ARTICLE

Corneal endothelial dam

age after cataract surgeryin eyes with pseudoexfoliation syndrome

Ken Hayashi, MD, Shin-ichi Manabe, MD, Koichi Yoshimura, MD, Hiroyuki Kondo, MD

Q 2013 A

Published

SCRS an

by Elsev

PURPOSE: To compare corneal endothelial cell damage and ocular inflammation after cataractsurgery in eyes with and without pseudoexfoliation (PXF).

SETTING: Hayashi Eye Hospital, Fukuoka, Japan.

DESIGN: Nonrandomized comparative study.

METHODS: This study comprised eyes with PXF (PXF group) and age-matched eyes without PXF(non-PXF group) scheduled for phacoemulsification. Preoperatively and 1 and 3 monthspostoperatively, corneal endothelial cell density (ECD) and central corneal thickness (CCT) weremeasured using a specular microscope. Flare intensity was measured using a flare meter, andcentral macular thickness was measured using optical coherence tomography.

RESULTS: Each group had 36 eyes. The mean ECD was significantly lower in the PXF group than inthe non-PXF group preoperatively and postoperatively (P%.0250). The percentage of endothelialcell loss was significantly greater in the PXF group than in the non-PXF group (P%.0216); thepercentage was 9.0% in the PXF group and 3.4% in the non-PXF group 3 monthspostoperatively. The mean CCT was similar between groups throughout the follow-up period;however, the percentage increase in CCT was significantly greater in the PXF group than in thenon-PXF group 1 month postoperatively (PZ.0152). Flare intensity and foveal thickness did notdiffer significantly between groups throughout the follow-up period (PR.3079).

CONCLUSIONS: Corneal endothelial cell loss and a transient increase in CCT were greater aftercataract surgery in eyes with PXF than in eyes without PXF. Thus, because the corneal endotheliumin eyes with PXF is vulnerable to cataract surgery, careful surgical procedures are necessary.

Financial Disclosure: No author has a financial or proprietary interest in any material or methodmentioned.

J Cataract Refract Surg 2013; 39:881–887 Q 2013 ASCRS and ESCRS

Pseudoexfoliation (PXF) syndrome is a common condi-tion characterized by the production and accumulationof an abnormal fibrillar extracellular material in manyocular and systemic tissues.1,2 The prevalence of PXFsyndrome increaseswith age andvarieswidely in racialand ethnic populations.3–7 The ocular manifestationof this syndrome is the deposition of PXF material inthe anterior eye segment, such as in the iris, anteriorchamber angle, lens surface, and zonule, which resultsin many complications, including glaucoma, cataract,poor mydriasis, and zonular instability.1,2,8

Cataract surgery in eyes with PXF is difficult due tozonular instability and poormydriasis.9–13 In addition,morphologic studies indicate that PXF material is pro-duced and accumulates in corneal endothelial cells,leading to a progressive change in the endotheliumas a consequence of the PXF process.14,15 Furthermore,many clinical studies have found decreased corneal

d ESCRS

ier Inc.

endothelial cell density (ECD)16–19 and decreased orincreased central corneal thickness (CCT) in eyeswith PXF.19–22 Despite abnormal corneal endothelialcells and difficulty of surgical techniques in eyes withPXF, previous studies23–25 showed that endothelialcell loss after cataract surgery in eyes with PXF doesnot differ significantly from that in eyes without PXF.

This study was designed to evaluate the degree ofcorneal endothelial damage and ocular inflammationafter cataract surgery in eyes with PXF. Age-matchedeyes without PXF that had the same surgical proce-dure served as controls.

