Content uploaded by Nicholas P Jones
Author content
All content in this area was uploaded by Nicholas P Jones on Jan 23, 2018
Content may be subject to copyright.
VISUAL OUTCOMES OF PARS PLANA
VITRECTOMY WITH EPIRETINAL
MEMBRANE PEEL IN PATIENTS
WITH UVEITIS
RAJEEV G. TANAWADE, FRCOPHTH, LOUKIA TSIERKEZOU, MD, MANDEEP S. BINDRA, FRCSED,
NIALL A. PATTON, FRCOPHTH, NICHOLAS P. JONES, FRCOPHTH
Purpose: To report the outcomes of pars plana vitrectomy with epiretinal membrane
(ERM) peel, with or without internal limiting membrane peel, in patients with uveitis.
Methods: Retrospective interventional case series of patients undergoing pars plana
vitrectomy with ERM peel between January 2005 and March 2012. Sixteen consecutive
patients (16 eyes) were identified, with a minimum postoperative follow-up of 6 months.
Visual acuity, anatomical outcomes, perioperative control of inflammation, and complica-
tions were assessed.
Results: The mean age at surgery was 47.3 years (range, 14–68 years), with a mean
duration of ERM at surgery of 21.3 months (3–84 months). At 6 months, visual acuity
improved in 31.25% of eyes, stabilized in 31.25%, and was worse in 37.5%. The causes
of reduced visual acuity postoperatively included severe preexisting macular pathology and
unoperated cataract.
Conclusion: Pars plana vitrectomy with ERM peel in eyes with uveitis may improve or
stabilize visual acuity, especially in eyes with macular traction, but in the absence of
traction, outcomes are variable and unpredictable. Prevention of ERM formation by
aggressive control of inflammation is important.
RETINA 35:736–741, 2015
Macular epiretinal membrane (ERM) formation,
with or without cystoid macular edema (CME),
is a well-recognized sight-threatening complication of
chronic uveitis
1
and causes retinal surface wrinkling,
striate distortion, and visual acuity loss.
2
Evidence for
the role of pars plana vitrectomy (PPV) with ERM
peel in these patients is sparse, with a variable but
often poor outcome being previously reported.
3,4
More
recent studies have, however, shown that surgery in
some forms of uveitis may be beneficial both in
improving visual acuity
5,6
and reducing CME.
1,7,8
We therefore evaluated the visual results, factors
affecting outcomes, and complications in our patients
with uveitis undergoing PPV with ERM peel.
Methods
A retrospective review was undertaken of the
clinical records of all patients with uveitis who had
undergone PPV with ERM peel between January 2005
and March 2012, with a minimum of 6 months
postoperative follow-up. The patients were identified
from the databases of the Manchester Uveitis Clinic
and the Manchester Royal Eye Hospital vitreoretinal
surgical unit. Data on patient characteristics, the
etiology and description of the uveitis, comorbidity
and previous treatment, surgical details, preoperative
medication, postoperative complications, and visual
outcome, were recorded. Postoperatively, the time
taken for the inflammation to return to the preoperative
baseline level was recorded.
In all cases, the indication for surgery was persis-
tently reduced visual acuity associated with ERM with
or without CME. The visual acuity was recorded in
logMAR for 14 of 16 eyes, the remaining 2 being
converted from Snellen to logMAR using an accepted
From the The University of Manchester, Manchester Academic
Health Science Center, Manchester Royal Eye Hospital, Central
Manchester Foundation Trust, Manchester, United Kingdom.
None of the authors have any financial/conflicting interests to
disclose.
Reprint requests: Rajeev G. Tanawade, FRCOphth, Manchester
Royal Eye Hospital, Oxford Road, Manchester M13 9WL, United
Kingdom; e-mail: rgtans@gmail.com
736
technique.
9
Postoperative visual change was defined as
a logMAR visual acuity difference of 0.2 log units
(Snellen equivalent = 2 lines) or greater. Intraocular
inflammation was graded as absent, mild (1+), moder-
ate (2+), or severe (3–4+).
