Glaucoma is the leading cause of irreversible blindness in

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1 CLINICAL SCIENCE Determinants of Postoperative Corneal Edema and Impact on Goldmann Intraocular Pressure Yuqiang Huang, MBBS,* Mingzhi Zhang, MD,* Chukai Huang, MBBS,* Bin Chen, PhD,* Dennis S. C. Lam, MD, FRCS,* Shaobin Zhang, MD,* and Nathan Congdon, MD, MPH* Purpose: Recent studies report that increased corneal edema because of contact lens wear under closed lids is associated with elevated Goldmann intraocular pressure (GAT IOP). We sought to assess whether the impact of postoperative corneal edema on GAT IOP would be similar and to determine the differential effect of different amounts of edema. Methods: The setting is a tertiary level cataract clinic in Shantou, China. Pre- and postoperative (day 1) GAT IOP, central corneal thickness (CCT), corneal hysteresis, corneal resistance factor, and radius of corneal curvature were measured for consecutive patients undergoing phacoemulsification surgery by 2 experienced surgeons. Corneal edema was calculated as the percentage increase in CCT. Results: Among 136 subjects (mean age, years; 53.7% women), the mean increase in CCT was 10.3% postoperatively. Greater corneal edema was associated with lower GAT IOP in unadjusted analyses (P, 0.03) and in linear regression models (P, 0.01). In the model, higher corneal resistance factor (P, 0.001), lower corneal hysteresis (P, 0.001), and steeper radius of corneal curvature (P, 0.001) were associated with higher GAT IOP. Among subjects with edema, the median, edema was associated with lower GAT IOP (P = 0.004), whereas among those with edema $ the median, edema was not associated with GAT IOP. An increase in CCT of 7% was associated with an 8 mm Hg underestimation of GAT IOP in our models. Conclusions: The effect of postoperative edema on GAT IOP seems to be the opposite of contact lens induced edema. The magnitude of the effect is potentially relevant to patient management. Received for publication April 5, 2010; revision received October 16, 2010; accepted October 23, From the *Joint Shantou International Eye Center of Shantou University and The Chinese University of Hong Kong, Shantou, China; and Department of Ophthalmology and Visual Sciences, The Chinese University of Hong Kong, Hong Kong, China. Supported by the Joint Shantou International Eye Center and The Chinese University of Hong Kong. The Ocular Response Analyzer used in this study was loaned free of charge by Reichert Ophthalmic Instruments. Dr. Congdon has received travel support from the Reichert Ophthalmic Instruments. The authors state that they have no proprietary interest in the products named in this article. Reprints: Mingzhi Zhang, Joint Shantou International Eye Center, Dongxia North Rd, Shantou, Guangdong, China ( zmz@jsiec.org). Copyright Ó 2011 by Lippincott Williams & Wilkins Key Words: corneal hysteresis, central corneal thickness, corneal edema, intraocular pressure (Cornea 2011;00: ) Glaucoma is the leading cause of irreversible blindness in the world, estimated to affect 60.5 million persons bilaterally. 1 Currently, the only proven method to reduce the risk of glaucoma 2 and glaucoma progression 3 is to lower intraocular pressure (IOP). Assessment of the success of pressure-lowering therapies is dependent on the accurate measurement of IOP, accomplished in many clinical settings through applanation of the cornea. Such measurements are susceptible, however, to inaccuracies because of variations in corneal parameters, among other factors. It has been recognized for decades that greater central corneal thickness (CCT) can lead to overestimation of the IOP. 4 Corneal biomechanical factors, such as viscoelasticity, also seem to play a role. Examples of such factors are corneal hysteresis (CH), which reflects the viscous or energy-damping properties of the cornea, and corneal resistance factor (CRF), an indicator of the cornea s elastic properties. 5 Reduction in these values may be associated with artificially low measured IOP during Goldmann applanation tonometry (GAT). 