Corneal endothelial cell protection with a dispersive viscoelastic material and an irrigating solution during phacoemulsification Low-cost versus expensive combination Barbara Kiss, MD, Oliver Findl, MD, Rupert Menapace, MD, Vanessa Petternel, MD, Matthias Wirtitsch, MD, Thomas Lorang, PhD, Manfred Gengler, PhD, Wolfgang Drexler, PhD Purpose: To evaluate the protective effect on corneal endothelial cells of a lowcost and an expensive combination of a dispersive viscoelastic material and an irrigating solution during phacoemulsification. Setting: Department of Ophthalmology, University of Vienna, Vienna, Austria. Methods: This prospective randomized examiner- and patient-masked study comprised 90 eyes of 45 consecutive patients with age-related cataract in both eyes. For each patient, the first eye was randomly assigned to receive hydroxypropyl methylcellulose 2% (Ocucoat®) and Ringer’s solution (low-cost combination) or sodium chondroitin sulfate 4%–sodium hyaluronate 3% (Viscoat®) and an enriched balanced salt solution (BSS Plus®) (expensive combination) during phacoemulsification. The contralateral eye received the other treatment. Endothelial cell function was evaluated by measuring corneal thickness (CT) using partial coherence interferometry, morphology assessment, and endothelial cell counts. Results: The acute postoperative increase in CT was ⫹9.8 m in the low-cost group and ⫹10.9 m in the expensive group; the difference between groups was not significant. After 1 month, the CT still differed significantly from baseline in the low-cost group. Three months after surgery, the CT had returned to baseline values in both groups. There was no significant between– group difference in endothelial cell counts or morphology. Conclusions: During phacoemulsification in a nonselected patient population, there was no difference in acute postoperative corneal edema and endothelial cell morphology after 3 months between a Viscoat and BSS Plus combination and an Ocucoat and Ringer’s solution combination. Eyes receiving the expensive combination had marginally faster recovery of corneal swelling by 3 months. However, the cost of Viscoat and 500 mL BSS Plus is 5 times that of Ocucoat and Ringer’s solution. J Cataract Refract Surg 2003; 29:733–740 © 2003 ASCRS and ESCRS
T
he corneal endothelium consists of a monolayer of cells on the posterior corneal surface that has no regeneratory ability after injury. The normal thickness and transparency of the cornea are maintained by a barrier function and the active fluid pump of corneal © 2003 ASCRS and ESCRS Published by Elsevier Science Inc.
endothelial cells.1,2 The natural loss of human endothelial cells is approximately 0.5% each year.3 Intraocular manipulation, such as that during phacoemulsification cataract surgery, causes fluid and lens fragment turbulence that can lead to endothelial cell damage such 0886-3350/03/$–see front matter doi:10.1016/S0886-3350(02)01745-5
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as a transient compromised function and permanent cell loss.4 – 8 Since the introduction of sodium hyaluronate in ophthalmic surgery in the early 1970s, viscoelastic materials have assumed a major role in anterior segment surgery. New viscoelastic materials have been developed to improve protection of corneal endothelial cells during phacoemulsification. Currently, there are 2 main types of viscoelastic materials for enhanced protection of the corneal endothelium: (1) high-viscosity, cohesive materials (eg, sodium hyaluronate), which are space maintaining, and (2) low-viscosity, dispersive materials (eg, sodium chondroitin sulfate 4%–sodium hyaluronate 3% such as Viscoat威 and hydroxypropyl methylcellulose 2% such as Ocucoat威), which adhere to the corneal endothelium, providing a protective layer throughout the surgical procedure. Such materials are often used in patients with a low preoperative endothelial cell count. In addition to viscoelastic materials, irrigating solutions should not alter the usual milieu of the cells, should maintain appropriate tonicity and electrolyte concentrations, and should provide an energy source during phacoemulsification.9 –12 Enriched balanced salt solutions such as BSS Plus威 (glucose glutathione bicarbonate solution) provide characteristics similar to those of the aqueous humor to maintain constant intraocular conditions.13–17 However, dextrose bicarbonate lactated Ringer’s solution for irrigation has been reported to be as effective as enriched BSS during phacoemulsification.18 This study compared the endothelial protective effect of a low-cost combination of a viscoelastic material and an irrigating solution, Ocucoat and Ringer’s soluAccepted for publication July 16, 2002. From the Departments of Ophthalmology (Kiss, Findl, Menapace, Petternel, Wirtitsch) and Medical Computer Sciences (Lorang, Gengler) and the Institute for Medical Physics (Drexler), University of Vienna, Vienna, Austria. Presented in part at the ASCRS Symposium on Cataract, IOL and Refractive Surgery, Boston, Massachusetts, USA, May 2000, and XVIIIth Congress of the European Society of Cataract & Refractive Surgeons, Brussels, Belgium, September 2000. None of the authors has a financial or proprietary interest in any material or method mentioned. Reprint requests to Oliver Findl, MD, Department of Ophthalmology, University of Vienna, Waehringer Guertel 18-20, A-1090 Vienna, Austria. E-mail:
[email protected]. 734
tion, with a more expensive combination of Viscoat and BSS Plus, which costs approximately 5 times more. We assessed their effect on corneal thickness (CT) and corneal endothelial cell function and morphology during phacoemulsification.