PATIENTS AND METHODS

Patients

Eyes of consecutive patients with PXF (PXF group)scheduled to have phacoemulsification and intraocular lens

0886-3350/$ - see front matter 881http://dx.doi.org/10.1016/j.jcrs.2013.01.032

882 CORNEAL ENDOTHELIAL DAMAGE AFTER CATARACT SURGERY IN EYES WITH PXF

(IOL) implantation between September 2011 and May2012 were screened by a clinical research coordinator. Thepresence of PXF material in the anterior eye segment wasdetermined by ophthalmologists using slitlamp microscopy.Exclusion criteriawere eyeswith pathology of the cornea, vit-reous, or macula; planned extracapsular cataract extraction;a history of ocular inflammation or surgery; a fully dilatedpupil diameter of less than 4.0mm; patient refusal; and antic-ipated difficulties with examination, analysis, or follow-up.For controls, eyes of age-matched patients without PXF(non-PXF group) were enrolled. These patients were within5 years of age of those in the PXF group and were scheduledto have cataract surgery with IOL implantation. When botheyes (with or without PXF) were operated on, only the firstoperated eye was included in the analysis. Screening wascontinued until 40 eyes were recruited for each group. Alleyes received the same single-piece hydrophobic acrylicIOL with a 6.0 mm round aspheric optic (Acrysof SN60WF,Alcon Laboratories, Inc.). This research adhered to the tenetsof the Declaration of Helsinki. The institutional review boardapproved the study protocol, and informed consent was ob-tained from each patient.

Surgical Technique

The same surgeon (K.H.) performed all cataract surgeriesusing previously described procedures.26 The surgeonmade a 2.4 mm clear corneal incision horizontally in eyeswith against-the-rule or oblique corneal astigmatism andsuperiorly in eyes having with-the-rule astigmatism. Thesoft-shell technique using a dispersive (sodium hyaluronate3.0%–chondroitin sulfate 4.0% [Viscoat]) ophthalmic visco-surgical device (OVD) and a cohesive (sodium hyaluronate1.0% [Healon]) OVD was used. Through the side ports,approximately 0.1 mL of dispersive OVD was injected intothe anterior chamber and 0.1 to 0.2 mL of cohesive OVDwas injected below the dispersive OVD to form a layer ofthe dispersive OVD beneath the corneal endothelium. A con-tinuous curvilinear capsulorhexis measuring approximately5.5 mm in diameter was created using a 25-gauge bentneedle. After thorough hydrodissection, phacoemulsificationof the nucleus and aspiration of the residual cortex were per-formed. The lens capsule was inflated with the cohesiveOVD, and then the IOLwas placed in the capsular bag. AfterIOL implantation, all OVDs were thoroughly removed. Inthis series, no surgical procedure was performed for pupilenlargement.

Main Outcome Measures

All eyes had examinations preoperatively and 1 and3 months postoperatively. Corneal ECD (cells/mm2) and

Submitted: November 13, 2012.Final revision submitted: December 27, 2012.Accepted: January 3, 2013.

From Hayashi Eye Hospital (Hayashi, Manabe, Yoshimura) and theDepartment of Ophthalmology (Kondo), University of Occupationaland Environmental Health, Fukuoka, Japan.

Corresponding author: Ken Hayashi, MD, Hayashi Eye Hospital,4-23-35, Hakataekimae, Hakata-Ku, Fukuoka 812-0011, Japan.E-mail: hayashi-ken@hayashi.or.jp.

J CATARACT REFRACT SURG

CCT (mm) were examined using a noncontact specularmicroscope (SP-9000, Konan Medical).26 The video imagein which the endothelial cell borders could be seen mostclearly was transmitted to the image-analysis computer,and the ECD was determined automatically. Reliabilityand reproducibility of the ECD data obtained using the auto-mated specular microscope when the ECD was virtuallywithin normal range were verified previously.27–29 Endothe-lial cell loss was expressed as a percentage of the preopera-tive ECD, and the increase in CCT was expressed asa percentage of the preoperative CCT.

The uncorrected distance visual acuity (UDVA) andcorrected distance visual acuity (CDVA) were examinedon decimal charts preoperatively and 1 and 3 monthspostoperatively; decimal visual acuity was converted to thelogMAR scale for statistical analysis. Flare intensity wasmeasured preoperatively and 1 week and 1 and 3 monthspostoperatively using a flare meter (FC-1000, Kowa Co.Ltd). The central retinal (foveal) thickness was measuredusing the Cirrus optical coherence tonometer (OCT)(Carl Zeiss Meditec AG).30 In eyes in which a clear OCTimage could not be obtained preoperatively because of densecataract, the OCT examination was performed 1 day aftersurgery and the value at 1 day was used as the preoperativevalue.31 Objective refractive status was measured using anautorefractometer (KR-7100, Topcon Corp.). The manifestspherical equivalent (SE) value was determined as thespherical power plus half the cylindrical power. Thesemeasurements were performed by 5 experienced ophthalmictechnicians unaware of the purpose of this study.