6 Several different devices have been designed and tested to decrease the impact of corneal parameters on measured IOP 7, but at the current time, GAT remains the most widely used modality. Corneal edema is a frequently encountered clinical entity, whereby fluid buildup occurs in the stroma or epithelium because of a variety of causes, such as failure of the endothelial pump mechanism. Conceptually, the potential impact of corneal edema on measured IOP is somewhat complex: although the CCT is increased, potentially increasing measured IOP, hydration of the epithelium, or stromal matrix may also reduce corneal stiffness, potentially lowering IOP measured by applanation. A number of investigators have attempted to assess the impact of isolated acute increase in corneal edema on measured IOP, most commonly through short-term wear of contact lenses under closed lids over a period of hours. Such studies have generally reported an increased CCT in the range of 10%, with observed increases in GAT IOP of approximately 2 mm Hg, significantly correlated with the amount of edema, calculated as percentage change in CCT However, reductions in GAT IOP, 12 and IOP by other pressure-measuring modalities, 11 have not been reported as frequently. The model of contact lens induced edema has the advantage of being rapid and easy to implement and of Cornea Volume 00, Number 0, Month

2 Huang et al Cornea Volume 00, Number 0, Month 2011 provoking an isolated increase in edema without presumably affecting the biomechanical structure of the cornea in significant ways. However, it is not clear that observations derived from this model are applicable to the common clinical situation of edema resulting from phacoemuslification surgery, where accurate measurement of IOP may be crucial for certain vulnerable patients. The phenomenon of acute corneal edema resulting from endothelial impairment after cataract surgery has been studied. 13,14 However, because of possible surgically induced changes in the IOP, the potential impact of edema on measured IOP in this setting can only be examined by assessing the correlation between change in CCT and postoperative IOP, which, to our knowledge, has not been done in published studies. We studied the changes in CCT, IOP, and other corneal and ocular biometric properties of the eye in a consecutive series of Chinese patients undergoing clear corneal phacoemulsification by 2 experienced surgeons. The principal aims of the current investigation are as follows: 1. To study the determinants of postoperative corneal edema (measured as % change in CCT) and its impact on GAT IOP. 2. To examine the hypothesis that the association between edema and measured IOP may be nonlinear, differing in amplitude and possibly direction depending on the amount of edema. METHODS Subjects were recruited for the current study from consecutive patients undergoing phacoemulsification cataract surgery by 2 experienced surgeons (M.Z. and S.Z.) at the Joint Shantou International Eye Center in Shantou, Guangdong, China. The following persons were excluded: subjects with previous ocular surgery including refractive surgery, simultaneous surgery for glaucoma or other conditions, and preexisting corneal abnormality because of infection, trauma, or other causes. Written informed consent was obtained from all subjects; the protocol was approved in full by the Ethics Committee at the Joint Shantou International Eye Center; and the study was conducted in accord with the tenets of the Declaration of Helsinki. Patient age and sex, the presence or absence of diabetes, endothelial cell count, best-corrected preoperative vision in the operative eye, and surgical parameters (location of wound, phacoemulsification time, and energy) were obtained from clinical records. At the time of the last preoperative visit, usually within 1 week of surgery, the following data were collected for the operative eye only: 1. Lens Opacity Classification System III cataract grading 15 of nuclear opalescence at the slit lamp by a single observer (Y.H.). 2. CH and CRF ½ocular response analyzer (ORA); Reichert Ophthalmic Instruments, Depew, NYŠ. A minimum of 3 measurements with desirable curves were made for each subject, and the mean for IOP, CH, and CRF each was calculated. The ORA determines IOP, CH, and CRF during rapid motion of the cornea in response to a short-duration (20 milliseconds) air impulse. These cause the cornea to move inward, through applanation, and into slight concavity. Subsequently, the air pump shuts off, and the cornea moves through a second applanation while returning from concavity to its normal convex curvature. The pressure values at the inward and outward applanation event times are averaged to give the ORA reading of IOP (denoted IOPg or Goldmann IOP ), whereas the value for CH, in mm Hg, is the difference between the 2 pressures. The CRF is derived from the formula (P 1 2 kp 2 ), where k is an empirical constant. A second measure of IOP is also calculated from P 1 and P 2, with P 2 multiplied by a constant k, chosen empirically to reduce the impact of corneal effects; this is denoted IOPcc or cornealcorrected IOP. The current report