Trabeculectomy Versus EX-PRESS Shunt Versus

Ahmed Valve Implant: Short-term Effects

on Corneal Endothelial Cells
GIAMBERTO CASINI, PASQUALE LOIUDICE, MARCO PELLEGRINI, ANGELA TINDARA SFRAMELI,
PAOLO MARTINELLI, ANDREA PASSANI, AND MARCO NARDI

PURPOSE:

To evaluate short-term changes in corneal

endothelial cells after trabeculectomy, EX-PRESS device
implantation, and Ahmed valve implantation for the
treatment of primary open-angle glaucoma.

DESIGN: Prospective, interventional, comparative case
series with contralateral eye control study.

METHODS: We prospectively evaluated the changes in
number, density, and shape of the corneal endothelium
cells in 128 eyes of 64 patients divided into 3 groups
depending on the treatment received. Corneal specular
microscopy was performed with a noncontact specular
microscope preoperatively and at 1 and 3 months after
surgery. The changes at each time point were compared
with those of the control group, which consisted of 32
contralateral glaucomatous eyes receiving antiglaucoma
medications without any previous glaucoma surgery.

RESULTS: In the subjects who underwent trabeculectomy, corneal endothelial cell density (ECD) significantly
decreased by 3.5% (P [ .012, paired t test) at 1 month
and 4.2% (P [ .007) at 3 months after surgery,
compared to the baseline values. In the Ahmed valve
group ECD did not change at 1 month after surgery and
had a significant 3.5% decrease at 3 months (P [ .04).
In the patients who underwent EX-PRESS implantation
and in the control group ECD did not change either at
1 month or at 3 months after surgery (P > .05).

CONCLUSIONS: EX-PRESS shunt, compared to trabeculectomy and Ahmed valve, seems to be a safer procedure
regarding the risk of endothelial cell loss. For this reason,
it may be the treatment of choice in patients with significant
low corneal ECD before surgery or other risk factors
for corneal damage. (Am J Ophthalmol 2015;160(6):
11851190. 2015 by Elsevier Inc. All rights reserved.)

LAUCOMA IS A SLOWLY PROGRESSIVE DISEASE

affecting the optic nerve, characterized by degeneration of retinal ganglion cells, loss of the retinal

Accepted for publication Aug 18, 2015.

From the Ophthalmology Unit, Department of Surgical, Medical,
Molecular and Critical Area Pathology, University of Pisa, Pisa, Italy.
Inquiries to Pasquale Loiudice, Dipartimento di Patologia Clinica,
Medica, Molecolare e dellArea Critica Unita` Operativa Oculistica
Universitaria Via Paradisa 2, 56124 Pisa, Italy; e-mail: ldcpasquale@
gmail.com
0002-9394/$36.00
http://dx.doi.org/10.1016/j.ajo.2015.08.022

2015 BY

nerve fiber layer, and thinning of the neuroretinal rim, with

consequent damage to the visual field and vision decline.
It is a leading cause of irreversible blindness worldwide.1
In Europe, glaucoma is the cause of blindness in
10.6%13.5% of cases and is present at the onset of approximately 4% of cases of moderate and severe vision impairment.2 The level of intraocular pressure (IOP), old age,
family history of glaucoma, African-Caribbean ethnicity,
use of topical or systemic corticosteroids, and central
corneal thickness are considered major risk factors,3,4
although optic nerve damage is seen in subjects with
normal IOP (normal-tension glaucoma).5,6
Glaucoma treatment aims to slow the progression of the
disease and preserve visual function without affecting
quality of life. Currently, lowering IOP is the mainstay of
glaucoma treatment. Medical therapy with antiglaucomatous drugs usually represents the first approach. The progression of perimetric damage and uncontrolled IOP, in spite of
maximum tolerated medical therapy and laser trabeculoplasty, are some of the indications for surgical treatment.
Nowadays, filtering surgery is the most frequently used
technique for surgical glaucoma treatment. It comprises
both posterior and anterior approaches, which are divided
into penetrating (ie, trabeculectomy, EX-PRESS device
implant) and nonpenetrating techniques (ie, deep sclerectomy, viscocanalostomy, angular implants).
Trabeculectomy is the most commonly performed glaucoma operation worldwide. Antifibrotic agents, such as
mitomycin C (MMC) and fluorouracil, may be applied
intraoperatively or via perioperative subconjunctival injection to reduce the episcleral proliferative response, which
blocks the aqueous outflow channel.7 Glaucoma drainage
implants are artificial devices inserted surgically into the
anterior chamber (AC) to drain the aqueous toward the
orbital surface of the eye. The Ahmed glaucoma valve is
one of the most commonly used drainage implants. It consists of a silicone tube connected to a silicone sheet valve,
which allows unidirectional liquid flow. The EX-PRESS
shunt is a nonvalved stainless steel tube that is inserted under a partial-thickness scleral flap to connect the AC to the
subconjunctival space.
Although glaucoma surgery has made significant progress in terms of safety, complications are still possible.
We studied the possibility of faster postoperative loss of
corneal endothelial cells, following a filtering procedure.

