Volume 144, Issue 3 , Pages 341-346, September 2007
Changes in Corneal Hysteresis After Clear Corneal Cataract Surgery
Article Outline
Purpose
To assess the changes in corneal hysteresis (CH) as measured by the Ocular Response Analyzer (ORA; Reichert Ophthalmic Instruments, Buffalo, New York, USA) to describe the influence of clear corneal cataract surgery on corneal viscoelastic properties and intraocular pressure (IOP) measured by noncontact tonometry (NCT) and Goldmann applanation tonometry (GAT).
Design
Retrospective, interventional, comparative study.
Methods
One hundred and one eyes of 101 consecutive patients who underwent routine clear corneal cataract surgery were evaluated. CH, NCT, and central corneal thickness (CCT) were measured by ORA before surgery and at postoperative day 1. A control group of 48 pseudophakic eyes (surgery >3 months previously) was included.
Results
CCT increased from 556.82 ± 32.5 μm before surgery to 580.26 ± 45.5 μm after surgery (P < .001; control, 555.16 ± 42.33 μm). Mean CH decreased from 10.35 ± 2.5 mm Hg before surgery to 9.20 ± 1.9 mm Hg after surgery (P < .001; control, 10.47 ± 1.63 mm Hg). NCT values rose from 17.85 ± 3.8 mm Hg before surgery to 20.10 ± 6.3 mm Hg after surgery. GAT values were 14.85 ± 2.8 mm Hg before surgery and 15.24 ± 4.1 mm Hg after surgery (P = .52). There was no significant difference of CCT or CH between the preoperative values and the values of the control group (CCT, P = .986; CH, P = .166), in contrast to the difference between postoperative values and the values of the control group (CCT, P = .005; CH, P = .031).
Conclusions
At day 1 after clear corneal cataract surgery, CH is diminished, whereas CCT is increased significantly. Postoperative corneal edema leads to a change of corneal viscoelastic properties, resulting in a lower damping capacity of the cornea. It is supposed that GAT and NCT measurements are significantly different because of postoperative changes in viscoelastic properties of the cornea.
Viscoelastic properties of the cornea currently are believed to have a major influence on tonometry. Therefore, diagnosing and monitoring glaucoma has been reviewed and new concepts have been proposed.1, 2, 3, 4, 5, 6, 7, 8 Up to now, corneal biomechanical properties have not been well understood. Therefore to date, central corneal thickness (CCT) is taken into account as the only parameter for corneal rigidity that can be determined in vivo.
Ideally, in elastic materials strain (deformation) is directly proportional to stress (applied force) and independent of the rate at which the force is applied. In contrast, in viscous materials, the relationship of strain and stress depends on the rate of deformation. In nature, there is hardly any ideal elastic material; viscous properties will always influence reactions on stress. Corneal hysteresis (CH) is described as the viscous damping because of the viscoelastic resistance of the cornea to a deformation pulse by an air puff of the tonometer. CH is measured by the Ocular Response Analyzer (ORA; Reichert Ophthalmic Instruments, Buffalo, New York, USA) using a patented dynamic bidirectional applanation process.9 It uses a rapid air puff to apply force to the cornea. With an electrooptical system, the corresponding deformation of the cornea is detected. The air pulse causes the cornea to move inward to pass a definite point of applanation and into a slight concavity. When the pressure of the air pulse decreases, the cornea returns to its normal configuration, passing a second time the definite point of applanation. The difference of these two pressure values at the definite point of applanation during the inward and outward movement is called corneal hysteresis. Because the ORA is a sophisticated noncontact tonometer (NCT), the average of these two pressure values is given as the NCT intraocular pressure (IOP) value.
The aim of the study was to investigate the effect of routine clear corneal cataract surgery on corneal viscoelastic properties determined by CH. Furthermore, the results of different IOP readings (NCT and Goldmann applanation tonometry [GAT]) in relation to postoperative changes of CCT and CH were analyzed.
