, it is conceivable that the retina would be displaced in
photoreceptors. Where patients do have double vision, the this direction, which we believe is a more likely explanation than
co-incident distortion means that prismatic correction is unlikely to theories related to the surface tension of oil.19
be able to induce fusion of the disparate images. Paradoxically, pris-
matic correction is therefore sometimes used to increase the dispar- Quantifying displacement
ity such that the patient can ignore the second image, as an One of our aims was to develop a means of quantifying dis-
alternative to the use of fogging lenses.12 placement such that comparisons could be made between
Macular folds are thought to arise from a combination of SRF, patients. Image magnification can vary with refractive error, and
intraocular gas and the effect of gravity on the SRF.13 Hypotony, potentially between visits due to small changes in focussing. All
scleral redundancy and undulations in the detached retina may images were therefore measured with reference to the optic disc
also play a contributory role.14 They may be formed deliberately diameter as a means of standardising the measurements.
in limited macular translocation surgery15 or inadvertently fol- Another challenge was how to identify points to measure
lowing retinal detachment surgery.16–18 It is likely that the retinal between as unless there is a vessel bifurcation, it is not possible
displacement detected here, which sometimes co-exists with to determine the precise point on a vessel ghost which corre-
partial thickness retinal folds, is a result of the same processes but sponds to a specific point on the corresponding retinal blood
to a lesser extent.5 8 14 19 It will therefore be interesting to see if vessel. It is to overcome this problem that the concentric circles
techniques to maximise drainage (eg, posterior retinotomies and were used; measurements were made between ghost vessel and
the use of perfluorocarbon liquids) or techniques to reduce the retinal blood vessel intersections on the same sampling circle.
propensity for folds to form in the presence of SRF (eg, small This method therefore involves an assumption that the shift of
volume 100% gas bubbles rather than complete gas fills, specific retinal blood vessels is primarily a rotation around the optic
post-operative posturing regimes, or pneumatic retinopexy) are disc, in keeping with the original description by Shiragami
effective at reducing displacement. At present there is no consen- et al.8 However, the results from our study indicate that there is
sus or proof of the effectiveness of these steps in reducing post- more to this movement than a simple rotation. Furthermore,
operative displacement and distortion. although shift of macula vessels was seen to be in the superior–
In the study by Shiragami et al8 of 43 consecutive patients inferior axis, it is to be noted that the vessels are predominantly
treated with vitrectomy and gas, perfluorcarbon liquids were horizontal and so shift in the horizontal axis would be harder to
used in the majority of cases (30/43) and in all cases drainage detect. In selected cases, shift in other directions could be seen
was through the break rather than via a posterior retinotomy. outside the macula (figure 2). The absolute values of displace-
Immediately following surgery, patients were sat up for several ment measured should therefore be used with caution but do
minutes before face-down or other positioning was commenced. allow comparisons over time, and have been sufficient to dem-
Displacement was detected in 27 of the 43 eyes (63%). In a onstrate here that the extent of movement is heterogeneous
smaller series by Codenotti et al,19 five out of five consecutive within the macula.
macular-off RRDs treated with vitrectomy and gas had evidence
of displacement; all of these patients were positioned face-down
immediately following surgery for an unspecified duration and CONCLUSION
then advised to avoid the sitting position. In our series there Macula displacement is common following vitrectomy retinal
were differences in drainage techniques, but almost all patients detachment repair with gas tamponade, and is associated with
were positioned macula down for over 60 min immediately fol- symptoms of distortion. It is heterogeneous within individuals,
lowing surgery. Despite this, there was still inferior displacement indicating variable stretch of the affected retina rather than a
in 72% of the fovea-involving detachments treated with vitrec- simple rotation. Measuring the extent of displacement will
tomy and gas. One explanation is that longer periods of post- permit comparisons over time and between individuals, and so
operative posturing could be required for full fluid reabsorption. opens the door for further research to study the aetiology and
However, the temporal displacement seen in study patient no. prognosis.
30 (figure 2 and see online supplementary data table) may indi- Contributors All authors contributed to study design and writing the paper. All
cate a potential risk from prolonged macula down posturing. An authors except for PH contributed to data collection. PH led the statistical analysis,
alternative approach, in the event of significant residual SRF, and described aspects of the study design.
may be to position patients supine with residual vitreous cavity Competing interests None.
fluid so as to avoid a fluid–gas gradient across the macula.11 Ethics approval Guy’s and St. Thomas’ NHS Foundation Trust R&D Department
There may be multiple reasons for displacement of blood vessels approved this study (reference RJ112/N127).
following surgery and it is likely that a larger study would be Provenance and peer review Not commissioned; externally peer reviewed.
required to identify specific risk factors.
To date, and to the best of our knowledge, all reported
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Macular displacement following


rhegmatogenous retinal detachment repair
Edward Lee, Tom H Williamson, Pirro Hysi, Manoharan Shunmugam,
Mahmut Dogramaci, Roger Wong and D Alistair H Laidlaw

Br J Ophthalmol 2013 97: 1297-1302 originally published online July 18,


2013
doi: 10.1136/bjophthalmol-2013-303637

Updated information and services can be found at:


http://bjo.bmj.com/content/97/10/1297

These include:

Supplementary Supplementary material can be found at:


Material http://bjo.bmj.com/content/suppl/2013/07/16/bjophthalmol-2013-3036
37.DC1.html
References This article cites 17 articles, 3 of which you can access for free at:
http://bjo.bmj.com/content/97/10/1297#BIBL

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Topic Articles on similar topics can be found in the following collections


Collections Retina (1458)
Ophthalmologic surgical procedures (1115)

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