Patients and Methods This prospective randomized examiner- and patientmasked study comprised 90 eyes of 45 consecutive patients with bilateral age-related cataract scheduled for small-incision cataract surgery with intraocular lens (IOL) implantation in both eyes. The median age of the patients was 77 years (range 54 to 88 years). In each patient, the first eye was randomly assigned to receive an Ocucoat and Ringer’s solution combination (low-cost group) or a Viscoat and BSS Plus combination (expensive group) The contralateral eye received the alternative treatment.
Measurements Central corneal thickness was assessed with partial coherence laser interferometry (PCI) preoperatively and 1 day, 1 week, and 1 and 3 months after surgery. Ten measurements per eye were obtained at each observation. The examiner was masked to the combination used. Partial coherence interferometry is a noncontact optical measurement technique for intraocular distances. The principle of the dual-beam version of PCI has been reported in detail.19 –21 With PCI, the precision of CT measurements is 0.3 m. A single CT measurement takes 0.5 seconds. During measurement, the eye fixates on the laser beam. The measurements with dual-beam PCI are precise because the technique is not sensitive to longitudinal eye movement. The endothelium of the central cornea was examined with a specular microscope (Noncon Robo-CA, Konan Medical Corp.) preoperatively and 3 months after surgery. Three endothelial cell photographs were taken per eye at each examination, and at least 50 endothelial cells were evaluated in each image. The images were stored on a personal computer. The endothelial cell density, hexagonality, and cell area were evaluated by 1 masked examiner. The mean of the 3 photographs was calculated. During surgery, the ultrasound time (seconds) and amount of irrigating solution used (milliliters) were also noted.
Surgical Technique All patients were operated on by the same surgeon (R.M.) in the same fashion. Approximately 1 to 2 hours before surgery, diclofenac (Voltaren Ophtha威), phenylephrine 2.5%, tropicamide 0.5% (Mydriaticum Agepha威), and cyclopentolate 1% (Cyclopentolate Thilo威) eyedrops were instilled. After peribulbar anesthesia was administered, a temporal singleplane 3.5 mm posterior limbal incision was created. The assigned viscoelastic material (Viscoat or Ocucoat) was then instilled into the anterior chamber. After a capsulorhexis was
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created and hydrodissection performed, phacoemulsification of the nucleus was done with an Oertli Orbit unit using a cracking technique. This was followed by aspiration of the cortical remnants and cleaning of the capsular bag. Ringer’s solution or BSS Plus, depending on the randomization, was used for irrigation. The capsular bag was expanded with the assigned viscoelastic material, and a foldable 3-piece silicone IOL was implanted in the capsular bag. The viscoelastic material was aspirated thoroughly from the retrolental space and the anterior chamber using an irrigation/aspiration (I/A) tip. For removal, the proximal optic edge was tilted up with a spatula and the I/A tip inserted behind the optic. After the central portion of the viscoelastic material was removed, the residual material was removed by sweeping the I/A tip across and along the capsule equator. The I/A tip was guided into the anterior chamber and the optic repositioned. As the aspiration opening was rotated to the right, the left, or posteriorly, the viscoelastic material was circumferentially removed from the prelental, retroiridal, and preiridal spaces. Because care was taken not to approach the structures of the endothelium and the chamber angle too closely, residual coating of these structures was observed. Finally, the I/A tip was positioned on the center of the optic. As the aspiration opening was directed upward and the tip pressed down on the optic, the anterior chamber was rinsed. The I/A tip was then retracted. The incision was left sutureless. No miotic agent was used intracamerally, and no antiglaucoma agent was instilled immediately after cataract surgery. After surgery the eye was patched with prednisolone ointment (Ultracortenol威). Treatment was started after the 20- to 24-hour visit with diclofenac (Voltaren Ophtha威) and prednisolone acetate 0.5% (Ultracortenol威) eyedrops 4 times a day for 1 month.