gives values only for IOPcc, to avoid any confusion between GAT and the ORA-derived Goldmann IOP. After measurements with the ORA, a single drop of proparacaine 1% (Alcaine; Alcon Laboratories, Fort Worth, TX) was placed in the eye, and ultrasonographic measurement of the axial length (AL), anterior chamber depth, and lens thickness (LT) was carried out (Cine Scan; Quantel Medical, Clermont-Ferrand, France). Five measurements were made, and the mean of each value was calculated and recorded. The CCT was measured ultrasonically (IOPac 20 MHz Pachymeter; Reichert Ophthalmic Instruments). A total of 10 measurements were made for each eye, with additional measurements obtained if the SD exceeded 10 mm. Vertical and horizontal radii of corneal curvature were assessed (RK-F1 Full Auto Refractor-Keratometer; Canon, Inc, Tokyo, Japan) as the median of 5 measurements. Finally, after application of topical fluorescein dye, GAT was used to measure the IOP, recorded as the mean of 3 measurements. On the first postoperative day, the following measurements were repeated, in this order: CH, CRF, GAT IOP, radius of corneal curvature, and CCT. Statistical Methods Statistical analysis was performed using the SPSS 15.0 for Windows software (SPSS, Inc, Chicago, IL). Significance of differences in the pre- and postoperative values for GAT IOP, IOPcc, CH, CRF, and CCTwere analyzed using the paired t test and Hotelling T 2 test. Postoperative corneal edema was calculated as the percentage increase in CCT using the following formula: CCT postoperative CCT preoperative CCTpreoperative 3100 Linear regression analysis was used to model univariate and multivariate associations between corneal edema and various potential predictors, including age, sex, diabetes status, preoperative corneal parameters (radius of corneal curvature, endothelial cell count, CCT, CH, and CRF), preoperative ultrasonic biometry (AL, anterior chamber depth, and LT), and operative parameters (wound location and phacoemulsification time and energy). Age, sex, and all other parameters with a P value # 0.15 in the univariate analysis were included in the multivariate model. A linear regression model was created for postoperative GAT IOP, transformed logarithmically to correct for a non normal distribution, and using the following potential explanatory variables: age, sex, diabetes status, change in CCT, postoperative corneal parameters (CCT, CH, CRF, radius 2 q 2011 Lippincott Williams & Wilkins

3 Cornea Volume 00, Number 0, Month 2011 Effect of Postoperative Edema on GAT IOP of corneal curvature, and wound location), and preoperative AL. Finally, to explore our hypothesis that the impact of edema on IOP might differ with different levels of edema, this model was applied separately for subjects having calculated edema values above and below the median (a 9.5% increase in CCT). A 2-tailed P value of, 0.05 was considered significant. RESULTS Among 136 participants in the current study, the mean age was years, 53.7% (73 of 136) were women and 10.3% (14 of 136) had been diagnosed with diabetes (Table 1). The mean preoperative best-corrected visual acuity of participants was (minimum angle of resolution, approximately equivalent to 6/48). Additional biometric data and clinical information on subjects cataracts and cataract surgery are given in Table 1. At the time of examination on postoperative day 1, subjects mean CCT had increased from a preoperative value of to mm, a mean increase of 10.3% TABLE 1. Baseline Demographic, Clinical, and Operative Characteristics of 136 Chinese Subjects Participating in a Study of Postoperative Corneal Edema and Intraocular Pressure Measurement Parameter Baseline Value Age (mean 6 SD) (yr) Sex, n (% female) 73/136 (53.7) Diabetes present, n (%) 14/136 (10.3) Right eye operated, n (%) 75/136 (51.1) Best-corrected preoperative visual (CF to 0.6) acuity, mean 6 SD (range) (logmar) Radius of corneal curvature (mean 6SD) (diopters) Vertical Horizontal Ultrasonic biometry, mean 6 SD (range) (mm) Anterior chamber depth ( ) Lens thickness ( ) Axial length ( ) LOCS III cataract grade, n (%) 0.1 to $ (14.7) $ (29.4) $ (35.3) $ (18.4) $5.0 1 (0.74) Missing 2 (1.48) Wound location, n (%) Superotemporal 16 (11.8) Superonasal 35 (25.7) Temporal 85 (62.5) Phacoemulsification (mean 6 SD) Time (s) Energy (W) All ocular parameters relate to the operative eye. CF, counting fingers; logmar, logarithm of the minimum angle of resolution (eg, the decimal equivalent of the Snellen fraction); LOCS, lens opacity classification system. (P, 0.001; median, 9.5%) (Table 2). Significant postoperative increases were also observed for