Br J Ophthalmol 1999;83:420-424 ( April )
Assessment of macular function by multifocal electroretinogram
before and after macular hole surgery
Ying-Jie Si,
Shoji Kishi,
Koji Aoyagi
Department of
Ophthalmology, Gunma University School of Medicine, Japan
Correspondence to: Ying-Jie Si, MD, Department of Ophthalmology, Gunma University School
of Medicine, 3-39-15 Showa-machi, Maebashi 371, Japan.
Accepted for publication 22 September 1998
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Abstract |
AIM To evaluate
macular function before and after successful surgical closure of
idiopathic macular holes using multifocal electroretinogram (ERG).
METHODS 40 patients
(40 eyes) with idiopathic macular holes were examined using multifocal
ERG both before and after vitreous surgery. The postoperative period
was from 1 to 12 months.
RESULTS Preoperatively,
the electrical retinal response densities in the foveal and the
perifoveal area were apparently decreased. After a mean
postoperative period of 3-6 months, the foveal and perifoveal area
electrical retinal response densities improved to two to four times the
preoperative level and the improvement continued to 1 year after surgery.
CONCLUSION In macular
holes, the decrease in retinal electrophysiological response was not
limited to the fovea but involved an area of the perifovea of 1.6 disc diameters. The electrical retinal response density of these areas
gradually improved after macular hole closure.
(Br J Ophthalmol 1999;83:420-424)
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Introduction |
Idiopathic macular holes are treatable with vitrectomy. After
successful hole closure, most patients gain two or more lines of visual
acuity until 6-12 months postoperatively, and resolution of
metamorphopsia occurs. The mechanism by which visual function improves
is not understood. Visual function before and after macular hole
surgery generally is assessed by visual acuity
measurement.1-6 However, the visual acuity level
represents only a part of the impaired visual function resulting from
macular hole development, which includes metamorphopsia, blurred
vision, and scotoma. There have been few methods to evaluate these
subjective symptoms. Some researchers used objective methods such as
focal electroretinogram (ERG) to evaluate macular
function,7-10 which reflects the different spatial
distributions of the retinal receptors and supporting tissues. However,
this method requires prolonged recording times and varying signal to
noise ratios. Because focal ERG was designed to assess the macular area
within 10 degrees, it cannot evaluate the electrophysiological response
in the perimacular area. Multifocal ERG, introduced by Sutter
et al,11 12 resolves these
limitations, because multiple retinal locations can be tested
simultaneously, and allows functional mapping of the retina.
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Patients and methods |
Forty eyes of 40 patients diagnosed with idiopathic macular holes
in stages 2 to 4 (three, 34, and three eyes, respectively), according
to Gass's classification,13 14 were examined by
multifocal ERG before and after vitrectomy. The ages of the patients
ranged from 48 to 78 years (average 64 years). The macular holes were successfully closed in all 40 eyes. All the patients were examined and
diagnosed by the same doctor (SK) before and after surgery and those
who had apparent cataract was excluded from our study in order to avoid
the cataract influence on our multifocal ERG study. Multifocal ERG were
recorded preoperatively and 3 months, 6 months, and 1 year after
surgery. A visual evoked response imaging system (VERIS III, Tomey
Corp, Nagoya, Japan) was used for the ERG recording. The multifocal ERG
stimulus matrix consisted of 103 hexagons that scale concentrically and
covered the central 50 degrees of the fundus area (Fig 1A). Each
hexagon alternated between black and white in binary m-sequences at the
rate of 75 Hz. The range of luminance levels is 5-200
cd/m2. The central hexagon (area 1, foveal area)
corresponded to approximately 2.8 degrees of the fundus area. We used
the cuneiform indicator rather than the pointer for fixation because
patients had a central scotoma. A Burian-Allen bipolar contact lens
electrode was used for signal derivation. A ground electrode was
attached to the earlobe. The pupil of one eye was dilated with 0.5%
tropicamide and 0.5% phenylephrine hydrochloride, and the fellow eye
was occluded. The net recording time for each eye was 4 minutes; the
entire procedure was divided into eight 30 second segments. The signal were amplified (100 000) and bandpass filtered (10-300 Hz). Three dimensional topography (Fig 1B) represented the retinal response density (amplitude per retinal area, nV/deg2). The
recording procedure was repeated if there were spurious potentials from
eye blinks or ocular movement were recorded.

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Figure 1
Schema of the stimulus matrix of multifocal ERG (A),
and three dimensional scalar plots of ERG responses obtained from the
left eye of a normal subject (B). There is a sharp peak at the foveal
area and slight depression at the optic disc (arrow).
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Results |
The mean preoperative retinal response densities in 40 eyes with
macular holes (three eyes with stage 2, 34 with stage 3, and three with
stage 4) examined were 3.77 (SD 2.03) nV/deg2 in area 1 (foveal area of 2.8 degrees) and 3.82 (2.58) nV/deg2 in
area 2 (perifoveal area of 3-9 degrees from the centre). At the
examination performed 3 months postoperatively, the mean retinal response densities improved to 6.99 (2.69) nV/deg2 in area
1; 5.01 (2.54) nV/deg2 in area 2. Six months after surgery
the mean retinal response density further improved to 8.27 (2.69)
nV/deg2 in area 1 while the mean retinal response density
in area 2 was at the same level (5.16 (2.38) nV/deg2).
Figure 2 shows the relation of the retinal response densities in area 1 before and 6 months after surgery in the 40 eyes (rp=0.57, p<0.001).
The retinal response density improved even in three eyes with unchanged
visual acuity. Although a positive correlation was seen between the
postoperative retinal response density and the visual acuity (rp=0.46,
p<0.01), the retinal response density varied at wide range in eyes
with the same visual acuity (Fig 3).

