O R I G I N A L A R T I C L E

Exfoliation Syndrome as a Risk Factorfor Corneal Endothelial Cell Lossin Cataract Surgery

KULDAR KALJURAND, MD,

PAIT TEESALU, MD, PhD A B S T R A C T

Purpose. To compare the influence of various cataractsurgery pre-, intra-, and postoperative characteristics tocornea endothelium and thickness in patients with andwithout exfoliation syndrome (PEX). Methods. In this pro-spective study 27 consecutive patients with and 26 patientswithout PEX as a control group scheduled for cataract sur-gery were studied. The corneal endothelial cells wereevaluated preoperatively and postoperatively at 1 day and1 month after surgery using noncontact specular micros-copy. Intraoperative parameters of operation time, phaco-emulsification (phaco) time, phaco power and amount ofbalanced salt solution (BSS) were recorded. The effects ofage, axial length, anterior chamber depth (ACD), and lensthickness were evaluated. Results. There were no signifi-cant preoperative differences in endothelium morphologybetween the two groups. The mean endothelial cell loss1 month after surgery was 18.1% in the PEX group and 11.6%in the control group (p = 0.06). Phaco time and used BSSvalues were significantly higher in patients with PEX but hadno significant influence on endothelial cell loss. In regressionanalysis phaco power (p = 0.02) and age (p = 0.004) had asignificant influence on endothelial cell loss. PEX in inter-action with overall phaco impact had a negative influence onendothelial cell loss (p = 0.05). Conclusions. PEX as a maineffect was not found to have a negative influence on endo-thelial cell loss. However, PEX in cases of high phaco impactsignificantly increases the risk of endothelial cell loss.

INTRODUCTION

The corneal endothelium is essential for maintenance

of normal corneal hydration. It consists of a mono-

layer of hexagonal cells, the density of which is

highest at birth and declines linearly with age (1,2).

This layer is highly vulnerable and has limited

regenerative capacity (3). Dysfunction of endothe-

lium results in corneal decompensation and decreased

vision. Exfoliation syndrome (PEX) is characterized

by the development of white, dundruff-like flakes

throughout the anterior ocular segments. It is well

known that the presence of PEX increases the

R E P R I N T SKuldar Kaljurand, MD, Department of Ophthalmology, University of Tartu,

J. Kuperjanovi 1, 51003, Tartu, Estonia. E-mail: kuldar.kaljurand@kliinikum.ee.

Drs. Kaljurand and Teesalu are from the Department of Ophthalmology,

University of Tartu, Tartu, Estonia.

The authors have stated that they do not have a significant financial interest or

other relationship with any product manufacturer or provider of services dis-

cussed in this article. The authors do not discuss the use of off-label products,

which includes unlabeled, unapproved, or investigative products or devices.

The authors have no financial or proprietary interest in any material or method

mentioned.

Submitted for publication: 5/8/07. Accepted: 6/29/07.

Annals of Ophthalmology, vol. 39, no. 4, Winter 2007

� Copyright 2007 by ASCO

All rights of any nature whatsoever reserved.

1530-4086/07/39:327–333/$30.00. ISSN 1558-9951 (Online)

ANN OPHTHALMOL. 2007;39 (4) ..............................................327

incidence of intraoperative and postoperative com-

plications in cataract surgery (4–6). Although cata-

ract surgery in the long run decreases intraocular

pressure, the transient pressure peaks occurring in the

early postoperative period are more common in eyes

with exfoliation (7). Insufficient mydriasis and

weakened attachments of the zonular fibers to the

ciliary body predisposes these eyes to surgical com-

plications, with a five- to tenfold increase in the rate

of zonular breaks, capsular dialysis, or vitreous loss

(8–10). Fortunately only a minority of eyes with PEX

syndrome develop the aforementioned severe com-

plications, which lead to significant loss of corneal

endothelial cells. Wirbelauer et al. (11) found that

uncomplicated cataract surgery induces similar

endothelial cell changes in patients with PEX com-

pared with age-matched controls. However, there is

no agreement between studies if unoperated eyes with

PEX compared with no exfoliation have quantitative

or qualitative morphological changes in corneal

endothelium (11,12). Various preoperative factors

such as anterior chamber depth (ACD), axial length,

and age have been proposed to influence the severity

of endothelium damage (13–15). These various pre-

operative factors might have unequal power of sig-

nificance in patients with and without PEX in

interaction with intra- and postoperative factors. The

aim of this study was to evaluate the influence of

various cataract surgery pre-, intra-, and postopera-

tive characteristics on cornea endothelium and

thickness in patients with and without PEX.

