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Visual field changes after pars plana vitrectomy

377

 

 

VISUAL FIELD CHANGES AFTER PARS PLANA VITRECTOMY AND INTERNAL LIMITING MEMBRANE PEELING

FRANCESCO MORESCALCHI, RAFFAELE TURANO, FABRIZIO DANIELI, STEFANO FORMENTI, FEDERICO GANDOLFO and ENRICO GANDOLFO

Department of Ophthalmology University of Brescia, Spedali Civili di Brescia, Brescia, Italy

Introduction

Macular distortion and macular edema with resulting macular dysfunction are recognized sequelae of epimacular proliferation and cellophane appearance of the posterior pole. Macular hole is also often surrounded by cellophane-like retina. This appearance represents retinal internal limiting membrane (ILM) distortion by surface proliferative cells. The cellophane-like quality of the ILM may also occur months after apparently successful epimacular proliferation removal, which limits visual recovery. The ILM is the basement membrane of the Müller cells, and can act like a scaffold for cellular proliferation in the pathophysiology of disorders affecting the vitreomacular interface. Specimens analyzed after vitrectomy for epimacular membrane removal often contain ILM fragments, which have been intentionally or unintentionally removed to treat traction maculopathy.1

When spontaneously denuded of the ILM in hemorrhagic macular cysts caused by Terson’s syndrome, the macula displays no significant reparative fibrosis and maintains excellent visual function at long-term follow-up.2,3

Some studies have pointed out that a small amount of traction exacerbates diabetic macular edema.4 Other authors have advocated intentional removal of macular ILM in macular hole surgery for the important reason of increased elasticity of the denuded macula in hole closure.5,6 Therefore, atraumatic removal of the macular ILM is recommended in the treatment of some forms of traction maculopathy, such as epimacular proliferation, macular hole, and some forms of chronic diabetic macular edema.7

Recently, techniques for the intraocular use of indocyanine green (ICG) dye in order to facilitate visualization of the ILM have been described. ICG staining of the ILM facilitates peeling, by providing a stark contrast between the stained ILM and the unstained retina.8-10 This new technique was an important surgical development, since

Address for correspondence: Francesco Morescalchi, MD, Clinica Oculistica Università degli Studi di Brescia, c/o Spedali Civili, Piazzale Spedali Civili 1, 25125 Brescia, Italy. Email: oculistica@genie.it

Perimetry Update 2002/2003, pp. 377–384

Proceedings of the XVth International Perimetric Society Meeting, Stratford-upon-Avon, England, June 26–29, 2002

edited by David B. Henson and Michael Wall

© 2004 Kugler Publications, The Hague, The Netherlands

378 F. Morescalchi et al.

it improved the capability to clean the posterior pole from every cellular proliferation, and thus prevent membrane relapse. However, recent studies supported the hypothesis that ICG dye could be toxic for the retina if injected directly into the eye; this damage possibly being due to direct contact with the retinal pigment epithelium,11,12 or with the inner retinal layers.13,14 Moreover, it is still unclear what the effect is of ICGassisted peeling of the ILM on macular function.

Most authors who used ICG dye for ILM peeling reported good results for visual acuity (VA), in either macular hole or epimacular membrane surgery. However, the VA level only represents part of the impaired visual function resulting from traction maculopathy, which also includes metamorphopsia, blurred vision, and impaired reading ability.

Visual field tests are one method of evaluating these visual disturbances. In the present investigation, we present visual field data after ICG-assisted peeling of the ILM in traction macular pathology.

Patients and methods

Twenty-two patients (24 eyes) with traction maculopathy (six eyes with macular hole, 14 with macular pucker, four with diabetic macular edema) were examined by visual field test before and after vitrectomy. The age of the patients ranged from 53 to 80 years (mean age, 67 years). Thirteen patients were female and 11 were male. A successful macular peeling operation was performed in all 24 eyes. Patients with cataract underwent a phacoemulsification three months before the start of the study. In patients with macular hole, a routine clear lens extraction by phacoemulsification and IOL implantation was performed just before vitrectomy.