ELSEVIER INC. ALL

RIGHTS RESERVED.

1185

A decrease in the number of corneal endothelial cells is a

physiological phenomenon due to aging. Cell density
ranges from almost 3000 cells/mm2 in a young adult to
just over 1000 cells/mm2 in patients over 80 years old.
Several risk factors are known to accelerate this loss,
including surgery, antiscarring agents, argon laser iridotomy, and glaucoma itself.816 Corneal decompensation
was reported as a late postoperative complication after
trabeculectomy and tube shunt surgery.17 In long-term
follow-up studies of Ahmed valve implantation, corneal
decompensation has been reported to occur in up to 30%
of patients.18 The aim of this study was to evaluate
short-term changes in corneal endothelial cells after
trabeculectomy, EX-PRESS shunt, and Ahmed glaucoma
valve implantation for the treatment of primary openangle glaucoma (POAG).

METHODS
IN THIS PROSPECTIVE, INTERVENTIONAL, COMPARATIVE

case series with contralateral eye control study, we

enrolled 64 subjects affected by POAG and requiring surgical treatment. The study was retrospectively approved
by the Ethical Review Board of the University of Pisa
(Comitato Etico, Pisa University, Pisa, Italy). A power
analysis was executed using the effect size from the results
of a previous study17 and indicated that 22 patients were
required to detect a 2.6% endothelial cell density
(ECD) decrease with a power of 80% and a significance
level of 0.05.
The patients were divided into 3 groups depending on
the type of glaucoma surgery received. Group 1 included
22 eyes of 22 patients who underwent trabeculectomy,
Group 2 included 24 eyes of 24 patients who underwent
EX-PRESS Glaucoma Filtration Device (Alcon, Fort
Worth, Texas, USA) implantation, and Group 3 included
18 eyes of 18 patients who underwent Ahmed glaucoma
valve (New World Medical, Inc, Rancho Cucamonga,
California, USA) implantation. We also included a
unique control group (32 eyes) to measure the contralateral eyes of subjects with glaucoma who were receiving
antiglaucoma medication without any previous surgery,
except for cataract surgery at least 180 days before enrollment. The choice of the type of treatment for the particular patient was made using agreed guidelines. For those
patients that had received long-term topical therapy for
inflamed conjunctiva and were at higher risk of bleb
fibrosis, the Ahmed valve was preferred. Patients whose
eyes had a wider angle at gonioscopy were assigned to
the EX-PRESS shunt group; otherwise, trabeculectomy
was performed.
Inclusion criteria were perimetric POAG, preoperative
uncontrolled IOP despite maximum tolerated medical
therapy, best-corrected visual acuity (BCVA) equal or
1186