PATIENTS AND METHODS

Thirty-seven consecutive patients scheduled for cata-

ract surgery (between March 2004 and December

2004) with PEX and 37 consecutive patients without

PEX as a control group (nonPEX) underwent pre-

operative ophthalmological examination, including

anterior segment biomicrosopy, binocular ophthal-

moscopy, and Goldmann applanation tonometry.

Previous ocular surgery, ocular trauma, high myopia,

history of uveitis, and abnormalities of the cornea

were exclusion criteria for the study. Patients with

mature cataract were not included in the study.

Nineteen patients with postoperative corneal oedema,

eight from the PEX and 11 from the nonPEX group,

were not included because of difficulties in endothelial

cell counting on the first postoperative day. Two pa-

tients from the PEX group with an endocapsular

ring placement were not included because this surgi-

cal maneuver might cause additional damage to

endothelium. None of the patients were contact-lens

wearers in their lifetime. All patients gave informed

consent, which was in accordance with the ethical

standards laid down in the Declaration of Helsinki.

The diagnosis of PEX was made after pupil dila-

tation with 1% cyclopentolate and 10% phenylephrine

hydrochloride. Exfoliative material was defined as

typical white-greyish material on the anterior surface

of the lens, on the corneal endothelium, and at the

pupil margin. The axial length, ACD, and lens

thickness were measured preoperatively by ultraso-

nography (Humphrey A/B scan system 837). Kera-

tometry was performed using an OAP211

keratometer (Carl Zeiss). Corneal endothelial cells

were photographed and corneal thickness was mea-

sured using an automatic noncontact specular

microscope (Topcon SP2000P). This device provides

rapid morphometric analysis and has reliable repro-

ducibility (16,17). Corneal endothelial cell density

(ECD), average cell area, and the coefficient of vari-

ation (CV) were recorded in the center of the cornea

and in four paracentral locations. The latter positions

were placed in the superior, inferior, temporal, and

nasal quadrants in a 6-mm-diameter circle, each po-

sition 3 mm from the center of the cornea. To

determine the endothelial cell density, the endothelial

cells were counted in a rectangular frame placed

manually with constant (0.1� 0.1 mm) area. Exam-

inations were made preoperatively, on the first post-

operative day and 4 weeks after surgery by the same

examiner (KK). The 4-week follow-up period was

considered to be sufficient because there are several

investigations suggesting that damage of corneal

endothelial cell is detectable already in the first post-

operative month (11,14,18,19).

All patients underwent phacoemulsification with-

out complications through a self-sealing limbal tunnel

incision. All operations were made using the same

phaco equipment (Protege, Storz Ophtahlmics) by

one experienced surgeon (PT). Topical anesthesia

with 2% oxubrucaine eye drops (Alcain, Alcon) and

the temporal approach was used in all cases. After the

circular continuous capsulorhexis (CCC) phacoe-

mulsification inside the capsular bag was performed.

After initial groove formation into the nucleus, the

chopping technique was used. Before CCC and

intraocular lens (IOL) implantation the viscoelastic

substance (Celoftal�, Alcon) was injected into the eye.

The wound was enlarged to 5 mm before the

implantation of the IOL (Bausch & Lomb, model

EZE-50). At the end of the operation the viscoelastic

material was removed from the anterior chamber as

ANN OPHTHALMOL. 2007;39 (4) ..............................................328

well as from behind the IOL. Postoperatively dexa-

methazone with chloramphenicol (Oftan DexaChl-

ora, Santen) drops were used five times daily for

3 weeks, and thereafter three times daily for 2 weeks.

Evaluated intraoperative factors were overall

operation time, elapsed phaco time, phaco power,

overall phaco impact (phaco time multiplied by phaco

power), and volume of balanced salt solution (BSS)

(Bausch & Lomb).

Statistics were performed using Student t-tests and

regression analysis. All data was analyzed using the

SAS software package (release 6.12, SAS Institute Inc.)

RESULTS

Mean patient age in the PEX group was 73 (range 51–

85) years ± 8.3 (SD) and in the nonPEX group was

68.1 (range 43–84) years ±8.0 (SD), (p = 0.02). Pre-

and postoperative visual acuities and the types of cat-

aract were similarly divided. Differences between the

two groups in mean axial length, ACD, lens thickness,

and keratometry were not significant. Pupil mean size

before dilatation and 24 hours after operation was

smaller in the PEX group, but not statistically signifi-

cantly so. Preoperative intraocular pressure (IOP) was

within the same range in both groups, but variability

was higher in the PEX group (Table 1). On the first

postoperative day IOP was higher in PEX group but

the difference between the groups did not reach sta-

tistical significance (24.8±11.7 vs. 19.7±6.0 mmHg,

p = 0.07), (Table 1). In regression analysis the pre-

and postoperative (24 hour) IOP, as the main effect,

did not influence central ECD (p = 0.9, p = 0.6 resp;

r2 = 0.47).