6
Results
Sixteen eyes of 16 consecutive patients undergoing
PPV with ERM peel were identified (7 male, 9 female);
the mean age at surgery was 47.3 years (range, 14–68
years). The mean documented duration of ERM at sur-
gery was 21.3 months (range, 3–84 months). The mean
postoperative follow-up was 18.5 months (range, 6–40
months). The etiology and description of the forms of
uveitis are shown in Table 1. Chronic idiopathic pan-
uveitis was the most common subset.
The preoperative diagnosis of ERM was made by slit-
lamp biomicroscopy, and with optical coherence tomog-
raphyin13eyes.Ofthese13eyes,opticalcoherence
tomography confirmed ERM alone (in 2), ERM with
CME (5), and ERM with vitreomacular traction (VMT)
and CME (6). By 3 months postoperatively, optical
coherence tomography was performed in 9 eyes,
showing resolution of VMT and CME in all.
The preoperative baseline antiinflammatory treat-
ment included oral prednisolone (5–25 mg) in 8 pa-
tients (enhanced perioperatively in 6), mycophenolate
mofetil (4), and azathioprine (3) (Table 2). Topical
prednisolone acetate 1% was administered with
increased frequency (4–6 times daily) in 3 eyes. One
patient received intravenous methylprednisolone 1 g
on the day of surgery. Preoperative anterior chamber
inflammation was absent in 12 eyes, and mild in 4, 2
of which resolved postoperatively within 1 week, 1
resolved at 2 weeks, and another resolved at 44 weeks.
Preoperative vitritis was recorded as absent (in nine
eyes), mild (two), moderate (three), and impossible
to assess owing to posterior capsule opacification
(one). Postoperatively, the vitreous inflammation
cleared at 3 months (in 2 eyes), 11 months (1), and
could not be graded in 2 eyes (silicone oil) with severe
irreversible preexisting pathology (1 macular granu-
loma, 1 longstanding tractional retinal detachment).
In 8 eyes, 20-gauge 3-port PPV was performed, and in
the other 8 eyes, 23-gauge (Table 2). Surgery was
performed by five different consultant surgeons. Mem-
brane peeling was assisted with Brilliant Peel (Geuder
AG, Heidelberg, Germany), Membrane Blue (DORC,
Zuidland, The Netherlands), or Membrane Blue-Dual
(DORC) dye. An ERM peel alone was performed in
eight eyes, but this was combined with internal limiting
membrane (ILM) peel in the other eight eyes; this choice
was made by the individual surgeon, and not according to
a predetermined protocol. Six eyes were noted at the time
of surgery to have a particularly strong adherent posterior
hyaloid. Internal tamponade was achieved with air (in 11
eyes), gas (3), or silicone oil (2). Gas tamponade was
used for iatrogenic retinal breaks and included SF
6
20%, C
2
F
6
18%, and C
2
F
6
20%. Silicone oil (5700CS)
tamponade was used in 1 eye with chronic hypotonous
maculopathy and in 1 eye with tractional retinal detach-
ment and proliferative vitreoretinopathy. Vitrectomy was
combined with phacoemulsification and lens implantation
(in 1 eye); with posterior capsulectomy (1); with cryo-
therapy for iatrogenic retinal breaks (2); with intravitreal
triamcinolone injection 4 mg/0.1 mL (4); and with intra-
vitreal bevacizumab injection 1.25 mg/0.05 mL (2). Six
patients received sustained release oral acetazolamide 250
mg 2 times a day for 3 days postoperatively, including
eyes with gas tamponade (3), silicone oil (1), intravitreal
bevacizumab (1), and 1 eye with chronic CME.
