Clinical Study
Microperimetric Assessment after Epiretinal Membrane Surgery:
4-Year Follow-Up
Marco Dal Vecchio, Carlo Lavia, Marco Nassisi, Federico M. Grignolo, and Antonio M. Fea
Department of Surgical Sciences, Eye Clinic, University of Turin, 10122 Turin, Italy
Correspondence should be addressed to Carlo Lavia; carlo.lavia@gmail.com
Received January ; Accepted March
Academic Editor: Samuel N. Markowitz
Copyright © Marco Dal Vecchio et al. is is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Purpose. To investigate retinal function using microperimetry in patients aected by idiopathic epiretinal membrane (iERM) and
cataract who underwent combined surgery: -year follow-up. Design. Prospective, interventional case series. Methods.eyesof
consecutive patients with iERM and age-related cataract underwent -gauge vitrectomy and cataract surgery. At baseline, and
days,andandyears,weexaminedretinalmeansensitivity(MS),retinalmeandefect(MD),xationstability,andfrequency
of microscotomas using MP microperimetry. Best-corrected visual acuity (BCVA) and central retinal thickness (CRT) using a
spectral domain optical coherence tomography (SD-OCT) were also performed. Results. All patients completed -year follow-up,
while patients reached last follow-up. Baseline MS and MD (. ± . and −. ± . dB) signicantly changed at one year
(. ± . and −. ± . dB, 𝑝 < 0.01), at four years (. ± . and −. ± ., 𝑝 < 0.01), and between one and four years
(𝑝 < 0.01) aer surgery. Compared to baseline, CRT and BCVA signicantly changed at one year and remained stable at four years.
No variations were observed in xation stability and frequency of microscotomas compared to baseline. Conclusions.Long-term
follow-up using microperimetry seems useful to evaluate patients aer iERM surgery: retinal sensitivity changes even when BCVA
and CRT remain stable.
1. Introduction
Idiopathic macular epiretinal membrane (iERM) is a rela-
tively common disorder, with an incidence reaching % in
those older than years [].
Dierent hypothesis has been advanced about iERM
pathogenesis. On one hand, iERM seems to begin with
microfractures in the inner retina aer posterior vitreous
detachment, while, on the other hand, it seems to occur when
the external layer of the posterior vitreous cortex remains
attached to the macula. iERM can vary from a single layer
to a thick, multilayer brocellular proliferation shrinking t he
retinal surface [].
Although patients with iERM can be asymptomatic at
the beginning, they may complain of various degree of visual
symptoms: distortion of lines (metamorphopsia), decreased
visual acuity, macropsia, micropsia, and monocular
diplopia.
In symptomatic patients, the surgical removal of the
epiretinal membranes with pars plana vitrectomy (PPV) is the
gold standard surgical procedure [, ].
PeelingoftheILMduringsurgeryisstilldebated.Accord-
ing to Bu et al., it could be advisable to remove ILM to
reduce ERM recurrence by eliminating the scaold for the
proliferation of brocellular tissue []. On the contrary, Liu
et al. reported that ILM + ERM peeling compared to ERM
peeling alone, achieved better best-corrected visual acuity
(BCVA) months aer surgery but not aer months,
showing that a longer follow-up would be advisable [].
Quality of life, contrast, and color sensitivity are becom-
ing useful parameters in the workup of patients aected by
iERM, together with visual acuity and retinal morphology.
Microperimetry provides information on foveal xation,
macular sensitivity, and depth of central mac ular defects and
is gaining interest in the assessment of various retinal diseases
[–].
Hindawi Publishing Corporation
Journal of Ophthalmology
Volume 2016, Article ID 7030791, 5 pages
http://dx.doi.org/10.1155/2016/7030791
Journal of Ophthalmology
Microper imetry, before and aer iERM surgery, can help
the surgeon in evaluating which kind of patients could benet
from surgery and what could be their prognosis. Moreover,
thanks to the autotracking system that corrects involuntary
eye movements and the possibility to do follow-up examina-
tions, it allows a greater reliability and reproducibility of the
tests than automated perimetry [, ].
Long-term follow-up is a useful tool to evaluate the
eectiveness of a treatment, especially when a total consensus
about the timing of a surgical procedure is still not available.
Aimofthestudywastoinvestigatethepotentialrecovery
of retinal functions assessing the microperimetric outcomes
in patients aected by iERM and cataract who underwent -
gauge PPV with ILM peeling combined with phacoemulsi-
cation and intraocu lar lens (IOL) implantation in a long-
term follow-up. CRT and visual acuity outcomes were also
analyzed.