The surgeon graded nuclear firmness preoperatively ac-cording to the Emery-Little classification.32 During cataractsurgery, surgical time (minutes), ultrasound time (seconds),mean ultrasound power (%), total ultrasound energy emitted(millijoules), and irrigation volume used (milliliters) wererecorded.

Statistical Analysis

Differences between the PXF group and the non-PXFgroup in ECD, percentage of endothelial cell loss, CCT, per-centage increase in CCT, flare intensity, foveal thickness,UDVA, CDVA, operative factors, and other continuous vari-ables were compared using the Mann-Whitney U test.Discrete variables between the 2 groups were comparedusing the chi-square test or Fisher exact probability test.Differences with a P value less than .05 were consideredstatistically significant.

RESULTS

Of the 40 eyes in the PXF group, 13 eyes had glaucoma.Four patients in the PXF group and 4 patients in thenon-PXF group were lost to follow-up. Data for36 eyes of 36 patients in the PXF group and 36 eyesof 36 patients in the non-PXF group were analyzed.Themean patient age was 73.3 yearsG 7.6 (SD) (range51 to 89 years); there were 33 men and 39 women.Table 1 shows the patients' demographics and opera-tive factors. There were no statistically significantbetween-group differences in age, sex, the ratio ofleft eyes to right eyes, manifest SE value, keratometriccylinder, nuclear firmness, surgery time, ultrasound

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Table 1. Patient characteristics and operative factors by group.

Parameter PXF Group Non-PXF Group P Value

Patient characteristicMean age (y) 74.6 G 7.1 72.0 G 8.0 .0677Male/female sex (n) 15/21 18/18 .6365Left/right eye (n) 17/19 19/17 .8139Mean SE (D) �1.73 G 3.25 �1.74 G 3.23 .9865Mean keratometriccylinder (D)

0.64 G 0.47 0.72 G 0.54 .6534

Mean nuclearfirmness

2.2 G 0.9 1.9 G 0.6 .0956

Mean ACD (mm) 3.13 G 0.44 3.34 G 0.38 .0487*Mean pupildiameter (mm)

5.53 G 0.76 6.22 G 0.86 .0002*

Operative factorMean surgerytime (min)

7.9 G 1.2 7.6 G 1.8 .1199

Mean US time (s) 43.1 G 14.5 42.6 G 20.0 .3885Mean US power (%) 50.6 G 11.2 46.7 G 10.4 .0828Mean totalUS energy†

22.0 G 4.4 23.2 G 5.3 .2001

Mean irrigationvolume (mL)

64.4 G 11.3 59.4 G 15.5 .0785

Means G SDACD Z anterior chamber depth; PXF Z pseudoexfoliation; SE Z mani-fest spherical equivalent value; US = ultrasound*Statistically significant difference†Total ultrasound power emitted (mJ)

Table 2. Eyes with greater than 10% or 20% endothelial cell lossby group.

Time/ECL

Number (%)

P ValuePXF Group Non-PXF Group

1 monthO10% 11 (30.6) 3 (8.3) .0346*O20% 6 (16.7) 0 .0249*

3 monthsO10% 14 (38.9) 5 (13.9) .0309*O20% 6 (16.7) 0 .0249*

ECC Z endothelial cell loss; PXF Z pseudoexfoliation*Statistically significant difference

883CORNEAL ENDOTHELIAL DAMAGE AFTER CATARACT SURGERY IN EYES WITH PXF

time, mean ultrasound power, total ultrasound poweremitted, or irrigation volume (PR.0677). The anteriorchamber depth (ACD) was shallower and the pupildiameter smaller in the PXF group than in thenon-PXF group (P%.0487). All surgeries wereuneventful.

Figure 1. The mean (GSD) ECD and percentage of endothelial cellloss by group (PEX Z pseudoexfoliation).