The complications of surgery included iatrogenic
retinal breaks in three eyes that were managed intra-
operatively with no subsequent retinal detachment;
cataract (three); fibrinous uveitis (two) that resolved
with intensive topical treatment; transient hypotony
(one); and transient secondary ocular hypertension
(one). Two of the three eyes with cataract subse-
quently underwent surgery with resultant improvement
in visual acuity. Residual ERM on biomicroscopy was
recorded in two eyes. The postoperative topical
regimen included prednisolone acetate 1% every 2
hours, chloramphenicol 0.5% 4 times a day, and
cyclopentolate 1% 2 times a day. The intraocular
inflammation returned to the preoperative baseline
level by a mean of 5 weeks (range, 1–44 weeks). Four
eyes demonstrated CME postoperatively—two under-
went orbital floor methylprednisolone injection, and
CME resolved in both; one with severe CME
Table 1. Description of the Type and Etiology of
the Uveitis
Chronic panuveitis
Idiopathic 3
Sarcoid-associated 1
Toxoplasmosis 2
Candidiasis 1
Chronic sclerouveitis
Idiopathic 1
Intermediate uveitis
Idiopathic 4
Chronic anterior uveitis
Idiopathic 2
Sarcoid-associated 1
Peripheral granuloma
Toxocariasis 1
Total 16
PPV WITH ERM PEEL IN UVEITIS TANAWADE ET AL 737
Table 2. Patient Descriptors, Surgery Type, Outcomes, and Complications
Case
Age at Surgery
(years), Sex
Uveitis Procedure,
Scleral Port Size
Perioperative Medication (Duration) VA, logMAR Complications
Description Etiology Pre Intra Post Pre Post Intra Post
1 50, F CAU NK PPV/PC/ERM +
ILM 20 G
Pred 5 mg once daily (12 years);
MYC 1.25 mg BID (9 years)
32 —Residual CME, ERM
IVT IVT
(5 months)
2 25, F CPU Candida PPV/ERM + ILM/
cryo 20 G
———34 —Macular scar
3 40, F CPU NK PPV/ERM/SO
20 G
Pred periop; MYC 0.5–1 mg BID (9
months)
1.56 2 —Persistent
hypotonous
maculopathy, SO
in AC
IVT
4 32, F INT NK PPV/ERM 23 G ———0.7 0.22 ——
5 62, F SCL NK PPV/ERM + ILM
23 G
Pred periop; MYC 1 mg BID
(9 months), [1.5 mg BID (1 month
preoperative)
0.8 0.3 ——
IVMP
6 60, M CPU Sarcoid PPV/ERM 23 G Pred periop IVB Diamox 0.6 0.5 —Cataract, transient
hypotony, residual
CME
7 68, F CPU Toxoplasma PPV/phaco/ERM
20 G
——Diamox 3 4 —Persistent tractional
detachment
8 47, M INT NK PPV/ERM 23 G MYC 500 mg BID (4 years), [1g
BID (1 month preoperative)
1.26 1.0 —Fibrinous uveitis
9 14, M CPU Toxocara PPV/ERM 20 G Pred periop 0.34 0.62 —Pigments on ALC,
CME, preexisting
macular dystopia
10 62, F CAU NK PPV/ERM + ILM/
cryo 20 G
——Diamox 0.58 0.9 Retinal
break
Cataract
11 36, F CPU Toxoplasma PPV/ERM 20 G AZA 125 mg/day (15 months);
septrin 960 mg BID (2 weeks
preoperative)
0.18 0.12 Retinal
break
—
Diamox
12 66, F CPU NK PPV/ERM 23 G —IVT Diamox 1.0 1.0 —Lamellar macular
hole, residual ERM
13 55, M INT NK PPV/ERM + ILM
23 G
AZA 50 mg BID (6 months)
IVB
0.62 0.96 —Cataract, residual
ERM, RPE
changes
14 43, M CAU Sarcoid PPV/ERM + ILM
23 G
Pred 10 mg
(5 years)
—Diamox 0.98 0.92 Retinal
break
Macular hole
15 46, M INT NK PPV/ERM + ILM
23 G
Pred periop IVT 1.0 0.5 ——
738 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2015 VOLUME 35 NUMBER 4
underwent intravitreal triamcinolone 2 mg injection
that was unsuccessful; and another resolved in 2
months with no treatment.
Visual improvement was noted in 5 of 16 eyes
(31.25%) at 6 months; of these 5, 3 had also
undergone ILM peel. The visual acuity was unchanged
in 5 of 16 eyes (31.25%) of which 2 had undergone
ILM peel, and it was worse in 6 eyes (37.5%) of which
3 had undergone ILM peel.