Goldmann IOP (P, 0.001) and IOPcc, as measured by the ORA (P, 0.001), whereas CH declined significantly (P, 0.001). No significant change was observed in CRF postoperatively (P = 0.32) (Table 2). In multiple regression models of postoperative corneal edema (calculated as the % increase in CCT), edema was significantly greater among those with longer phacoemulsification time during surgery (P = 0.02) and with flatter corneas (P = 0.02). Persons with diabetes had significantly less corneal edema (P = 0.04) (Table 3). Age, sex, preoperative endothelial cell count, LOCS III nuclear cataract grade, LT, phacoemulsification energy, and cataract surgical wound location were not significantly associated with calculated corneal edema in either univariate or multivariate model (Table 3). Linear regression models were used to examine the impact of various potential predictors on postoperative GAT IOP (logarithmically transformed to correct for a non normal distribution). A higher CRF (P, 0.001), lower CH (P, 0.001), and steeper radius of corneal curvature (P, 0.001) were associated with a higher GAT IOP, whereas greater corneal edema was associated with a lower GAT IOP (P = 0.01) in multiple regression models (Table 4). We sought to examine our hypothesis that different levels of edema might impact differently on measured IOP. Among subjects with edema less than the median (percentage change in CCT, 9.5%), edema was significantly associated with a lower GAT IOP (P = 0.004), whereas among those with greater amounts of edema, corneal edema was not associated with GAT IOP (Table 5). DISCUSSION The purpose of the current study was to examine the impact of postoperative corneal edema on GAT IOP. Our results suggest that higher amounts of edema are consistently associated with lower measured IOP in the postoperative setting. This outcome is the opposite of that reported in a number of studies assessing the short-term impact of wearing soft contact lenses under closed lids. These studies have generally reported increasing IOP in the range of 2 mm Hg associated with the acute onset of edema, with the rise in IOP significantly correlated with percent change in CCT The amount of edema observed in these studies, an approximately 10% increase in CCT, is comparable to that seen in our study. However, our results are consistent with those reported by Simon et al, who carried out GAT measurements on cadaver eyes undergoing osmotically controlled hydration measured by pachymetry. They found that GAT readings were inversely correlated with change in corneal thickness, with a decrease of 9.2 mm Hg being observed between minimum and maximum hydration. 16 The reasons for these apparently contradictory results are not clear. Corneal edema in contact lens wear, especially with closed lids as in overnight wear, seems to result from breakdown of epithelial and endothelial barriers, reduction in epithelial and endothelial sodium potassium ATPase pump function, and increase in osmotic pressure because of buildup of lactate in the stroma. All these are ultimately the q 2011 Lippincott Williams & Wilkins 3

4 Huang et al Cornea Volume 00, Number 0, Month 2011 TABLE 2. Pre- and Postoperative Characteristics of 136 Chinese Subjects Participating in a Study of Postoperative Corneal Edema and IOP Measurement Characteristic Preoperative Value, Mean 6 SD (Range) Postoperative Value, Mean 6 SD (Range) P CCT (mm) ( ) ( ),0.001 CH (mm Hg) ( ) ( ),0.001 CRF (mm Hg) ( ) ( ) 0.32 IOP (ORA corneal-corrected ) (mm Hg) ( ) ( ),0.001 IOP (Goldmann) (mm Hg) (6 20) (5 29),0.001 All ocular parameters relate to the operative eye. consequence of corneal hypoxia, hypercapnia, and acidosis. 17 Inflammatory factors secreted by the epithelium may also play a role. 17,18 Edema after phacoemulsification surgery may be a consequence of the effects of irrigating solutions, air bubbles, and phacoemulsification energy on endothelial cells and the endothelial glycoprotein layer. 18 It is possible that the apparent differences in GAT IOP measurements on the edematous cornea, resulting from short-term contact lens wear versus phacoemulsification cataract surgery, may result from differences in the distribution of fluid in the cornea because of these different mechanisms. Changes in corneal biomechanical parameters, such as CH and CRF, observed in this and other studies can in principle lend insight into this hypothesis. However, direct comparison of corneal biomechanics during contact lens wear and after phacoemuslification is complicated by factors such as the presence of a surgical wound in the latter. We observed a statistically significant decline in CH in the immediate postoperative period, which is consistent with the findings of 2 other published studies of phacoemulsification-induced corneal edema. 