J CATARACT REFRACT SURG

The mean ECD was significantly lower in the PXFgroup than in the non-PXF group before surgery and1 and 3 months after surgery (P%.0250) (Figure 1). Thepercentageof endothelial cell loss3monthsafter surgerywas 9.0% in the PXF group and 3.4% in the non-PXFgroup; the percentage cell loss was significantly greaterin the PXF group than in the non-PXF group (P%.0216)(Figure 1). The percentage of cell loss of more than 10%or20%was significantlygreater in thePXFgroup than inthe non-PXF group (P%.0231) (Table 2).

The mean CCT did not differ significantly betweenthe 2 groups throughout the follow-up period(Figure 2). The mean percentage increase in CCT wasgreater in the PXF group than in the non-PXF group1 month after surgery (PZ.0152) (Figure 2), althoughthe difference between groups was not significant at3 months (PZ.5581).

The mean flare intensity tended to be greater in thePXF group than in the non-PXF group; however, thedifference was not significant throughout the follow-up period (PR.3271) (Table 3). The mean foveal

Figure 2. The mean (GSD) CCT and percentage increase in CCT bygroup (CCTZ central corneal thickness; PEXZ pseudoexfoliation).

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Table 3. Comparison of the mean flare intensity, foveal thick-ness, and percentage increase in foveal thickness betweengroups.

Parameter

Mean G SD

P ValuePXF Group Non-PXF Group

Flare intensity (mg/dL)Preop 15.6 G 10.5 12.8 G 9.2 .11861 wk postop 19.2 G 17.3 11.5 G 5.1 .49141 mo postop 21.7 G 17.8 12.5 G 6.2 .09013 mo postop 16.8 G 13.3 11.0 G 4.5 .1740

Foveal thickness (mm)Preop 213 G 24 221 G 24 .46011 mo postop 216 G 18 220 G 26 .87983 mo postop 220 G 20 228 G 29 .4010

Increase in fovealthickness (%)

1 mo postop 2.00 G 6.49 �0.23 G 6.31 .59123 mo postop 3.98 G 9.70 3.43 G 7.43 .6627

PXF Z pseudoexfoliation

Table 4. Comparison of mean UDVA and CDVA betweengroups.

Parameter

Mean G SD

P ValuePXF Group Non-PXF Group

LogMAR UDVAPreop 1.02 G 0.50 0.91 G 0.37 .67141 mo postop 0.31 G 0.36 0.18 G 0.21 .14843 mo postop 0.31 G 0.36 0.13 G 0.16 .0466*

LogMAR CDVAPreop 0.47 G 0.21 0.57 G 0.29 .30561 mo postop 0.08 G 0.14 0.02 G 0.06 .25073 mo postop 0.08 G 0.14 0.00 G 0.04 .1438

CDVA Z corrected distance visual acuity; PXF Z pseudoexfoliation;UDVA Z uncorrected distance visual acuity*Statistically significant difference

884 CORNEAL ENDOTHELIAL DAMAGE AFTER CATARACT SURGERY IN EYES WITH PXF

thickness was similar between the 2 groups through-out the follow-up period (PR.3079) (Table 3). Thepercentage increase in the mean foveal thickness wasalso similar between the 2 groups (PR.4404) (Table 3).

The mean UDVA and CDVA were similar betweenthe PXF group and the non-PXF group before and aftersurgery (PR.0265) (Table 4).

The subgroup analysis of the PXF group with andwithout glaucoma showed no significant difference

Table 5. Comparison of the mean ECD, percentage of endothe-lial cell loss, CCT, and percentage increase in CCT between eyeswith and without glaucoma.

Parameter

Mean G SD

P ValueEye WithGlaucoma

Eyes WithoutGlaucoma

ECD (cells/mm2)Preop 2534 G 243 2646 G 203 .11861 mo postop 2286 G 318 2385 G 293 .52373 mo postop 2410 G 339 2353 G 320 .6627

CCT (mm)Preop 530 G 49 534 G 36 .49131 mo postop 548 G 54 547 G 38 .77543 mo postop 535 G 48 532 G 36 .9065

Endothelial cell loss (%)1 mo postop 10.0 G 6.5 9.7 G 10.1 .46033 mo postop 5.1 G 7.3 10.9 G 11.3 .0934