The causes of reduced visual acuity (in six eyes)
included severe, irreversible preexisting macular pathol-
ogy (two), one with a post-Candida macular scar and
one with longstanding Toxoplasma-induced tractional
retinal detachment; pigment deposition on anterior lens
capsule with residual CME in an eye with preexisting,
Toxocara-induced severe macular dystopia (one); cata-
ract (two); and persistent hypotonous maculopathy
(one). In those five eyes where visual acuity did not
improve, associated pathology included cataract (in one),
lamellar macular hole (one), surgery-induced macular
hole (one), posterior capsular opacification with residual
CME (one), and possible amblyopia (one). The median
logMAR visual acuities (n = 14) before and 6 months
after surgery were 0.75 and 0.76, respectively (Figure 1),
after excluding 2 eyes with preexisting poor visual acuity
(less than hand motion).
9
One of 2 eyes recorded as
having tangential macular traction showed visual
improvement and the other eye stabilized (Figure 2,
A and B). Of the 6 eyes with preoperative VMT,
the visual acuity improved in 2, was unchanged in 3
(Figure 2, C and D), and reduced in 1 eye.
Discussion
Vitrectomy may be indicated in patients with
uveitis for inflammatory vitreous opacification, vitre-
ous hemorrhage, tractional retinal detachment or
Table 2. (Continued )
Case
Age at Surgery
(years), Sex
Uveitis Procedure,
Scleral Port Size
Perioperative Medication (Duration) VA, logMAR Complications
Description Etiology Pre Intra Post Pre Post Intra Post
16 52, F CPU NK PPV/ERM + ILM
20 G
Pred periop; AZA 75 mg BID
(5 years)
0.3 0.32 —PCO, residual CME
OFMP
(3 months)
AC, anterior chamber; ALC, anterior lens capsule; AZA, azathioprine; BID, 2 times a day; CAU, chronic anterior uveitis; CPU, chronic panuveitis; Cryo, cryotherapy; F, female; INT,
intermediate uveitis; Intra, intraoperative; IVB, intravitreal bevacizumab; IVMP, intravenous methylprednisolone; IVT, intravitreal triamcinolone; M, male; MYC, mycophenolate mofetil;
NK, not known; OFMP, orbital floor methylprednisolone injection; Pre, preoperative; Post, postoperative; PC, posterior capsulectomy; PCO, posterior capsular opacification; Phaco,
phacoemulsification with intraocular lens implantation; Pred, prednisolone; Pred periop, perioperative prednisolone 25 mg, started preoperative, continued 1 week postoperative, later
dose reduced by 5 mg/week; RPE, retinal pigment epithelium; SCL, sclerouveitis; SO, silicone oil; VA, visual acuity.
Fig. 1. Scatter plot of preoperative and postoperative (6 months) log-
MAR visual acuity (n = 14), after excluding 2 eyes with preexisting
poor visual acuity (#hand motion).
9
PPV WITH ERM PEEL IN UVEITIS TANAWADE ET AL 739
rhegmatogenous retinal detachment, persistent CME,
and ERM.
5–7,10–15
The incidence and severity of ERM may relate to
the diagnosis and duration of uveitis, and this has been
reported in pars planitis (30% incidence; 6.5%
severe),
16
Behcet disease (17%),
17
and sarcoidosis
(6%).
18
Vitrectomy with ERM peel in eyes with uve-
itis has been shown to have a poor visual outcome.
4
Epiretinal membrane peel in specific subgroups of
uveitis has more recently been reported with beneficial
effects on both visual acuity and CME: a literature
review of PPV in uveitis examined 44 interventional
case series but reported membrane peeling in only 12.
8
A retrospective series of PPV and ERM peel in sarcoid
uveitis reported a beneficial effect on CME.
1
A similar
series in patients with intermediate uveitis concluded
that it is a safe procedure and may result in improve-
ment of visual acuity.