above 24 letters using Early Treatment of Diabetic Retinopathy Study (ETDRS) methodology, and the ability to
return in the 4 months following surgery for scheduled
visits. Exclusion criteria were allergy to medication used
during and after surgery, previous ocular surgery except
for cataract surgery at least 180 days before enrollment,
eyes receiving a topical anhydrase inhibitor, any corneal
disease, presence of an intraocular lens in the anterior
chamber, postoperative complications such as flat anterior
chamber or need to refill the anterior chamber, and
significant comorbid disease that could interfere with the
follow-up.
Baseline data, including age at surgery, sex, type of glaucoma, glaucoma medications, number of previous intraocular surgeries, and lens status, were recorded. All operations
were performed by the same experienced surgeon with a
standard technique after obtaining informed consent.
Before surgery, and 1 month and 3 months after surgery,
a complete ocular examination was performed, including
BCVA (ETDRS optotype), IOP measurement (Goldmann
applanation tonometry), slit-lamp examination, and
corneal specular microscopy on the central area with a
noncontact specular microscope (Tomey EM-3000,
Nagoya, Japan). Noncontact specular microscopy is a standard technique used to assess corneal ECD and
morphology; it has the advantage of being a simple, repeatable, and noninvasive examination.19 Specular microscopy was performed by the same expert physician and
endothelial cell data were based on the average of 3 measurements. The following parameters were analyzed: ECD,
coefficient of variation (CV) of cell area (polymegathism),
hexagonality (pleomorphism), and central corneal thickness (CCT).
Statistical analysis was performed using SPSS software
(SPSS Inc, Chicago, Illinois, USA). Homogeneity of variance was assessed with Levenes test. Paired t tests were
used to compare ECD, polymegathism, pleomorphism,
and CCT before and after surgery. The comparison of
changes in ECD among groups did not fulfill the assumptions of homogeneity of variance, so the Mann-Whitney
U test was used. Differences were considered significant
when P < .05.

RESULTS
SUBJECT CHARACTERISTICS ARE SUMMARIZED IN TABLE 1.

Patient age, sex, lens status, and the number of previous

intraocular surgeries did not differ significantly across the
trabeculectomy, EX-PRESS shunt, Ahmed valve, and control groups.
After surgery with all 3 procedures there was a significant
decrease in IOP and number of antiglaucoma medications.
Conversely, changes in IOP and number of antiglaucoma
medications were not significant in the control group

AMERICAN JOURNAL OF OPHTHALMOLOGY

DECEMBER 2015

TABLE 1. Trabeculectomy Versus EX-PRESS Shunt Versus Ahmed Valve Implant and Corneal Endothelial Cells: Demographic
Characteristics of Patients Enrolled in the Study

Number of eyes
Mean age 6 SD (y)
Sex (male/female)
Lens status, no. eyes (%)
Phakia
Aphakia or pseudophakia
No. of past intraocular surgeries, mean 6 SD

Trabeculectomy

EX-PRESS

Ahmed

Control

22
64.6 6 9.3
12/10

24
63.6 6 7.5
15/9

18
69.2 6 8.4
7/11

32
66.4 6 7.7
18/14

14 (63.6)
8 (36.4)
0.8 6 0.9

14 (58.3)
10 (41.7)
0.7 6 0.7

11 (61.1)
7 (38.9)
0.9 6 0.7

22 (68.7)
10 (31.3)
0.6 6 0.5

.150a
.490b
.873b

.368a

One-way analysis of variance.

x test.

b 2

TABLE 2. Intraocular Pressure (mm Hg) and Number of Antiglaucoma Medications Before and After Trabeculectomy, EX-PRESS
Shunt, and Ahmed Valve Implantation
Trabeculectomy (n 22)
Time of Examination

Baseline
1 month
3 months

EX-PRESS (n 24)

Ahmed (n 18)

Control (n 32)

IOP (mm Hg)

Eye Drops

IOP (mm Hg)

Eye Drops

IOP (mm Hg)

Eye Drops

IOP (mm Hg)

Eye Drops

26.6 6 3.4
19.9 6 3.5a
20.3 6 4.0a

3.0 6 0.7
1.5 6 1.1a
1.3 6 0.9a

26.5 6 4.5
19.4 6 4.2a
20.0 6 3.0a

3.1 6 0.8
1.3 6 1.0a
1.3 6 0.9a

27.7 6 3.2
18.9 6 3.9a
19.5 6 3.5a

3.2 6 0.7
1.2 6 0.9a
1.0 6 0.9a

19.9 6 2.6
19.4 6 3.2
19.5 6 2.8

2.7 6 0.8
2.6 6 0.9
2.6 6 0.8

Data are presented as mean 6 standard deviation.

P < .05 compared with baseline (paired t test).