13,14 However, unlike our study, Kucumen et al 14 measured declines in both CH and CRF 1 week postoperatively, at which time the increase in CCT over the preoperative value was only about 2%. CH and CRF values returned to preoperative levels over 3 months. These findings suggests either that small amounts of edema can exert a significant impact on corneal biomechanics (which is consistent with our findings) or that other surgically induced changes, such as the incision or removal of the crystalline lens, may also impact corneal biomechanics. The study of contact lensinduced edema by Lu et al 8 reported an increase in CRF and no significant difference in CH after contact lens wear, a very different profile from that observed in our own and other 13,14 studies of phacoemulsification. Further studies are needed to better understand the observed biomechanical differences between edema resulting from contact lens wear and that resulting from intraocular surgery. A secondary purpose of this study was to examine the hypothesis that different amounts of corneal edema might have different impacts on measured IOP. In fact, our results provide some evidence of a threshold effect. Among subjects having corneal thickening less than the median (approximately 9.5%), there was a significant inverse association between the amount of edema and GAT IOP, whereas above this level, no such TABLE 3. Linear Regression Model of Potential Predictors of Postoperative Corneal Edema* on Postoperative Day 1 After Phacoemulsification Cataract Surgery Among 136 Chinese Patients Univariate Analysis Multivariate Analysis Variable Beta P Beta P Age (yr) Female Diabetes present Vertical radius of corneal curvature (diopters) Preoperative Goldmann IOP (mm Hg) Preoperative CCT (mm) Preoperative CH (mm Hg) Preoperative CRF (mm Hg) Axial length (mm) Preoperative endothelial cell count Lens thickness (mm) Cataract grade Phacoemulsification energy (W) Phacoemulsification time (s) Temporal position of wound *Calculated as (postoperative CCT 2 preoperative CCT)/(preoperative CCT). 4 q 2011 Lippincott Williams & Wilkins

5 Cornea Volume 00, Number 0, Month 2011 Effect of Postoperative Edema on GAT IOP TABLE 4. Linear Regression Models Showing Potential Predictors of Postoperative Goldmann IOP* Among 136 Chinese Subjects on Postoperative Day 1 After Phacoemuslification Surgery Multivariate Model Including Univariate Model CH and CRF Variable Beta P Beta P Age (yr) Female Diabetic % Increase in CCT Postoperative CCT (mm) Postoperative CH (mm Hg) ,0.001 Postoperative CRF (mm Hg) 0.023, ,0.001 Vertical radius of corneal ,0.001 curvature (diopters) Axial length (mm) 0.016,0.001 Position of wound Phacoemulsification time *Log-transformed to create a normal distribution. association was observed. This finding is consistent with a model whereby modest amounts of corneal edema render the cornea softer or more compliant, but where once a certain reserve is exhausted, further increase in edema eliminate this effect. We observed significantly less corneal swelling among patients with diabetes as compared with those without diabetes. This is consistent with reports of significantly less contact lens associated corneal swelling in patients with diabetes as compared with normal controls and also less swelling in patients with diabetes during induced hyperglycemia than among the same subjects while euglycemic. 19 This may be due either to decreased endothelial permeability and/or decreased corneal lactate production (because of reduced anaerobic metabolic activity in the diabetic cornea). 19 Because hypoxia is not thought to play a role in phacoemulsificationinduced corneal edema, the former explanation may be more relevant to the results of the current study. The clinical implication of our main result is that GAT IOP measurements in the postoperative period tend to be artificially low in persons with corneal edema, potentially leading to clinically significant undertreatment of vulnerable individuals. The results of our regression models across the full range of observed edema indicate that a 10% increase in CCT because of edema might be associated on average with a 3 to 4 mm Hg underestimation of IOP. However, our models suggest that corneas with modest amounts of edema may actually be susceptible to an even greater degree of underestimation: an increase in CCT of 7%, for example, would be associated with an 8 mm Hg underestimation of IOP. This is comparable with the figure of 9 