Methods
Clinical Examination and Clear Corneal Cataract Surgery
Measurements with the ORA, ultrasonic pachymetry, and GAT of 101 eyes of 101 consecutive patients who underwent routine clear corneal cataract surgery were analyzed before surgery (within two weeks ahead of surgery) and on the first postoperative day. Each clinical examination consisted of visual acuity, GAT, biomicroscopy of the anterior and posterior segment, and ORA examination. GAT was measured once in each eye by experienced ophthalmologists (A.H., K.L., M.-O.F., and B.S.). ORA examination was performed four times; the average values were taken for statistic evaluation. Out of scale values were abandoned, as were measurements that could not be repeated three times.
Tonometry and ORA measurements were carried out within an interval of 10 to 45 minutes during regular office hours between 8 am and 4 pm, mostly in the morning hours until noon. Ultrasonic pachymetry (20 MHz) was performed with the ORA integrated hand-held pachymeter. Each of our patients underwent routine clear corneal cataract surgery by four different experienced surgeons (A.H., B.S., and W.W.). The surgeons used identical materials as far as the intraoperative use of viscoelastic materials (hydroxypropyl methylcellulose), knives (NanoEdge, phaco slit-knife angled, bevel up, 2.85 mm; Geuder AG (Heidelberg, Germany) and ShortCut Implant knife, 4.1 mm angled; Alcon, Inc, Hemel Hempstead, Herts, United Kingdom), and the type of the foldable intraocular lens (AcrySof; Alcon Pharma GmbH, Freiburg, Germany; Alcon, Inc) as well as the manner of implanting is concerned. A clear corneal incision was performed parallel to the limbus diagonally through the cornea and entered the anterior chamber at a distance of approximately 1.5 mm from the limbus and approximately 5.5 mm from the center of the cornea.
Control Group
As a control group, we analyzed the data of 48 eyes of 48 pseudophakic patients who had undergone clear corneal cataract surgery at least three months ahead of the ORA examination.
Statistical Analysis
The two-sample Wilcoxon (or Mann–Whitney U) test for nonparametric numbers was used for determining whether the values of a particular variable differ between two groups. The bivariate correlation procedure was accomplished for nonparametric numbers, resulting in the Spearman R coefficient. Statistical analyses were performed using SPSS software version 12.0 (SPSS, Inc, Chicago, Illinois, USA). A P value less than .05 was considered to be statistically significant.
Results
We examined 101 eyes of 101 consecutive patients (55 female, 46 male); mean age was 71.3 ± 8.5 years (95% confidence interval [CI], 54.6 to 88.0 years). Fifty right and 51 left eyes were operated on and analyzed. CCT increased from 556.82 ± 32.5 μm before surgery (95% CI, 493.1 to 620.5 μm) to 580.26 ± 45.5 μm after surgery (95% CI, 491.1 to 669.4 μm). The mean CH decreased from 10.35 ± 2.5 mm Hg before surgery (95% CI, 5.36 to 15.33 mm Hg) to 9.20 ± 1.9 mm Hg after surgery (95% CI, 5.41 to 12.99 mm Hg). NCT values rose from 17.85 ± 3.8 mm Hg before surgery (95% CI, 10.4 to 25.3 mm Hg) to 20.10 ± 6.3 mm Hg after surgery (95% CI, 7.66 to 32.45 mm Hg). GAT values were 14.85 ± 2.8 mm Hg before surgery (95% CI, 9.30 to 20.41 mm Hg) and 15.24 ± 4.1 mm Hg after surgery (95% CI, 7.28 to 23.20 mm Hg).
Significant differences between preoperative and postoperative values were found for CCT, CH, and NCT IOP values (P < .0001, Wilcoxon test; FIGURE 1, FIGURE 2, FIGURE 3). GAT was the only parameter that did not show any significant differences (P = .520, Wilcoxon test) in the preoperative and postoperative examination (Figure 3). Neither in the preoperative group nor in the control group was a correlation between age and CCT (P = .662 and .260, respectively) or CH (P = .931 and .622, respectively).
FIGURE 1.
Graph showing central corneal thickness before surgery (CCT preoperative) and on the first postoperative day (CCT postoperative) after clear corneal cataract surgery as well as CCT of the pseudophakic control group (CCT intraocular lens [IOL]). Mean values with 95% confidence interval (CI) are given in micrometers.