TABLE 3. Endothelial Cell Count (Cells/mm2) Before and

After Trabeculectomy, EX-PRESS Shunt, and Ahmed Valve
Implantation
Time of
Trabeculectomy
Examination
(n 22)

EX-PRESS
(n 24)

Ahmed
(n 18)

Control
(n 32)

Baseline
2277 6 426 2329 6 220 2273 6 195 2219 6 205
1 month
2173 6 286 2314 6 147 2240 6 168 2231 6 112
3.5
0.2
1.4
0.5
%a
.012
.509
.020
.132
P valueb
3 months 2160 6 291 2298 6 170 2186 6 137 2219 6 184
%a
4.2
0.3
3.5
0
.007
.280
.043
.919
P valuec
Data are presented as mean 6 standard deviation.
Percentage decrease in cell number from baseline.
b
Paired t test comparing cell number at 1 month with baseline.
c
Paired t test comparing cell number at 3 months with baseline.
a

(Table 2). Performing a Pearson correlation, we did not find

any correlation between preoperative IOP and ECD decrease
after surgery (Group 1 P .091; Group 2 P .972; Group 3
P .435), nor did we find a correlation between preoperative
number of medications and ECD decrease (Group 1
P .846; Group 2 P .566; Group 3 P .959).
VOL. 160, NO. 6

Among subjects who underwent trabeculectomy,

corneal ECD was significantly decreased by 3.5% 1 month
after surgery (P .012, paired t test) compared to baseline
values; 3 months after surgery ECD was significantly
decreased by 4.2% (P .007). Among subjects who underwent Ahmed valve implantation, ECD decreased by 1.4%
(P .020) 1 month after surgery and by 3.5% 3 months after surgery (P .043). Among patients who underwent EXPRESS implantation and in the control group, ECD did not
change either 1 month or 3 months after surgery (P > .05)
(Table 3).
A comparison of changes in ECD between groups
revealed that at 1 month the trabeculectomy group had
an ECD decrease that was significantly different from the
control group (P < .05, Mann-Whitney U test); the ECD
changes among the EX-PRESS shunt, Ahmed valve, and
control group were not significantly different at 1 month.
At 3 months, the ECD changes in the trabeculectomy
and Ahmed valve groups were significantly different from
the control group (P < .05). In contrast, there were no significant differences between the EX-PRESS shunt and control groups (Table 4). Morphologic evaluation of corneal
endothelial cells using coefficient of cell size variation
(polymegathism) and hexagonality (pleomorphism)
revealed no significant changes from baseline in any of
the groups (P > .05).

GLAUCOMA SURGERY EFFECTS ON CORNEAL ENDOTHELIAL CELLS

1187

TABLE 4. Mean Change in Endothelial Cell Count (Cells/mm2) After Trabeculectomy, EX-PRESS Shunt, and Ahmed Valve Implantation
Comparison

Trabeculectomy (n 22)

EX-PRESS (n 24)

Ahmed (n 18)

Control (n 32)

Baseline vs 1 month
Pa
Baseline vs 3 months
Pa

103 (3.5%) 6 156

<.000
116 (4.2%) 6 161
.004

5 (0.2%) 6 94
.759
16 (0.3%) 6 140
.753

33 (1.4%) 6 55
.322
87 (3.5%) 6 109
.053

11 (0.5%) 6 43
1 (0%) 6 48

Data are presented as mean (%) 6 standard deviation.

Compared with control group (Mann-Whitney U test).