The mean preoperative ECD values, average cell

size, and thickness of cornea did not differ signifi-

cantly between the PEX and nonPEX groups (Ta-

ble 2). The mean preoperative corneal central ECD

was 2543 (±417) in the PEX group and 2594 (±519)

in the nonPEX group. The mean paracentral ECD

was 2479 (±422) in the PEX group and 2455± (475)

in the nonPEX group. Preoperative mean central

ECD values were higher than paracentral cell counts,

2.5% and 5.4%, respectively, in the PEX group and

nonPEX group.

We found a statistically significant difference in

paracentral but not central endothelial cell loss in the

first postoperative day between the PEX and nonPEX

groups (Table 2). The decrease of the central ECD

was 9.8% (p = 0.04) in the PEX group and 9.5%

(p = 0.04) in the nonPEX group. The decrease of the

paracentral ECD was 8.2% (p<0.001) in the PEX

group and 1.1% (p = 0.4) in the nonPEX group.

One month after the operation the cornea was more

affected centrally as well as paracentrally in the PEX

group than in the nonPEX group (Table 2). The

TABLE 1

Pre- and Postoperative Variables

Variable PEX group nonPEX group p

Age, years 73.5 (±8.3) 68.1 (±8.0) 0.02

Sex, F:M 19:8 20:6

Pupil, preop ø (mm) 3.6 (±0.6) 3.9 (±0.7) 0.1

Pupil, postop ø (mm) 4.8 (±0.9) 5.0 (±0.9) 0.4

IOP, preop, mmHg 17.6 (±4.5) 16.7 (±2.7) 0.4

IOP, postop (24 hour) 24.8 (±11.7) 19.7 (±6.0) 0.07

IOP, postop (1 month) 16.5 (±3.4) 17.3 (±5.4) 0.6

ACD, mm 2.98 (±0.4) 2.98 (±0.4) 0.9

Lens thickness, mm 4.4 (±0.6) 4.3 (±0.6) 0.7

Axial length, mm 23.2 (±0.7) 23.4 (±1.2) 0.5

Keratometry K1 43.5 (±1.6) K1 43.3 (±1.2) 0.7

K2 43.8 (±1.3) K2 43.1 (±1.3) 0.09

IOP = intraocular pressure.

ACD = anterior chamber depth.

ANN OPHTHALMOL. 2007;39 (4) ..............................................329

TA

BLE

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s

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Pre

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nonP

EX

pP

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PE

XP

osto

p24

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EX

pP

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p1

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PE

XP

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p1

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EX

p

ECD

±SD

(cell/mm

2)

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2543±

417

2594±

519

0.7

2293

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438

2347

�±

449

0.9

2083

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447

2344

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2480±

422

2455±

475

0.7

2246

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2428±

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0.01

2176

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2294

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Averagecellarea±

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(lm

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401±

83

396±

86

0.5

455

�±

102

441

�±

90

0.7

500

�±

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441±

90

0.4

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420±

95

434±

97

0.8

476

�±

156

430±

98

0.02

483

�±

122

454

�±

103

0.06

Coef.ofvariation±

SD

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22.4±

5.7

24.4±

7.6

0.3

25.5

�±

7.3

26.0±

5.8

0.8

24.1±

5.2

23.8±

7.0

0.8

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22.3±

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23.7±

6.6

0.08

25.5

�±

7.1

25.6

�±

7.3

0.9

24.2

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24.3±

5.5

0.9

Cornealthickness±

SD

(mm)

Central

0.515±

0.031

0.520±

0.035

0.6

0.559

�±

0.041

0.553

�±

0.046

0.6

0.519±

0.035

0.523±

0.042

0.7

Paracent

0.515±

0.033

0.524±

0.035

0.6

0.556

�±

0.041

0.556

�±

0.060

0.9

0.520±

0.036

0.527±

0.038

0.2

EC

D=

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elia

lcell

density.

SD

=sta

ndard

devia

tion.

para

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al.

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5,

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op

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�p

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5,

pre

op

vs.

posto

p1

month

.

ANN OPHTHALMOL. 2007;39 (4) ..............................................330

decrease of mean central corneal ECD compared with

preoperative values was 18.1% (p<0.001) in the PEX

group and 11.6% (p = 0.08) in the nonPEX group,

but the difference between the two groups had

a statistically weak significance (p = 0.06). The

decrease of mean ECD values in the paracentral part

had the same tendency but was less weaker (12.3% in

the PEX and 6.6% in the nonPEX group) and was not

statistically significant.