Statistical Analysis The sample size for CT changes was calculated as 44 patients by assuming a significance level of 5% and a statistical power of 80% to detect a mean difference of 5.0 m, representing approximately 1% of the central CT. Based on data from an unpublished pilot study, the standard deviation of the differences was assumed to be 11.5 m. Observed data are presented as means and standard deviations. The precision of the techniques is defined as the standard deviation of multiple consecutive measurements of the central CT. To compare the means, paired t tests were applied and, where appropriate, the 95% confidence interval (CI) was reported. Correlations were investigated using scatterplots and Spearman correlation coefficients. All P values are results of 2-sided tests; P ⫽ .05 was considered statistically significant. The Statistica® software package (release 4.5, StatSoft Inc.) was used for computations.
Results Forty-four patients completed CT measurements in both eyes at baseline and 1 day after surgery. Case-wise
deletion was performed for statistical analysis, resulting in 36 patients with a complete data set for CT changes at all time points; 39 patients were used for endothelial cell count parameters. The mean phacoemulsification time was 28 seconds ⫾ 17 (SD) in the low-cost group and 28 ⫾ 14 seconds in the expensive group (P ⫽ .90). Irrigation volume was 149 ⫾ 22 mL in the low-cost group and 142 ⫾ 23 mL in the expensive group (P ⬍ .01). The central CT was significantly greater than baseline 1 day and 1 week after surgery (Figure 1, Table 1). There was an acute increase in CT from preoperatively to the first postoperative day (Figure 2). One month postoperatively, the CT was still significantly higher than baseline in the low-cost group (P ⬍ .01); however, the difference between the low-cost and expensive groups was not statistically significant (P ⫽ .24) (Figure 1, Table 1). By 3 months, the CT had returned to baseline values in both groups (Figure 2, Table 1). The data of all 44 patients who completed the preoperative and the first postoperative follow-up were evaluated to confirm a similar acute decrease in CT in both groups. The mean decrease was ⫹11.0 ⫾ 12.1 m (95% CI ⫹7.3 to ⫹14.7) in the low-cost group (P ⬍ .01) and ⫹12.6 ⫾ 13.2 m (95% CI ⫹8.6 to ⫹16.6) in the expensive group (P ⬍ .01). The mean CT did not differ significantly between groups at any measurement (Table 2). At 1 and 3 months, the change from baseline was significantly different between groups. At all measurements, the mean difference between the 2 groups was less than
Figure 1. (Kiss) Change in central CT from baseline in the low-cost group (solid squares) and expensive group (open circles) (means ⫾ SEM) (N ⫽ 36) (pre ⫽ preoperative; d ⫽ day; w ⫽ week; m ⫽ month).
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Table 1. Baseline values and change (absolute and relative) in CT (N ⫽ 36). Low Cost
Expensive †
Exam
CT (m)*
CT (%)
P Value
CT (m)*
CT (%)
P Value†
Preop
529.0 ⫾ 30.0
—
—
531.0 ⫾ 30.0
—
—
Postop 1d
⫹9.8 ⫾ 12.0
⫹1.9
⬍.01
⫹10.9 ⫾ 11.1
⫹2.1
⬍.01
1 wk
⫹8.7 ⫾ 12.4
⫹1.6
⬍.01
⫹7.9 ⫾ 9.0
⫹1.5
⬍.01
1 mo
⫹4.7 ⫾ 8.6
⫹0.9
⬍.01
⫹1.8 ⫾ 9.1
⫹0.3
.24
3 mo
⫹1.5 ⫾ 5.3
⫹0.3
.11
⫺0.4 ⫾ 5.5
⫺0.1
.66
*Mean ⫾ SD † Difference between baseline and follow-up within groups, t test
5 m, which has been defined as clinically relevant; the confidence intervals slightly exceeded this limit once. The endothelial cell density (N ⫽ 39) slightly decreased in both groups, but neither had a significant difference from baseline (low-cost group, ⫺4.0% ⫾ 12.6%, 95% CI ⫺8.1 to ⫹0.1; expensive group, ⫺0.3% ⫾ 8.5%, 95% CI ⫺3.1 to ⫹2.4) (Figure 2, Table 3), nor was there a significant difference between groups (P ⫽ .15). There was a small change in hexagonality that did not reach the level of significance within or between groups. The cell area increased slightly in the low-cost group (Table 3) (P ⫽ .05); the change in the expensive group was not significant. The coefficient of variation in cell size decreased significantly (⫺0.02 ⫾ 0.05; P ⬍ .01) in the expensive group. No cell parameter showed a significant change between the groups. The acute CT change from preoperatively to the first postoperative day and the change in corneal cell count from preoperatively to 3 months after surgery were not significantly correlated (low-cost group, r ⫽ 0.01, P ⫽ .94; expensive group, r ⫽ ⫺0.09, P ⫽ .61) (Figure 3).