All eyes underwent complete pars plana vitrectomy, including removal of the posterior hyaloid, if not yet detached, and removal of all the visible epiretinal membranes. ILM maculorrhexis was the usual method of ILM removal.4 Using direct grasping of the ILM with end-opening forceps, a small ILM flap was raised and a rhexis created, slowly tearing the ILM in a circular motion, concentric with the fovea. This maneuver requires patience and good visualization, in order to avoid engaging the neurosensory retina. The aim of maculorrhexis was to produce minimal foveal traction during complete removal of the macular ILM. If the fovea was noted to be under traction during this procedure, the peeling force vector was re-directed slightly toward the fovea, until the traction was resolved. Tearing was then continued. All these maneuvers can be technically challenging, even for experienced vitreoretinal surgeons, because of the difficulty in visualizing this diaphanous structure. For this reason, 0.1-0.3 ml of 0.25% ICG solution (IC-GreenTM Akorn Inc., Buffalo Grove) was instilled directly into the posterior vitreous cavity, after having turned off the infusion. In this way, the ICG dye tended to settle over the macula, and was then passively aspirated after about one minute by means of a Charles’ needle.

After ICG removal, the ILM was peeled throughout the posterior pole (from the temporal edge of the optic nerve to the temporal vascular arcades) using Eckardt’s intraocular forceps. Complete air-fluid exchange was then followed by treatment of the macular holes, filling the eye with a long-acting gas (C3F8 15%) at the end of the procedure. The differential retinal light threshold was measured across the visual field

Visual field changes after pars plana vitrectomy

379

before and after surgery by the means of a Humphrey Field Analyzer (HFA-II, San Leandro, CA). The central visual field was tested using the 10-2 and 24-2 (or 30-2) programs. Visual field tests were carried out, together with far and near visual acuity tests and reading speed.

Results

The mean preoperative visual acuity was 0.13 (Snellen). Postoperative follow-up ranged from four to eight months (mean, four months). No complications occurred during the follow-up period. The mean postoperative visual acuity was 0.37. The improvement in visual acuity (Table 1) was two lines or more in 17 eyes (two patients with macular hole, 12 with macular pucker, and three diabetics with macular traction). In the remaining seven eyes, visual acuity remained unchanged (four patients with macular hole, two with macular pucker, and one with diabetic traction maculopathy). One case of macular hole surgery was not successful in terms of healing of the macular hole.

Reliable determinations of differential retinal light threshold using the HFA were obtained from all patients, who showed negligible false-positive or false-negative responses at each testing session. Table 2 summarizes the results of visual field tests. Preoperatively, the average mean deviation (MD) was -6.38 dB in the central 10°, which represents the foveal area, and -7.12 dB in the central 24°, representing the posterior pole. Four months after surgery, visual field recording revealed an average

Table 1. Visual acuity (VA)* and mean sensitivity (MS)** variation four months after ILM peeling

 

VA

VA

VA

MS

MS

MS

 

improved

worse

unchanged

improved

worse

unchanged

 

 

 

 

 

 

 

Macular hole

2

0

4

1

2

3

Macular pucker

12

0

2

4

3

7

Diabetic with macular

 

 

 

 

 

 

traction

3

0

1

1

0

3

 

 

 

 

 

 

 

*improvement or worsening of two or more visual acuity lines; **increase or decrease of 4 dB or more of differential light threshold

Table 2. Preand postoperative (four months) visual acuity, mean deviation (10-2 program) and reading speed (words per minutes)

 

VA before

VA after

MD (10-2)

MD (10-2)

Reading

Reading

 

surgery

surgery

before

after

 

 

speed before

speed after

 

 

 

surgery

surgery

 

surgery

surgery

 

 

 

 

 

 

 

 

 

 

 

Macular holes (six)

0.09 ± 0.01

0.16 ± 0.11

-9.89 ± 9.2

-9.3

±

3.5

48.4

± 24.9

52

± 30.2

Macular pucker (14)

0.17 ± 0.13

0.50 ± 0.27*

-4.6 ± 2.7

-5.7

±

4.0

88.3

± 20

120

± 29*

Macular traction

 

 

 

 

 

 

 

 

 

 

(four)