The average cell area was similar in the two groups

preoperatively, but was more increased in the PEX

group than in the nonPEX group 1 month after sur-

gery. The average increase in cell area was 99 lm2

centrally and 63 lm2 paracentrally in the PEX group

and 45 and 20 lm2, respectively, in the nonPEX

group (Table 2). In our study no preoperative dif-

ferences were found between the two groups in the

coefficients of variation (standard deviation/average

cell size� 100). The postoperative (24 hour) increase

of CV indicated a temporary heterogeneity of cell size

after surgery that returned near to the baseline value

during 1 month (Table 2). Corneal thickness did not

differ significantly between the two groups preoper-

atively. On the first postoperative day the thickness of

the central as well as the paracentral cornea was sig-

nificantly increased in both groups, indicating oede-

ma. The thickness of the cornea had returned to the

preoperative state 1 month after the operation

(Table 2).

Operation parameters are provided in Table 3.

Although the PEX group showed longer operation

time and more phaco power than the nonPEX group,

the difference between the two groups was not

statistically significant. Also the difference in overall

phaco impact between the two groups was not sig-

nificant. Consumption of BSS and phaco time showed

significant differences between the groups (p = 0.001

and p = 0.05, respectively).

In regression analysis the consumption of BSS and

phaco time variables did not have a statistically sig-

nificant influence on ECD 1 month after surgery.

Regression analysis revealed that phaco power had a

significant negative impact on ECD (centrally

r2 = 0.47, p = 0.02; paracentrally r2 = 0.39,

p<0.001). PEX as the main effect or in interaction

with phaco power did not have an influence on

endothelial cell loss (p = 0.2). There was also a sig-

nificant influence of overall phaco impact on overall

ECD (central + 4 paracentral) decline (r2 = 0.30,

p = 0.02). PEX in interaction with overall phaco

impact had a significant influence on endothelial cell

loss (r2 = 0.27, p = 0.05).

A statistically significant negative association be-

tween the age of patients and the postoperative cen-

tral as well as overall ECD 1 month after surgery was

found in regression analysis in this study (r2 = 0.47,

p = 0.004 and r2 = 0.45, p = 0.004, respectively).

Presence of PEX did not have an impact on ECD in

interaction with age (p = 0.7).

Between the preoperative ECD and the change in

ECD there was also a statistically significant negative

association in regression analysis, indicating that, the

larger the preoperative cell density, the larger the

postoperative cell loss (r = 0.45, p<0.001). PEX did

not have influence to postoperative ECD in interac-

tion with preoperative ECD (p = 0.5).

TABLE 3

Operation Parameters of the Study Groups

Variable PEX group (±SD) nonPEX group (±SD) p

Oper. time, minutes 12.4 (±4.3) 11.1 (±2.9) 0.2

Phaco power, % 44.0 (±13.2) 41.0 (±16.6) 0.5

Phaco time, seconds 92 (±44) 71 (±32) 0.05

Overall phaco impact 25.96 20.8 0.2

BSS, mm 26.8 (±7.1) 19.8 (±7.5) 0.001

PEX = patients with exfoliation.

nonPEX = patients without exfoliation.

BSS = balanced salt solution.

Overall phaco impact = phaco power multiplied by phaco time.

ANN OPHTHALMOL. 2007;39 (4) ..............................................331

DISCUSSION

Exfoliation syndrome is a common clinical feature in

patients with cataract (20,21). Because of insufficient

mydriasis and zonular weakness patients with PEX

are more susceptible to intraoperative complications

(4,9). It is also assumed that patients with PEX are

more susceptible to endothelial decompensation after

intraocular procedures.

Several studies have demonstrated quantitative or

qualitative morphological changes in corneal endo-

thelium in patients with exfoliation syndrome

(11,18,21,22). These studies have reported a reduc-

tion of the central ECD ranging from 10% to 21%. It

has been suggested that corneal endothelium metab-

olism is unsettled in eyes with exfoliation syndrome

inducing a loss of endothelium cells. On the other

hand, Puska et al. (12) did not find quantitative or

qualitative morphological changes in corneal endo-

thelium comparing the cornea in both eyes of patients

with unilateral PEX. They also found that normo-

tensive eyes with PEX had higher values of central

corneal thickness (CCT) and IOP. In contrast, Inoue

(22) found the CCT in PEX eyes to be significantly

thinner than that of the controls. Stefaniotou et al.