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Figure 2
Relation between preoperative and postoperative
retinal response density 6 months after surgery. Retinal response
density increased in all eyes (p<0.001).
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Figure 3
Association between visual acuity and the
retinal response density 6 months after surgery. A positive correlation
between response density and visual acuity is seen (p<0.01). Retinal
response density varied in eyes with the same visual acuity.
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The retinal response density gradually increased until 1 year
postoperatively in six of the 40 patients who were examined by the
multifocal ERG 12 months after vitrectomy. The mean central postoperative retinal response density (area 1) was 8.74 (2.45) nV/deg2.
CASE 1
A 75 year old man with a stage 3 macular hole in his left eye had
a preoperative visual acuity level of 0.1. The topography of the
retinal response density was markedly depressed in the macular area
(Fig 4A, B). The retinal response density of area 1 was 4.14 nV/deg2. A multifocal ERG was repeated at 1, 3, and 6 months postoperatively. The retinal response density of area 1 improved
to approximately 5.78, 7.76, 11.91 nV/deg2 accompanied by a
visual acuity improvement to 0.2, 0.3, and 0.5, respectively. The
postoperative changes of multifocal ERG topography are seen in Figure 4
(C, D and E, F).

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Figure 4
Multifocal ERG of a 75 year old man with a stage 3 macular hole (case 1, left eye) before and after surgery. Preoperative
fundus photograph (A) and multifocal ERG topography (B). Foveal and
perifoveal area (areas 1 and 2) showed crater like depression.
Multifocal ERG recorded at 1 month (C) and 3 months (D)
postoperatively. The peak recovered in the macular area. Fundus
photograph (E) and multifocal ERG topography (F) 6 months
postoperatively.
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CASE 2
A 62 year old man with a stage 3 macular hole in his right eye
underwent a preoperative multifocal ERG, the topography of which showed
a marked central depression of approximately 8 degrees both in the hole
and the surrounding area. The central retinal response density was 3.17 nV/deg2 preoperatively and improved to 9.12 nV/deg2 6 months postoperatively. The visual acuity
improved from 0.1 to 0.4 (Fig 5).

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Figure 5
Fundus photograph and multifocal ERG of a 62 year old
man with a stage 3 macular hole (case 2, right eye) before and after
surgery. (A) Fundus photograph preoperatively. Macular hole is larger
than that of the patient in case 1. (B) Multifocal ERG topography
showed more widespread crater-like depression in macular area than that
in case 1. Fundus photograph (C) and multifocal ERG topography (D) 6 months postoperatively. Macular hole had closed. The peak of the
retinal response density was restored in macular area in the topography
of multifocal ERG.
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Discussion |
The results of multifocal ERGs recorded preoperatively in 40 eyes
showed marked decreases in retinal response densities that were not
only limited to the fovea but also involved the perifoveal area. We
previously observed the morphological features of macular holes
using scanning laser ophthalmoscopy.15 Henle's fibre
layer was elevated around the macular holes, forming radiating striae. They were seen in approximately 10 degrees of the perifoveal area in
full thickness holes. The findings of optical coherence tomography indicated that the perifoveal radiating striae represent intraretinal splitting or retinoschisis.16 Decreased retinal response
density in the perifoveal area (area 2) seems to reflect perifoveal retinoschisis.
The improvements in the retinal response density in the foveal
area (area 1) appeared to reflect the closure of the macular holes with
proliferated glial cells and centripetal displacement of surrounding
photoreceptor cells.17 18 Resolution of the central
scotoma seems to be attributed to anatomical repair in area 1. The
radiating striae of the Henle's fibre layer disappeared following
macular hole closure.15 The improvement of retinal response density in area 2 along with resolution of metamorphopsia is
presumably achieved by reattachment of perifoveal retinoschisis. The
improvement of the retinal response density continued to 12 months
postoperatively. The increases in the mean postoperative retinal
response density in the 40 study eyes in area 1 indicate that the
intraretinal neural network was restored with time after the closure of
the macular holes.
The origin of the electrophysiological responses in the multifocal
ERG remains controversial. Recently, some researchers studied the
effect of filter bandwidth on the multifocal ERG.19 Other researchers recorded multifocal ERG in normal eyes and eyes with diabetic retinopathy.20-22 A multifocal ERG study in eyes
with branch retinal artery occlusion demonstrated decreased
electrophysiological responses in the ischaemic area,23
suggesting that the multifocal ERG reflects not only the
electrophysiological responses of cones but also that of the inner
retinal layer including bipolar and Mueller's cells. In eyes with
macular holes, a decreased retinal response density seems to reflect
the loss of photoreceptors in the fovea and the retinoschisis in the
perifoveal area. Multifocal ERG is a useful method to evaluate retinal
function in macular holes before and after surgery.
In full thickness macular holes, electrophysiological dysfunction was
not limited to the fovea but involves its surrounding area. Reparation
of the intraretinal neural network seems to continue up to 1 year after
surgical closure of macular holes.
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Acknowledgments |
Presented in part on 14 May at the 1997 annual meeting of the
Association for Research in Vision and Ophthalmology, Fort Lauderdale, Florida, USA.
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© 1999 by British Journal of Ophthalmology
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