5
Successful removal of ERMs
has also been reported in Candida chorioretinitis but
the visual results clearly depend on the severity of
macular damage.
19–21
Dev et al
6
reported visual outcomes after PPV for
ERM associated with pars planitis in 7 eyes, with
a visual improvement of 71% at 3 months to 54
months ($3 lines). Kiryu et al
5
reported the results
of PPV with ERM peel in 11 eyes with sarcoid uveitis,
with 7 eyes also undergoing lensectomy. In their
series, a maximum visual improvement of $2 Snellen
lines was noted in 9 of 11 eyes (82%) at 1 month to 12
months but after follow-up ranging from 12 months to
38 months, only 5 eyes (45%) had maintained it.
5
We
report the outcomes of PPV with ERM peel in 16 eyes
with uveitis. In our series, preexisting, severe macular
pathology followed by unoperated cataract were the
causes for reduced visual acuity postoperatively.
Removal of idiopathic ERMs has been analyzed
with or without ILM peel,
22,23
and the efficacy of ILM
removal seems uncertain; one study concluded that
ILM peel should be considered only where the ILM
is so strongly adherent to the ERM that the removal of
the ERM alone is difficult
22
and noted that macular
thickening with loss of the normal foveal contour was
Fig. 2. Ocular coherence tomography in a 60-year-old man with chronic panuveitis (Case 6, Table 2) demonstrating ERM with CME preoperatively
(A) and resolution postoperatively (B) after PPV with ERM peeling, and a 52-year-old woman with chronic panuveitis (Case 16, Table 2) demon-
strating ERM and VMT preoperatively (C) and resolution postoperatively with minimal residual macular edema at 3 months (D) after PPV with
combined ERM–ILM peeling.
740 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2015 VOLUME 35 NUMBER 4
more frequently found, with no functional differences
in the ILM peel group; others in contrast reported no
deleterious effects after ILM peel in eyes with macular
pucker and suggested that ILM peel may remove
a potential scaffold for myofibroblasts and other pro-
liferating cells that would otherwise cause recurrent
macular distortion.
23
Wiechens et al,
14
performing
PPV in intermediate uveitis with CME but without
ERM, found that ILM peel made no difference to out-
come. In our study, there was no demonstrable advan-
tage from combined ERM–ILM peel.
Vitrectomy with ERM peel can improve CME firstly
by removing inflammatory mediators
1,11
and secondly
by reducing retinal traction. In our series, ERM peel
with or without ILM peel demonstrated a resolution
of preoperative VMT and CME in the eyes that under-
went an optical coherence tomography at 3 months.
There are several limitations to our study: it is small
and retrospective, involves several surgeons’results,
and the decision to peel the ILM was not established
by protocol. There were associated media opacities
affecting visual acuity, and the minimum postopera-
tive follow-up was limited to 6 months. The visual
outcomes after ERM peel in eyes with uveitis were
multifactorial and vision improved in only a minority
of eyes. Those with VMT can show clear improve-
ment, whereas those with severe, preexisting macular
pathology are unlikely to benefit from surgery.
Vitrectomy with ERM peel is beneficial in eyes with
uveitis and macular traction with or without CME. In
other eyes, results are disappointing, highlighting the
need for enhanced control of intraocular inflammation
to limit the development of ERM.
Key words: cystoid macular edema, epiretinal
membrane peel, internal limiting membrane peel, ocu-
lar coherence tomography, pars plana vitrectomy, uve-
itis, vitreomacular traction.
References
1. Kiryu J, Kita M, Tanabe T, et al. Pars plana vitrectomy for
cystoid macular edema secondary to sarcoid uveitis. Ophthal-
mology 2001;108:1140–1144.
2. Haivala DR, Parke DW II. Macular epiretinal membranes. In:
Albert DM, Jacobiec FA, eds. Principles and Practice of Oph-
thalmology. 3rd ed. Philadelphia, PA: Elsevier; 2008. Available
at: http://www.expertconsultbook.com. Accessed December 18,
2012.
3. Margherio RR, Cox MS Jr, Trese MT, et al. Removal of epi-
macular membranes. Ophthalmology 1985;92:1075–1083.