Increase in CCT (%)1 mo postop 3.4 G 3.3 2.6 G 4.1 .26803 mo postop 1.0 G 2.5 -0.3 G 3.9 .0439*

CCT Z central corneal thickness; ECD Z endothelial cell density*Statistically significant difference

J CATARACT REFRACT SURG

in mean ECD, percentage of endothelial cell loss,CCT, increase in CCT 1 month postoperatively, flareintensity, foveal thickness, increase in foveal thickness,UDVA, or CDVA between eyes with PXF glaucomaand eyes without PXF glaucoma (PR.0234) (Table 5).The mean increase in CCT 3 months postoperativelywas significantly greater (PZ.0439) and the ACD sig-nificantly shallower (PZ.0098) in eyes with glaucomathan in eyes without glaucoma.

Figure 3 shows photographs of the endothelialcells of a representative eye in the PXF group and thenon-PXF group. In PXF eyes, the size of the endothelialcells was increased (cell size 399 mm2 preoperativelyand 590 mm2 3 months postoperatively) and the cellshape became more variable after cataract surgery.In contrast, in non-PXF eyes, cell size did notchange markedly (cell size 346 mm2 preoperativelyand 354 mm2 3 months postoperatively) and the cellshape was virtually uniform and hexagonal beforeand after surgery.

DISCUSSION

In this study, the mean ECDwas significantly lower ineyes with PXF than in eyes without PXF before and af-ter cataract surgery. The percentage of endothelial cellloss was significantly greater in eyes with PXF than ineyes without PXF, despite the similarities in nuclearfirmness and operative factors. The percentage of cellloss 3 months after surgery in the PXF group was9.0%, while that in the non-PXF groupwas 3.4%. In ad-dition, the incidence of eyes with a percentage cell lossof greater than 20% was significantly greater in thePXF group than in the non-PXF group; the percentageat 3 months was 16.7% in the PXF group and 0% in thenon-PXF group. Furthermore, the percentage increasein CCTwas significantly greater in eyes with PXF thanin eyes without PXF 1 month after surgery. These

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Figure 3. Specular microscopic photographs of corneal endothelial cells of a representative eye in the PXF group and the non-PXF group(PEX Z pseudoexfoliation).

885CORNEAL ENDOTHELIAL DAMAGE AFTER CATARACT SURGERY IN EYES WITH PXF

findings suggest that corneal endothelial cells of PXFeyes are essentially deteriorated and are more vulner-able to cataract surgery than healthy endothelial cells.

A subgroup comparison between eyes withglaucoma and those without glaucoma found nosignificant difference in the mean ECD, endothelialcell loss, CCT, or increase in CCT 1 month aftersurgery. Only the increase in CCT 3 months aftersurgery was significantly greater in eyes withglaucoma than in eyes without glaucoma. The meanincrease in CCT, however, was 1.0% in eyes withglaucoma and �0.29% in eyes without glaucoma; thedifference was very small. Few studies have comparedcorneal endothelial injury due to cataract surgery ineyes with PXF glaucoma and eyes without PXFglaucoma. Our study suggests that corneal endothelialdamage does not differ markedly between eyes withglaucoma and those without glaucoma.

Flare intensity was slightly greater in eyes with PXFthan in eyes without PXF during the follow-up period;however, the difference did not reach statistical signif-icance. Furthermore, foveal thickness was similar ineyes with PXF and eyes without PXF and in PXF eyeswith glaucoma and PXF eyes without glaucoma.

J CATARACT REFRACT SURG

Schumacher et al.33 and Abela-Formak et al.,34 how-ever, found that flare intensity was greater in eyeswith PXF than in eyes without PXF after cataract sur-gery. Y€uksel et al.35 also showed that foveal thicknessafter cataract surgery was greater in eyes with PXFglaucoma than in eyes without PXF glaucoma or ineyes without PXF. These inconsistencies might be dueto the degree of PXF deposition. In the present study,eyes with poor mydriasis due to extensive PXF deposi-tion were excluded to equalize the operative factors;only eyes with slight deposition of PXF material wereenrolled.We consider that postoperative ocular inflam-mation is notmarkedly greater in eyeswith PXF than ineyes without PXF as long as PXF eyes do not requirespecial surgical procedures, such as pupil dilation orthe use of capsule stabilization devices.