(23) in turn found significantly lower cell density and

thicker cornea in the PEX group than in the controls

but there was no difference between the eyes with

PEX and normal fellow eyes. In our study the mean

preoperative ECD as well as corneal thickness values

did not differ significantly between the PEX and

nonPEX groups. No significant differences between

the groups in CCT were found in all stages of this

study. In the first postoperative day a significant in-

crease of CCT was recorded due to corneal edema but

there was no significant difference between the values

of CCT at baseline and after 1 month. Similarly to

many other studies (22,24) we did not find a corre-

lation in the regression analysis between endothelial

cell loss and CCT.

Several studies have found that corneal endothelial

cells have decreased cell density, an increased CV of

cell area, and a decreased percentage of hexagonal

cells with increasing age (1,22). Age has also been

found to be an important variable to relevant to ECD

in cataract surgery (13,15). It is well known that the

prevalence of PEX increases with age (4,7,25). In our

study, as in a number of previous investigations

(4,6,7,21), patients with PEX were significantly older

than the controls because of the method of recruit-

ment. To evaluate the influence of aging and PEX to

ECD we performed regression analysis with age and

PEX as covariates. We found that in both groups age

of the subject was the most significant factor associ-

ated with higher cell loss during cataract surgery

independently of PEX or other variables.

In our study the cornea was more affected centrally

as well as paracentrally in the PEX group than in the

nonPEX group 1 month after the operation, but the

difference between the two groups had a statistically

weak significance (Table 2). Moreover, age but not

PEX, as the most influential preoperative factor,

seems to take credit for this difference. One could, of

course, speculate that in elderly people the synergy of

aging and exfoliation syndrome might lead to pro-

nounced metabolic disturbances of corneal endothe-

lium due to the effects overlapping. The differences in

corneal endothelium between PEX and nonPEX eyes

might therefore be more obvious in the elderly, but

further studies are needed to clarify this issue.

The relationship between endothelial cell loss and

morphometric parameters of the eye as well as

parameters of surgical procedure have been evaluated

in several studies. Walkow and colleagues (14) found

the to be an important factor in cell loss only when

correlated with lens thickness and longer operation

time. They also found a significant correlation be-

tween endothelial cell loss and axial length, but not

between endothelial cell loss and ACD. In contrast,

Kuchle et al. (15) found a significant relationship in

cataract surgery between ACD and endothelial cell

loss in patients with PEX but not between AL and

ECD. In our study no correlation between AL, ACD,

keratometry, lens thickness, and pre- and postopera-

tive ECD was found. Although shallow anterior

chamber and short axial length could dispose reduc-

tion of endothelial cells in cataract surgery, we believe

that surgeon technique and the phaco settings used

are more important.

In this study among intraoperative parameters, the

only significant variable for ECD loss was phaco

power. The presence of PEX did not affect ECD in

regression analysis. Walkow and colleagues (14)

found phaco time to be the most significant intraop-

erative factor in endothelial cell loss. Wirbelauer and

colleagues (11) did not find differences in phaco time

and power between PEX and nonPEX patients, and

neither variable had an influence on ECD in their

study. In our study there was a significant difference

between the two groups in phaco time, which could be

explained by more-cautious surgical technique in

PEX eyes due to insufficient mydriasis and zonular

weakness. We did not find a direct relationship

ANN OPHTHALMOL. 2007;39 (4) ..............................................332

between phaco time and ECD, but time became sig-

nificant in interaction with phaco power. Moreover, in

regression analysis PEX in interaction with overall

phaco impact (phaco time multiplied by power) had a

significant influence on endothelial cell loss. This

indicates that PEX in cases with high phaco impact

(e.g., hard nucleus) significantly increases the risk of

endothelial cell loss.

Similarly to other studies (7,26) we found signifi-

cant rise of IOP in the first postoperative day that

returned to the baseline value during 1 month. Po-

hjanen and colleagues (7) found normalized IOP

1 week after cataract surgery. Patients with PEX had

a tendency to postoperative rise of IOP but not sig-

nificantly compared to the control group. IOP post-

operative peak is transient and does not have a

significant influence on endothelial cell damage.

Regression analysis of our data showed that pre- and

postoperative IOP did not have an effect on ECD in

either group.

In summary, we found age to be the most impor-

tant parameter in endothelial cell loss in patients with

and without PEX. Phaco power was the most

important intraoperative variable for endothelial cell

loss. Although endothelial cell loss was more ex-

pressed in the PEX than in the nonPEX group, a

statistically significant negative correlation was

determined only in interaction with the overall phaco

impact. An experienced surgeon using highly adhesive

viscoelastic should operate in cases of presumably

prolonged operation time on eyes with a hard nucleus

and PEX.

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