4. Verbraeken H. Therapeutic pars plana vitrectomy for chronic
uveitis: a retrospective study of the long-term results. Graefes
Arch Clin Exp Ophthalmol 1996;234:288–293.
5. Kiryu J, Kita M, Tanabe T, et al. Pars plana vitrectomy for
epiretinal membrane associated with sarcoidosis. Jpn J Oph-
thalmol 2003;47:479–483.
6. Dev S, Mieler WF, Pulido JS, et al. Visual outcomes after pars
plana vitrectomy for epiretinal membranes associated with pars
planitis. Ophthalmology 1999;106:1086–1090.
7. Sullu Y, Alotaiby H, Beden U, Erkan D. Pars plana vitrectomy
for ocular complications of Behçet’s disease. Ophthalmic Surg
Lasers Imaging 2005;36:292–297.
8. Becker M, Davis J. Vitrectomy in the treatment of uveitis. Am
J Ophthalmol 2005;140:1096–1105.
9. Holladay JT. Visual acuity measurements. J Cataract Refract
Surg 2004;30:287–290.
10. Mieler WF, Will BR, Lewis H, et al. Vitrectomy in the
management of peripheral uveitis. Ophthalmology 1988;95:
859–864.
11. Diamond JG, Kaplan HJ. Lensectomy and vitrectomy for com-
plicated cataract secondary to uveitis. Arch Ophthalmol 1978;
96:1798–1804.
12. Heiligenhaus A, Bornfeld N, Foerster MH, Wessing A. Long-
term results of pars plana vitrectomy in the management of
complicated uveitis. Br J Ophthalmol 1994;78:549–554.
13. Waters FM, Goodall K, Jones NP, et al. Vitrectomy for vitre-
ous opacification in Fuchs’heterochromic uveitis. Eye (Lond)
2000;14:216–218.
14. Wiechens B, Nölle B, Reichelt JA. Pars-plana vitrectomy in
cystoid macular edema associated with intermediate uveitis.
Graefes Arch Clin Exp Ophthalmol 2001;239:474–481.
15. Tranos P, Scott R, Zambarakji H, et al. The effect of pars plana
vitrectomy on cystoid macular oedema associated with chronic
uveitis: a randomised, controlled pilot study. Br J Ophthalmol
2006;90:1107–1110.
16. Malinowski SM, Pulido JS, Folk JC. Long-term visual out-
come and complications associated with pars planitis. Ophthal-
mology 1993;100:818–825.
17. Tugal-Tutkun I, Onal S, Altan-Yaycioglu R, et al. Uveitis in
Behçet disease: an analysis of 880 patients. Am J Ophthalmol
2004;138:373–380.
18. Levy-Clarke G, Saligan L. Ocular manifestations of sarcoido-
sis. In: Albert DM, Jacobiec FA, eds. Principles and Practice of
Ophthalmology. 3rd ed. Philadelphia, PA: Elsevier; 2008.
Available at: http://www.expertconsultbook.com. Accessed
December 18, 2012.
19. McDonald HR, De Bustros S, Sipperley JO. Vitrectomy for
epiretinal membrane with Candida chorioretinitis. Ophthalmol-
ogy 1990;97:466–469.
20. Naoi N, Sawada A. Effect of vitrectomy on epiretinal mem-
branes after endogenous fungal endophthalmitis. Jpn J Oph-
thalmol 1996;40:434–438.
21. Smiddy WE. Treatment outcomes of endogenous fungal en-
dophthalmitis. Curr Opin Ophthalmol 1998;9:66–70.
22. Lee JW, Kim IT. Outcomes of idiopathic macular epiretinal
membrane removal with and without internal limiting mem-
brane peeling: a comparative study. Jpn J Ophthalmol 2010;
54:129–134.
23. Park DW, Dugel PU, Garda J, et al. Macular pucker removal
with and without internal limiting membrane peeling: pilot
study. Ophthalmology 2003;110:62–64.
PPV WITH ERM PEEL IN UVEITIS TANAWADE ET AL 741