DISCUSSION
THE CORNEAL ENDOTHELIUM WORKS AS A CELLULAR PUMP

regulating hydric and ionic movement between the cornea

and its environment. A functioning endothelium is essential for corneal integrity and transparency.20 Corneal ECD
decreases with age, at a normal rate of 0.6% per year.21 Any
corneal trauma, such as surgery, is likely to disrupt the
normal morphologic pattern and to accelerate the physiologic loss of this monocellular layer, which has no replication properties in humans.22,23
Trabeculectomy, EX-PRESS device implant, and
Ahmed valve implant are penetrating techniques that
involve the temporary opening of the anterior chamber.
In the last 2 cases, biocompatible materials (the inner
part of the device or the tube of the valve) are introduced
into the anterior chamber. The exact effects of these techniques on the homeostasis of the eye and, in particular, on
corneal endothelial cells are unknown.
In the current study, we found a significant decrease in
corneal ECD after trabeculectomy and after Ahmed valve
implantation, in agreement with the results of previous
studies.17,24 By contrast, in the case of EX-PRESS shunt implantation, we observed that none of the endothelial cell
parameters changed after 1 month or 3 months. The EXPRESS shunt was more recently introduced into clinical
practice than the other procedures, and to our knowledge,
no previous study has examined the changes in endothelium associated with its implantation.
In a 2-year prospective study evaluating corneal endothelium changes after Ahmed valve placement, Lee and associates24 reported a significant ECD decrease compared to
baseline at 1 month (4.6%) and further decreases of 8.6%,
12.6%, and 15.4% at 6, 12, and 24 months, respectively.
Similarly, trabeculectomy is known to decrease corneal
ECD. Storr-Paulsen and associates25 compared ECD after
MMC-augmented trabeculectomy and reported a 9.5%
decrease at 3 months and a 10% decrease at 12 months.
Arnavielle and associates17 reported similar results in a
study of ECD after trabeculectomy without the use of
MMC (7% decrease at 3 months, 9.6% at 12 months).
Low preoperative cell density, peripheral anterior synechiae, intraocular inflammation, and the distance from
1188

the tip of the tube to the cornea are risk factors for postoperative decreased corneal ECD and might be used as predictors of the potential risk of corneal decompensation.26,27
Several hypotheses have been formulated to explain the
decreased endothelial cell density after glaucoma implant
surgery. One states that damage is due to jets of aqueous humor fluid through the silicone tube caused by the heartbeat.
Since the jet flow is fastest near the silicone tube, endothelial cells closer to the tube may be particularly affected.28
The Ahmed valve could also cause chronic inflammation
in the anterior chamber owing to a foreign body reaction
to the silicone tube.28 A study in rabbits showed that
chronic inflammation caused the release of prostaglandins,
which increased corneal endothelial permeability and
caused a reduction in corneal ECD.29 Another possibility
is that drainage devices increase the mechanical loss of
corneal endothelial cells by transient tubeendothelial
cell contact when the patient blinks or rubs the eye.18
The exact mechanism for endothelial cell loss after trabeculectomy is also not fully understood and is probably multifactorial. MMC demonstrated a toxic effect on corneal
endothelium15; the exposure of human donor corneas to
MMC resulted in endothelial damage and rapid sustained
corneal swelling.30 This effect may depend on the presence
of MMC-generated alkylating agents that interfere with periodic DNA repair of corneal endothelial cells. However, a
decrease in ECD was also observed in studies of trabeculectomy without the use of MMC,17 indicating that other factors contribute to the endothelial damage. Other proposed
mechanisms ascribed damage to glaucoma medication and
preservative toxicity, contact between cornea and iris or
lens during or after surgery in cases with shallow ACs, and
protracted high preoperative IOP, which can directly
compress corneal endothelial cells and cause hypoxic damage owing to impaired aqueous humor flow.8,18,28,31
Even if the changes in the ECD observed in this study
were mild, we know that corneal decompensation is not uncommon after glaucoma surgery. The clinical impact of cell
loss is correlated with preoperative ECD. Patients with glaucoma have fewer endothelial cells.8 Age, previous cataract
surgery, and the presence of corneal dystrophies may also
contribute to low corneal ECD before surgery, increasing
the risk of corneal decompensation. Risk factors for greater