Discussion In our study, the phacoemulsification time was equal between the groups and irrigation volume was only slightly higher in the low-cost group. There was an acute, significant increase in the central CT after phacoemulsification cataract surgery in both groups. Over the following weeks, the CT continuously decreased and returned to baseline values by 3 months in the low-cost group and 1 month in the expensive group. The absolute 736
CT data did not differ significantly between the groups at any time. However, the mean change in CT versus baseline was significantly different between the groups after 1 month and tended to be smaller in the expensive group after 3 months. We observed a mean endothelial cell loss of ⫺4.0% in the low-cost group and ⫺0.3% in the expensive group. Neither endothelial cell loss nor percentage of hexagonal cells differed significantly from baseline. In the low-cost group, the increase in cell area reached the level of significance. In the expensive group, the coefficient of variation in cell size decreased significantly. However, no change in endothelial cell variables differed between the groups. Corneal thickness increases when the pump and barrier functions of the endothelium are compromised. Corneal pachymetry provides a measurement of the amount of surgically induced endothelial injury.2 In this study, we used a pachymetry technique, PCI, that provides submicrometer precision and high resolution. Precision is approximately 1 order better than that of conventional ultrasound or optical pachymetry. Therefore, we were able to detect very small changes in CT between study groups. After phacoemulsification, other authors report an acute reversible increase in central CT, similar to our results.22–25 With the development of viscoelastic materials, different observations about their protection of the endothelium have been made. Compared to Healon威 (sodium hyaluronate 1%), Viscoat, a dispersive (adhesive) viscoelastic material, coats the corneal endothelium more readily and tends to remain in the eye intraoperatively.26,27 Therefore, it has been suggested that Viscoat offers greater endothelial protection during phacoemul-
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Figure 2. (Kiss) Acute postoperative increase in CT from preoperatively to the first postoperative day (n ⫽ 36) (upper) and percentage change in cell density (CD) (n ⫽ 39) between preoperatively and 3 months postoperatively (lower). In the box plots, the whiskers show the minimum and the maximum, the box depicts the 25th and 75th percentiles and the median, the circles are outliers, and the asterisk represents an extreme value.
sification.28 A difference in acute corneal swelling has been observed between Viscoat and Healon GV威 (sodium hyaluronate 1.4%)24 and Ocucoat and Healon.25 One week postoperatively, Ravalico et al.29 found a significant difference in CT change between Viscoat and hydroxypropyl methylcellulose 2%. Most investigators observed that corneal swelling decreased to baseline values within at least 2 weeks and could not find differences between viscoelastic materials over the long term.24,29 –33 Corneal endothelial cell loss has been reported to be 1.4% for Ocucoat and 0.3% for Viscoat34 after 3 months, similar to our results. Although endothelial cell counts remain irreversibly altered 1 year postoperatively, cell function usually returns to normal after cataract surgery.35 Endothelial cell repair leads to a reduction in endothelial cell density, a proportional increase in mean cell size, and disruption of the normal hexagonal pattern.36 Analysis of endothelial cell size and shape provides a more sensitive indicator of endothelial cell damage than cell density measurements alone.37 Contradictory reports of changes in endothelial cell counts with different viscoelastic materials have been published. Glasser and coauthors38 observed that Healon, Viscoat, and methylcellulose 2% were equally effective in reducing endothelial cell loss by rubbing an IOL over the endothelium of rabbit corneas in vitro. Lane et al.39 found similar amounts of endothelial cell loss in eyes receiving Healon, Viscoat, and Ocucoat. However, Glasser and coauthors28 observed less endothelial cell loss in eyes treated with Viscoat and Ocucoat than in those receiving Healon, which was confirmed by Monson et al.40 In contrast, Ravalico et al.29 found greater endothelial permeability and a more active pump after 30 days with hydroxypropyl methlycellulose 2% than
Table 2. Differences in CT changes from baseline between groups (low cost– expensive) (N ⫽ 36). Mean Difference (m)
SD (m)
Lower Limit
Upper Limit