mm Hg reported by Simon et al 16 for cadaver eyes. This artificial undermeasurement of IOP after phacoemulsification because of corneal edema should be distinguished from a genuine long-term reduction in pressure of 2 to 3 mm Hg after cataract surgery. This phenomenon has been widely reported and seems to be due at least in part to deepening of the anterior chamber and widening of the angle. The results and implications of our study must be understood within the context of its limitations. Although the contact lens model of edema allows before and after measurements of IOP to be made and the impact of lens wear inferred directly, such before and after comparisons of IOP are unlikely to be meaningful in the setting of phacoemulsification, as too many other factors besides corneal swelling have been altered. We relied instead on the correlations between measurements of IOP and edema made cross-sectionally in the postoperative setting. Although inferences of causal associations based on cross-sectional measurements are inherently limited, it does not seem likely that lower pressure readings would have TABLE 5. Linear Regression Models Showing Potential Predictors of Postoperative Goldmann IOP* Among 136 Chinese Subjects on Postoperative Day 1 After Phacoemuslification Surgery Subjects With Corneal Edema,Median Subjects With Corneal Edema $Median Univariate Multivariate Univariate Multivariate Variable Beta P Beta P Beta P Beta P Age (yr) Female Diabetic % Increase in CCT Postoperative CCT (mm) Postoperative CH (mm Hg) , ,0.001 Postoperative CRF (mm Hg) 0.024, , ,0.001 Vertical radius of corneal curvature (D) Axial length (mm) 0.021, Temporal position of wound Phacoemulsification time Subjects divided into those with corneal edema, and $ to the median value. Corneal edema is calculated as (postoperative CCT preoperative CCT)/(preoperative CCT). *Log-transformed to create a normal distribution. q 2011 Lippincott Williams & Wilkins 5

6 Huang et al Cornea Volume 00, Number 0, Month 2011 caused edema, particularly because,5% of our subjects had postoperative IOP in the hypotonus range. Although it is true that factors such as retained viscoelastic and postoperative inflammation may affect IOP in this setting, such factors would in general tend to obscure rather than increase any apparent relationship between corneal edema and measured IOP. It is theoretically possible that increased phacoemulsification time could have confounded our results, leading to both increased corneal edema and increased ciliary body trauma/lower IOP, thus establishing a spurious relationship between the IOP and edema. However, our inclusion of phacoemulsification time in our models of potential determinants of measured IOP (Tables 4 and 5) makes this possibility less likely. In addition, we attempted to measure a variety of factors that might potentially confound the association between edema and measured IOP, such as history of diabetes and postoperative CH, CRF, and CCT. However, the possibility cannot be excluded that other important confounders were not assessed. As with the majority of other studies of corneal edema, we have relied on calculated estimates based on percentage change in CCT. Unlike some other recent reports, 8 we have not employed noncontact methods of assessing CCT. It must therefore be acknowledged that corneal deformations resulting from the use of a contact pachymeter likely led to some inaccuracy in our measurement of CCT and thus in our derived values for edema. Finally, we have not attempted to correlate our GAT IOP measurements with data based on cannulation pressure of the eye. The focus of the current investigation is not on assessing the true change in IOP between the operative and post-operative setting, but rather on elucidating factors affecting the measurement of IOP with GAT. The strength of this study lies in having assessed corneal edema, its determinants, and its effects on IOP in the clinically meaningful setting of phacoemulsification. We report results that are the opposite of those derived from more common studies of edema in the setting of contact lens wear 8 11 and have observed a magnitude of effect potentially relevant to patient management in the clinical setting. Further work will be required to provide clinicians with practical algorithms and devices to accurately and rapidly assess the likely impact of postoperative corneal edema on GAT IOP measurements in their patients. REFERENCES 1. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and Br J Ophthalmol. 2006;90: Kass MA, Heuer DK, Higginbotham EJ, et al. 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