0.21 ± 0.16

0.55 ± 0.24*

-13.5 ± 5.1

-12.0 ±

6

64.4 ± 31.9

122

± 19.4*

All 24

0.13 ± 0.09

0.37 ± 0.26*

-6.38 ± 5.8

-7.0

±

3.9

74

± 41

117

± 42*

 

 

 

 

 

 

 

 

 

 

 

* ANOVA test p < 0.05

380

 

 

F. Morescalchi et al.

Table 3. Static perimetry findings in all patients who underwent ICG-assisted ILM peeling

 

 

 

 

 

 

 

 

 

 

Preoperative

1 month

4 months

ANOVA

 

 

 

 

 

 

 

 

 

Mean sensitivity

25.3 dB ± 4.8

23.7 dB ± 4.4

24.8 dB ± 3.3

F = 2.9,

p =

0.07

Mean deviation

-6.38 dB ± 5.8

-7.9 dB ± 5.7

-7.0 dB ± 3.9

F = 0.4,

p =

0.4

Pattern standard deviation

5.5 dB ± 5

4.5 dB ± 2.8

3.4 dB ± 2.1

F = 1.16, p =

0.332

 

 

 

 

 

 

 

MD of -7.0 dB in the central 10° and of -7.58 dB in the central 24°. Preand postoperative (four months) mean sensitivity (MS), MD, and pattern standard deviation (PSD) did not show any statistically significant modification (ANOVA test).

A trend toward a decrease in MS (mean, -1.6 dB) into the central 10° was registered during the first month of follow-up. After four months, the central MS had a tendency to return to the preoperative level (Table 3). Four months after the operation, the visual field test (10-2 program) revealed an improved retinal differential light threshold (+4 dB or more) in six eyes, stable in 13 eyes, and worsened (-4 dB or more) in five eyes (two patients with macular hole, three with macular pucker; Table 1).

Postoperatively, in one patient with macular hole, a new absolute central scotoma was detected. In two patients with macular pucker, an absolute fascicular defect (first case) and an absolute focal defect (second case) were evident after surgery. Improvement of reading speed was evident in two patients with macular hole, in 12 patients with macular pucker, and in all patients with traction macular edema.

Discussion

To the best of our knowledge, there are few previous reports in literature on modification of the central visual field after epiretinal membrane surgery. Most patients with no macular hole showed a satisfactory recovery after ICG-assisted successful removal of the membrane. VA improved in 83% of cases, although some patients complained of abnormal vision, metamorphopsia, and blurred vision.

In this study the preoperative visual field tests showed a decrease in the retinal differential light threshold across the entire posterior pole. This suggests a substantial functional alteration of the retina, underlying the epiretinal membrane. The elevation of the macula and the retinal distortion, due to the hypocellular contraction of the epiretinal membrane, as well as the macular edema, may explain the functional alteration of the retina.

Removal of the epiretinal membrane might have caused damage to either of the inner retinal layers or the photoreceptors. The traction release on the inner surface of the retina may reduce distortion of the photoreceptors, leaving retinal ganglion cell activity mostly unchanged.

A possible toxic effect of ICG staining on the proteins of the inner retinal layers (the axonal layer) could lead to a significant decrease of sensitivity. From our preliminary data, there were no statistically significant modifications before or after surgery of MD, MS, or PSD in patients affected by macular pucker or diabetic tractional macular edema.

During ILM peeling, in most cases, it was possible to observe widening of the

Visual field changes after pars plana vitrectomy

381

Fig. 1a. Seventy-year-old female suffering from a macular pucker in the left eye. Preoperative VA: 0.5. Date of surgery: October 11th, 2001. Final VA: 1. The first visual field was performed the day before surgery. Significant improvement of the MS in the central area was seen during follow-up.