The mean UDVA and CDVA in the PXF group weresimilar to those in the non-PXF group. In addition,the UDVA and CDVA were not significantly differentin eyes with glaucoma and eyes without glaucoma.These results suggest that the vulnerability of the cor-neal endothelial cells in eyes with PXF does not affectvisual acuity as long as the central visual field defectsdue to glaucoma are not prominent.

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886 CORNEAL ENDOTHELIAL DAMAGE AFTER CATARACT SURGERY IN EYES WITH PXF

Previous morphologic studies showed that PXFmaterial is producedandaccumulates in the corneal en-dothelial cells and that the endothelial cells degenerateprogressively as a consequence of the PXF process.14,15

Furthermore, many clinical studies have shownthat the corneal ECD decreases and the CCT increasesor decreases in eyes with PXF compared with eyeswithout PXF.19–22 Despite the abnormality of theendothelial cells and difficult surgical techniques re-quired for PXF eyes, previous studies did not find a sig-nificant difference in endothelial cell loss after cataractsurgery between eyes with PXF and those withoutPXF.23–25 In these studies, themeanpercentage of endo-thelial cell loss in healthy, non-PXF eyes was greaterthan 10%, higher than that obtained in the presentstudy.We assume that a larger incision or former surgi-cal techniques used in the previous studies might beassociated with the greater percentage cell loss in thehealthy, non-PXF eyes. In our study, endothelial celldamage after cataract surgery was significantly greaterin eyeswithPXF than in eyeswithoutPXF, even thoughsmall-incision surgery was performed using recent ad-vanced techniques and devices.

To prevent severe endothelial injury during cataractsurgery in eyes with PXF, accurate preoperativeassessments of corneal endothelial status and zonularinstability are required. For assessment of endothelialstatus, the evaluation of the CCT is also important inaddition to the ECD. When the CCT is increased ordecreased, the endothelial function may be compro-mised.26 In addition, K€uchle et al.12 report that anACD of less than 2.5 mm is a risk factor for zonularinstability. Furthermore, poor mydriasis may also beassociated with zonular weakness. Accordingly, thepreoperative measurement of the ACD and pupildiameter after full dilation is recommended in eyeswith PXF. When the ACD is shallow and mydriasis ispoor, pupil-enlarging devices or a capsule-supportingdevice, such as flexible iris retractors, should beprepared.

In conclusion, corneal endothelial cell loss after cata-ract surgery in eyes with PXFwas substantially greaterthan that in eyes without PXF. The transient increase incorneal thickness was also greater in eyes with PXFthan in eyeswithout PXF,which implies the vulnerabil-ity of corneal endothelial cells to cataract surgery.In particular, approximately 17% of eyes with PXFhad severe cell loss (O20%), even in cases inwhich spe-cial surgical procedures were not used. Accordingly,for more challenging cases with PXF, including thosewith poor mydriasis or zonular instability, surgeonsshould use special surgical devices and procedures toprevent endothelial cell injury, including the soft-shelltechnique, pupil-enlargement devices, and capsule-supporting devices. Furthermore, glaucoma surgery,

J CATARACT REFRACT SURG

specifically trabeculectomy using mitomycin-C, orglaucoma implant surgery causes severe endothelialcell injury,36–38whichmay lead to cornealdecompensa-tion in eyes with PXF glaucoma. Additional studiesare required to evaluate corneal endothelial cell dam-age after glaucoma surgery in eyes with PXF.

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WHAT WAS KNOWN BEFORE

� Many studies found that corneal ECD decreased and CCTdecreased or increased in eyes with PXF. However, previ-ous studies showed that corneal endothelial cell loss aftercataract surgery in eyes with PXF does not differ signifi-cantly from that in eyes without PXF.

WHAT THIS PAPER ADDS

� Corneal endothelial cell loss and transient increase in CCTwere greater after cataract surgery in eyes with PXF than inhealthy eyeswithout PXF, suggesting the vulnerability of thecorneal endothelium to cataract surgery in eyes with PXF.

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- VO

L 39, JUNE 2013

First author:Ken Hayashi, MD

Hayashi Eye Hospital, Fukuoka, Japan