2. Materials and Methods
is interventional open label study has been approved by the
Local Institutional Ethics Committee and Review B oard and
registered on ClinicalTrials.gov (number NCT). e
research adhered to the tenets of the Declaration of Helsinki
and written informed consent was obtained from all patients
before participation in the study.
From October to July , eyes of consecutive
patients aected by idiopathic epiretinal membranes and
variousdegreeofcataractwererecruitedforthestudy.All
patients underwent a combined -gauge PPV, phacoemul-
sication, and IOL implantation.
Inclusion criteria were iERM clinical nding, macular
thickness > 𝜇m as measured by Spectral-Domain OCT
(SD-OCT,RTVue,Optovue,Fremont,CA),presenceof
metamorphopsia at the Amsler grid chart, and a visual acuity
loss of Snellen lines in the last six months.
Exclusion criteria were glaucoma, corneal or lens opaci-
ties that precluded an acceptable retinal visualization, ocular
axial length > mm (measured with A-Scan biometry),
epiretinal membrane secondary to trauma or vascular dis-
eases, any macular degeneration, diabetic retinopathy, and/or
previous ophthalmic surgery.
All patients underwent a routine ophthalmic examination
(before and at , , , , , and days aer surgery)
including slit-lamp biomicroscopy, B CVA with t he Early
Treatment Diabetic Retinopathy Study (ETDRS) score at
meters, dilated fundus examination, and intraocular pressure
measurement using Goldmann Tonometry.
OCT examination calculating central retinal thickness
(CRT) in the central mm using the Macular Map ×
mm (MM) and microperimetry with the MP (Nidek
Technologies, Padova, Italy) were performed before surgery
and at , , and days aer surgery.
Pa tients were called back to our center four years aer the
intervention to assess long-term functional and morphologi-
cal outcomes.
2.1. Surgical Proce dure. An expert vitreoretinal surgeon
(MDV)performedallsurgicalprocedures.Aertheinsertion
of three -gauge cannulas, t hrough a . mm clear-cornea
incision, phacoemulsication of the lens was performed.
A foldable intraocular lens (IOL) Akreos AO (Bausch and
Lomb, Rochester, NY, USA) was implanted in all cases.
e core vitrectomy was performed with the Accu-
rus machine G+ (Alcon Laboratories, Fort Wort h, TX,
USA). e posterior hyaloid membrane, if not spontaneously
detached, was dyed with micronized tri amcinolone acetonide
(IVT, BIOOS, Italy), separated by aspiration, and removed.
Aer the extension of vitrectomy to the ora serrata the
MembraneBlue-Dual dye (DORC, Zuidland, Netherlands)
was used in order to peel the ERM and the ILM within
the vascular arcades, with a -gauge micro forceps (Alcon
Laboratories). A second stain with MembraneBlue-Dual
dye was applied to check whether the ILM peeling was
completed. An accurate inspect ion of the peripheral retina
and the photocoagulation of eventual retinal holes, tears, or
rhegmatogenous degenerations was followed by the exchange
of the balanced salt s olution (BSS) with ltered air and
cannulas removal.
Tobramycin .% and dexamethasone .% eye drops
were prescribed times a day for a month aer surgery.
2.2. Microperimetry. All images were acquired by an expert
examiner.
Patient sat in front of the MP with the head carefully
aligned in the chin rest and against the forehead strap.
All subjects underwent the exam under dim light con-
ditions with dilated pupil in the study eye. Fellow eye was
patched. Aer the baseline visit, all other examinations were
performed using the “follow-up” mode.
A
∘
grid of spots was centered on the fovea region.
Stimulus size was Goldmann III white spot, with a stimulus
duration of ms. reshold strategy was HFA -, and
background luminance was . cd/m
2
( asb).
Stimulus attenuation ranged from dB that represents
the instrument’s maximum stimulus luminance to dB that
represents the minimum stimulus luminance.
e xation point was set as single white cross of
∘
of spa-
tial width. e automatic eye tracker was used to compensate
eye movements and to calculate horizontal and vertical shis
relative to a reference frame during the examination. e
recorded xation points were classied into three categories
for xation stability analysis (stable, relatively unstable, and
unstable). Fixation was regarded as “stable” if more than
% of the xation points were inside the
∘
diameter circle,
as “r elatively unstable” if <% were inside the
∘
diameter
circle but more than % inside the
∘
diameter circle, and as
“unstable” if <% were inside the
∘
diameter circle. Fixation
stability was considered for statistical analysis.