P Value*
⫺1.0
11.0
⫺4.8
2.9
.58
Preop–1 wk
0.8
11.1
⫺3.0
4.5
.67
Preop–1 mo
2.9
6.7
0.6
5.1
.02
Preop–3 mo
1.9
5.2
0.1
3.6
.04
Period Preop–1 d
95% CI
CI ⫽ confidence interval *Difference between groups, t test
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Table 3. Baseline values and change (mean of absolute changes and of percentage changes) in endothelial cell morphology 3 months after surgery (N ⫽ 39). Low Cost Parameter
Baseline
Change (P Value)
Expensive Change (%)
Baseline
Change (P Value)
Change (%)
Cell density (cells/mm )
2349 ⫾ 369
⫺62 ⫾ 233 (.11)
⫺4.0 ⫾ 12.6
2315 ⫾ 318
0 ⫾ 188 (1.00)
⫺0.3 ⫾ 8.5
Hexagonality (%)
49.8 ⫾ 5.2
⫺0.8 ⫾ 7.6 (.51)
⫺3.3 ⫾ 17.3
51.0 ⫾ 7.0
⫺0.2 ⫾ 8.2 (.88)
⫺2.0 ⫾ 8.2
Cell area (m2)
441 ⫾ 94
18 ⫾ 56 (.05)
2.7 ⫾ 10.0
444 ⫾ 82
Coefficient of variation
0.23 ⫾ 0.04
0.01 ⫾ 0.06 (.63)
2
⫺1.5 ⫾ 23.4
0.24 ⫾ 0.06
2 ⫾ 37 (.79) ⫺0.02 ⫾ 0.05 (⬍.01)
0.0 ⫾ 8.4 ⫺10.4 ⫾ 18.9
Means ⫾ SD
Figure 3. (Kiss) Correlation between acute postoperative change in central corneal thickness (CT) and change in endothelial cell density (CD) in the low-cost group (cCD; cCT) (upper) and the expensive group (eCD; eCT) (lower) (n ⫽ 32) (d ⫽ day; m ⫽ month). 738
with Viscoat. In our study, we observed no significant differences in endothelial cell density or other cell size and shape parameters between groups. In contrast to the studies mentioned, our study used a randomized “bilateral” study design with intraindividual comparison between eyes. Observations of the correlation of cell loss with total phacoemulsification time and energy have been contradictory. Some studies report that cell loss after phacoemulsification is greater than after intracapsular or extracapsular cataract extraction (ECCE) and that the cell loss increases with prolonged phacoemulsification time.41– 46 Other investigations could not confirm a correlation.47 In our study, phacoemulsification time was equal in both groups; therefore, we did not expect that this parameter would influence the results in either group. Postoperative changes in corneal endothelial cell loss have been reported to be correlated with CT.48 We found no correlation in either group. In studies of irrigating solutions used during phacoemulsification cataract surgery, BSS Plus caused significantly less corneal swelling on the first postoperative day than citrate–acetate bicarbonate solution17 or Ringer’s solution.49 A study of corneal endothelial cell size preoperatively and 2 months after ECCE and IOL implantation showed a nonstatistically significant trend in favor of BSS Plus over dextrose bicarbonate lactated Ringer’s solution.50 Araie15 suggests that BSS Plus and glutathione bicarbonate Ringer’s solution are less harmful to the endothelial barrier function than a citrate–acetate bicarbonate solution. To date, there are no observations of changes in endothelial cell size or hexagonality with re-
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spect to different irrigating solutions.18 Our study indicates that different combinations of viscoelastic materials with Ringer’s solution or BSS Plus do not cause significant differences in the acute change in CT and only a slight change in the recovery of corneal swelling resulting from a marginally higher change from baseline to 3 months postoperatively in the Ringer’s solution and Ocucoat group. No difference in endothelial cell parameters between the 2 irrigating solutions was observed. In our study, there was no significant difference in acute corneal endothelial swelling between the expensive combination and the low-cost combination. Surgery was performed by 1 experienced surgeon who attempted to reduce turbulence in the anterior chamber as much as possible. A less experienced surgeon might have induced more stress on the corneal endothelium. All our patients had a corneal cell density within the normal range. Dispersive viscoelastic materials such as Viscoat may still be the first-line agent in patients with cornea guttata. We have not compared endothelial cell protection with these 2 combinations in patients with compromised endothelial cell counts. In conclusion, with respect to CT, Viscoat and BSS Plus, the more expensive combination, might be marginally more effective in helping the eye recover from corneal stress. The low-cost combination, Ocucoat and Ringer’s solution, was similar to the more expensive combination with regard to acute corneal swelling and changes in corneal endothelial cell function and morphology during small-incision cataract surgery with foldable IOL implantation in patients with normal endothelial cell counts.
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