382

F. Morescalchi et al.

Fig. 1b. Photograms showing the posterior pole before and three months after ILM peeling.

denuded retinal area as well as some small hemorrhages along the retinal fibers. This mechanical stress could be responsible for the decrease of central retinal function during the first month. Recovery of MS was often noted after the first month, together with improvement in visual acuity and reading speed. This corresponded to amelioration of the discriminative ability of the eye. The decrease of retinal distortion and the progressive restoration of the intraretinal neural network after the resolution of macular edema, together with retinal reattachment, may account for the slight improvement of the macular threshold (Figs.1a and b). However, even after the release of the epimacular membrane, some degree of retinal dysfunction may persist. On the other hand, surgery for the treatment of epiretinal membranes may lead to unintentional

Visual field changes after pars plana vitrectomy

383

injury of the underlying retina. This often depends on the degree of adherence of the epiretinal membrane.

In two cases of macular pucker (11%), we discovered an absolute visual field defect postoperatively. Traction during the epiretinal membrane or ILM peeling could lead to retinoschisis or to accidental interruption of the intraretinal neural network. In these two cases, adhesion of the epiretinal membrane was very strong, even when care was taken to minimize foveal traction during peeling. Additional care is needed when working near the optic disc where the axonal fibers are more crowded and a small injury could lead to significant damage.

Some considerations should be given to the use of ICG dye in patients with macular hole. While our sample size was too small to come to any definite conclusions, we did not record any significant improvement of macular function in 66% of our patients. A possible explanation for this could be that the preoperative visual acuity was generally poor (mean VA = 0.08).

In some cases, we noticed pigmentation under the closed macular hole which may have been due to ICG damaging the pigment epithelium. Other authors have suggested that ICG leads to pigmentary modifications of the fundus.12,13 In our case series, MD worsened in two patients, but on the whole, even if new central visual field defects were evident in some cases, MD worsening was not significant.

The detection of postoperative absolute paracentral visual fields accounts for reports of blurred vision and slow reading speed, despite good postoperative anatomical results and visual acuity improvement. These postoperative paracentral visual field defects have been described previously by some authors using the scanning laser ophthalmoscope in patients operated on for macular holes without the use of ICG staining.15

Conclusions

In macular disease with no full thickness retinal defects, we did not observe any detectable adverse effects from ICG staining. Postoperatively, there was significant improvement in visual acuity and reading speed, with stabilization of MD and PSD. This reflects improvement of the functional activity of the macula. There was no cases of epiretinal membrane relapse. Paracentral visual field defects may occasionally be created by surgical maneuvers which usually did not influence postoperative visual acuity, and which were noticed in 11% of cases with macular traction. Further longterm follow-up investigations are required.

In patients with macular hole, the functional consequences of the use of ICG still remains unclear. Factors that may induce damage to the innermost retina should be suspected and investigated further before recommending the routine use of ICG for staining the ILM.

References

1.Yoon HS, Brooks HL, Capone A, L’Hernault NL and Grossniklaus HE: Ultrastructural features of tissue removed during idiopathic macular hole surgery. Am J Ophthalmol 122:67-75, 1996

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2.Morris R, Kuhn F, Witherspoon CD, Meister V, Dooner J: Hemorragic macular cysts in Terson’s syndrome and its implications for macular surgery. Dev Ophthalmol 44-54, 1997

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5.Olsen T, Sternberg PJ, Capone AJ, Martin D, Grossniklaus H, Aaberg TS: Macular hole surgery using thrombin activated fibrinogen and selective removal of the internal limiting membrane. Retina 18:322-329, 1998

6.Mester V, Kuhn F: Internal limiting membrane removal in the management of full-thickness macular holes. Am J Ophthalmol 129:769-777, 2000

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12.Sippy BD, Engelbrecht NE, Hubbard GB et al: Indocyanine green effect on cultured human retinal pigment epithelial cells: implication for macular hole surgery. Am J Ophthalmol 132:433-435, 2001

13.Gandorfer A, Haritoglou C, Gass AC, Ulbig MW, Kampik A: Indocyanine green-assisted peeling of the internal limiting membrane may cause retinal damage. Am J Ophthalmol 132:431-433, 2001

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16.Melberg NS, Thomas MA: Visual field loss after pars plana vitrectomy with air/fluid exchange. Am J Ophthalmol 120:386-388, 1995

17.Hutton WL, Fuller DG, Snyder WD, Fellman RL, Swanson WH: Visual field defects after macular hole surgery. Am J Ophthalmol 103:2152-2159, 1996

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