AMERICAN JOURNAL OF OPHTHALMOLOGY

DECEMBER 2015

endothelial damage are a flat anterior chamber after surgery,

the presence of peripheral anterior synechiae, and the distance from the tip of the tube to the cornea.26,27 To
ensure a fair comparison of results after the different
procedures, we decided to exclude patients with flat
anterior chambers after surgery or with risk factors for
lower ECD before surgery (such as previous eye surgery
and any corneal disease). This may explain why the ECD
decrease observed is lower than others reported in literature.
The clinical impact of a small decrease in ECD is not
clear. In our study, there was no significant change in the
CV of cell area, hexagonality, or corneal central thickness.
This may be due to the slight effect that the surgical procedures investigated in this paper had on corneal endothelial
cells. Furthermore, the current study employed short-term
monitoring, and other effects may appear later. In addition,
other similar studies24 found no change in pleomorphism or
polymegathism. In our research, patients in the trabeculectomy group exhibited decreased ECD that occurred early
after surgery and did not change at 3 months. These results
are consistent with other studies.25 By contrast, the Ahmed
valve group had a more progressive endothelial cell loss. It
is reasonable to suppose that the corneal ECD loss observed
in the Ahmed valve group at 3 months would increase
further, since in similar studies on Ahmed valve implantation with a longer follow-up, the ECD decreased progressively for up to 2 years.24 These data reinforce the
hypothesis that the risk of endothelial damage after Ahmed
valve implantation is ongoing because of the persistence of
the tube within the AC and the direct connection between
the chamber and the extraocular space. Conversely, causes
of endothelial damage after trabeculectomy (such as MMC,
flat AC, or acute inflammation) are likely to occur during
surgery or shortly thereafter, without a prolonged effect
on the corneal endothelium.
The observed differences in the effects of the EX-PRESS
shunt group compared to the Ahmed valve group and the
trabeculectomy group may be attributed to the different
level of invasiveness of the techniques. Although the EXPRESS shunt is a foreign body in the anterior chamber, if

compared to the Ahmed valve it has a smaller size and is

made of steel instead of silicone; this may result in less
corneal contact and lower chronic inflammation in the
AC. Furthermore, surgical implantation of the EXPRESS shunt involves a mini traumatic procedure that
does not require a large opening of the trabecular meshwork
or an iridectomy, as happens in trabeculectomy. This may
reduce operative time and postoperative inflammation.
The clinical impact of a small decrease in ECD is not clear.
In our study there was no significant change in the coefficient of cell area, in hexagonality or in CCT. This may
be due to the slight effect of the surgical procedures treated
in this paper on the corneal endothelial cells. Furthermore,
this is a short-term monitoring, and other effects may
appear later. In addition, other similar studies24 also found
no change in pleomorphism or polymegathism.
In conclusion, the EX-PRESS shunt procedure compared
to trabeculectomy and Ahmed valves showed no shortterm effects on corneal endothelial cell in patients affected
by POAG. For this reason, it may be the treatment of
choice in patients with significant low corneal ECD before
surgery or other risk factors for corneal damage. On the
other hand, this population of patients may benefit from
a tube shunt, as trabeculectomy and EX-PRESS shunts
are more likely to fail after corneal surgery. In our study,
none of the patients showed signs or symptoms attributable
to corneal disease at the baseline visit. All patients enrolled
in the study had an endothelial cell count equal to or
greater than 2000 cells/mm2, so, in our opinion, no concern
about future corneal surgery was necessary. The main limitation of this study is the small number of subjects
involved. The conclusions drawn from it are also based
on a short follow-up and for this reason they should be
interpreted with caution; studies with longer follow-up
are required to confirm the long-term safety of the EXPRESS device. However, this is the first study that has
compared endothelial changes after trabeculectomy, EXPRESS shunt, and Ahmed valve implantation, and it can
therefore serve as a starting point for further prospective
research.

FUNDING/SUPPORT: NO FUNDING OR GRANT SUPPORT. FINANCIAL DISCLOSURES: THE FOLLOWING AUTHORS HAVE NO
financial disclosures: Giamberto Casini, Pasquale Loiudice, Marco Pellegrini, Angela Tindara Sframeli, Paolo Martinelli, Andrea Passani, and Marco
Nardi. All authors attest that they meet the current ICMJE criteria for authorship.
The authors thank Dr Timothy Albert (Optometrist, Ophthalmology Unit, Department of Surgical, Medical, Molecular and Critical Area Pathology,
University of Pisa, Pisa, Italy) for English revision. Additional English professional assistance has been performed by Aimee Emeriau (Department of
Philology, Literature and Linguistics, University of Pisa, Pisa, Italy).

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AMERICAN JOURNAL OF OPHTHALMOLOGY

DECEMBER 2015

Biosketch
Dr Giamberto Casini received his medical degree from Pisa University in Italy where he also completed his residency. Later
he obtained a master in ophthalmoplasic surgery in Policlinico Universitario Agostino Gemelli, Rome, Italy. Nowadays
Dr Casini serves as consultant at the Ophthalmology Unit of the University Hospital of Pisa, Italy. His professional
interests applies mainly to the vitreo-retinal surgery as well as to glaucomas medical and surgical treatment.

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