Mean sensitivity (MS), mean defect (MD), and the total
number of absolute scotoma locations (points with a thresh-
old value of dB) in the
∘
central area were evaluated.
Mean retinal s ensitivity is the arithmetic mean of all the
measured absolute thresholds expressed in dB; mean retinal
defect is the arithmetic mean of all local defects, including the
values above the upper limits (expressed in dB).
Journal of Ophthalmology
T : Demographic characteristics.
Patients 𝑛/eyes 𝑛
/
Male/female
(%)/ (%)
Age at enrollment, years (mean
values ± standard deviation)
. ± . (range –)
Patients at year follow-up
(%)
Patients at years follow-up
(.%)
2.3. Outcome Measures. Primary outcome measures were the
changes in MS and MD.
Secondary outcomes were the changes in BCVA, CRT,
xation stability at
∘
and
∘
, and frequency of microscotomas
in the
∘
area.
2.4. Statistical A nal ysis. Statistical analysis was carried out
with Analyse-it statistical soware for Microso Excel (ver-
sion .; Analyse-it Soware, Leeds, UK). e Shapiro-Wilk
testwasemployedtoverifyifdatawerenormallydistributed.
Dierences in BCVA, CRT, and microperimetry values before
and aer surgery were determined with the Wilcoxon signed-
ranks tests.
e values of 𝑝 < 0.05 were considered statistically
signicant.
Data are presented as mean ± standard deviation.
3. Results
patients aected by iERM and age-related cataract were
enrolled. ere were males and mean age was . ±
years. All patients completed the -year follow-up visit,
whereas of them (.%) completed the -year follow-up.
Preoperative demographics are reported in Table .
patients were unable to attend the last follow-up visit:
had moved to another city, were unable to come to our
center, and of them died.
In the patients who completed the -year follow-up,
no signicant dierences at all study visits were detected
compared to the patients who completed the one-year
visit.
All data were normally distributed.
Microperimetric MS and MD trends are reported in
Figure . Secondary outcomes trends are reported in Table .
Statistical analysis is resumed in Table .
3.1. Intraoperative and Postoperative Complications. No sig-
nicant intraoperative complications were recorded. In one
case (.%), a l aser photocoagulation was required due to
alittleiatrogenicholebeyondthevasculararcades,without
consequencesforthemacularfunctionorthevisualacuity.
patients (%) developed posterior lens capsule opacity
and underwent YAG laser capsulotomy before follow-up
exams.
3.2. Best-Corrected Visual Acuity . Preoperative mean visual
acuity sig nicantly improved (𝑝 < 0.01)aersurgeryatboth
and years. e highest gain in mean visual acuity was
Preoperative 90 days 180 days 1 year 4 years
Preoperative
90 days 180 days 1 year 4 years
12.50 ± 3 .41
10.48 ± 4.17
12.32 ± 3.86
12.33 ± 3.66
14.18 ± 3.46
−9.18 ± 4.40
−6.96 ± 3.15
−7.11 ± 3.48
−7.49 ± 3.41
−4.66 ± 2.85
0.00
2.00
4.00
6.00
8.00
10.00
12.00
14.00
16.00
18.00
20.00
Mean sensitivity (DB)
0
−2
−4
−6
−8
−10
−12
−14
−16
−18
−20
Mean defect (DB)
Mean sensitivity (mean ± SD)
Mean defect (mean ± SD)
F : Mean sensitivity and mean defect values before and aer
surgery (mean ± standard deviation).
documented at years although no signicant dierences
were found between year and years (𝑝 = 0.08).
Compared to baseline, at one and years, / (.%)
and / patients (.%) presented a gain in visual acuity >
ETDRS lines, respectively.
Mean BCVA change was of . ETDRS lines at one year
and . ETDRS lines at years.
3.3. OCT-CRT. Preoperative mean CRT signicantly
changed (𝑝 < 0.01)aersurgeryatbothandyears.
Baseline mean value was . ± . 𝜇m, while at one and
four years . ± . 𝜇mand.± . 𝜇mwere,
respectively, measured. In one patient, the CRT increased
( 𝜇matoneyearand𝜇matyears)probablydueto
preoperative borderline CRT value ( 𝜇m). No signicant
changes were observed in mean CRT values between and
years (𝑝 = 0.08).
3.4. Microperimetry. Signicant dierences (𝑝 < 0.01)were
found between preoperative and postoperative data at one
and four years for both mean retinal sensitivity and mean
defect (Figure ).
At baseline, one year, and fo ur years the mean retinal
sensitivity in the
∘
central area was . ± . dB, . ±
. dB, and . ± . dB, respectively.
At baseline, one year, and fo ur years the mean retinal
defect in the
∘
central area was −. ± . dB, −. ±
. dB, and −. ± . dB, respectively.
Signicant dierences were found in MS and MD
between one and four years aer surgery (𝑝 < 0.001).
Journal of Ophthalmology
T : Secondary outcomes (mean values ± standard deviation; LogMAR: logarithm of minimal angle of resolution; CRT: central retinal
thickness).
Baseline Day Day Day years
LogMAR . ± . . ± . . ± . . ± . . ± .
CRT (𝜇m) . ± . . ± . . ± . . ± . . ± .
Fixation in central
∘
(%) ± . . ± . . ± . . ± . . ± .
Fixation in central
∘
(%) . ± . . ± . . ± . . ± . . ± .
Microscotomas in central
∘
(𝑛).± . . ± . . ± . . ± .± .
T : Statistical analysis (MS: mean sensitivity; MD: mean defect; Fix: xation; BCVA: best-corrected visual acuity ; CRT: central retinal
thickness).
𝑝 value–Wilcoxon test MS MD
∘
microscotoma Fix
∘
Fix
∘
BCVA CRT
Preoperative versus days . . . . . <. <.
Preoperative versus days . . . . . <. <.
Preoperative versus year . . . . . <. < .
Preoperative versus years . <. . . . <. <.
year versus years . <. . . . . .
No signicant dierences in xation stability in the
central
∘
and
∘
werefoundatallvisits.esameobservation
was made for the number of microscotomas in the central
∘
.
4. Discussion
Surgical approach in symptomatic patients with iERM
showed good results in terms of visual acuity and retinal
function recovery with minimal surgical complications and
no recurrence of pathology.
e application of dyes during vitreoretinal surgery
improved visualization of ERM and the vitreoretinal inter-
face. e toxic eect of dyes used during the peeling cannot
be excluded. However, Trypan blue and Brilliant blue G used
in this study are recognized safe staining agents with no or
minimal toxic eects on retina at the concentrations used
[].
When patients present a certain degree of cataract, the
association of PPV with cataract surgery enables a better
visualization of the retina.
Moreover, PPV in phakic eyes determines a progression
of nuclear sclerosis [], and, aer vitreoretinal surgery,
phacoemulsication is more dicult and with a greater rate
of complications [, ].
Our patients showed a signicant and early improvement
of functional outcomes and a reduction of CR T at OCT, as
reported in the literature [–].
Although aer iERM surgery BCVA continues to improve
up to years, best values are reached at about year, in
accordance with our ndings, as no changes have been
detected between and years [–].
As observed by Ripandelli et al. in patients who under-
went ILM peeling, in our study the number of microscotomas
in the
∘
analyzed area improved aer surgery, although not
signicantly [].
With a steady xation stability over time, MS and MD
interestingly increased between and years, demonstrating
a signicant dissociation between BCVA and retinal sen-
sitivity, as has already been demonstrated in other retinal
pathologies, underlying the microperimetry capability to
detect even subtle changes in patients’ quality of life [].
As in our study combined surgery was performed in all
cases, it was impossible to determine if the immediate post-
operative outcome improvements were completely associated
with the iERM removal or with cataract extraction or both.
On the other hand, the double procedure removed an
important potential confounding factor in the evaluation of
the outcomes aer surger y.
is study has some limitations: the small sample size
analyzed might have inuenced the power of the study, the
incomplete follow-up of some patients (only % at four
years), and the absence of a quantication of metamorphop-
sia (e.g., M-Chart) providing another quality of life parameter
[].
5. Conclusions
In conclusion, microperimetry proved an eective diagnostic
tool in evaluating subtle changes in retinal function, unde-
tectable with a visual acuity exam. Long-term follow-up aer
vitreoretinal surgery would b e advised to reveal changes in
retinal sensitivity aecting patients quality of life.
e use of high denition imaging techniques to analyze
further aspects of this pathology such as correlation between
long-term anatomical changes and microperimetric data are
recommended.
Competing Interests
e authors declare that they have no competing interests.
Journal of Ophthalmology
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