FIGURE 2.
Graph showing corneal hysteresis before surgery (CH preoperative) and on the first postoperative day (CH postoperative) after clear corneal cataract surgery as well as corneal hysteresis of the pseudophakic control group (CH intraocular lens [IOL]). Mean values with 95% confidence interval (CI) are given in millimeters of mercury (mm Hg).
FIGURE 3.
Graph showing noncontact tonometry (NCT intraocular pressure [IOP]) and Goldmann applanation tonometry (GAT) values before surgery (preoperative) and on the first postoperative day after clear corneal cataract surgery. Mean values with 95% confidence interval (CI) are given in millimeters of mercury (mm Hg).
NCT measurements of IOP as measured by the ORA instrument were higher than GAT values in each group (P < .0001, Wilcoxon test; Figure 3). Correlations between CH and the measurements obtained with GAT were not statistically significant in any of the groups (before surgery, P = .596, r = −0.066; control, P = .163, r = 0.205; postoperative day one, P = .06, r = −0.206). Correlations between CH and NCT measurements were not significant in the preoperative (P = .118, r = −0.157) and control (P = .973, r = 0.005) groups, but were significant at postoperative day 1 (P = .002, r = −0.302). In the preoperative and control groups, CH was related significantly to CCT (P = .001, r = 0.324; P = .001, r = 0.5, respectively). In contrast, at postoperative day one, CH was not related to CCT (P = .768, r = 0.03).
Mean CCT of the pseudophakic control group was 555.16 ± 42.33 μm (95% CI, 472.20 to 638.13 μm). CH was 10.47 ± 1.63 mm Hg (95% CI, 7.28 to 13.66 mm Hg). Statistical analysis using the Wilcoxon test showed no significant differences between our preoperative values and the values of the pseudophakic group (CCT, P = .986; CH, P = .166), in contrast to the difference between our postoperative values and the values of the pseudophakic group (CCT, P = .005; CH, P = .031), which is statistically significant.
Discussion
The biophysical factors that contribute to rigidity and elasticity of the cornea in vivo, that is, the factors that maintain the corneal shape, are not well understood. Among others, CCT has been assumed to be a major factor for corneal rigidity, and it is the only parameter that can be measured easily and in vivo up to now. With the ORA, a new metric, the CH, can be determined and its influence may be analyzed.
Our measurements were carried out during regular office hours between 8 am and 4 pm. They were performed within an interval of approximately 10 to 45 minutes between GAT and ORA measurement. Laiquzzaman and associates have shown that CH and CCT do not depend on diurnal variation, and IOP seemed to vary independently of variations in CH or CCT.10 Kida and associates affirmed that 24-hour changes in CH were not significant.11 Neither Luce nor Laiquzzaman and associates could not show differences between the right and left eye.9, 10 Therefore, we analyzed all eyes without differentiation, but included only one eye of each patient in this analysis.
The type of intraoperative clear corneal incision may be a confounding factor for corneal edema, and thus possibly for changes of CH. Therefore, we included only eyes that were operated on by four surgeons who have been trained the same way and used the same materials and knives during surgery. Because it has been shown that CCT increases after clear corneal cataract surgery,12 we wanted to find out about the influence of increased postoperative CCT on CH and on NCT as measured by the ORA in comparison with GAT.
CCT
In our group, CCT increased significantly from 556.82 ± 32.5 μm before surgery to 580.26 ± 45.5 μm at postoperative day 1 after clear corneal cataract surgery, as was shown in an earlier publication.12 Corneal edema seems to be the major cause for increasing CCT after clear corneal surgery, which normalizes thereafter. Falkenberg and associates showed that CCT increased by an average of 37 μm at postoperative day 1 and decreased within an average follow-up of 27 weeks after surgery back to preoperative values using the noncontact method of Orbscan (Bausch & Lomb; GmbH, Feldkirchen, Germany) pachymetry.12
For CCT measurements, we used the integrated handheld ultrasonic pachymeter of the ORA. It is certainly not possible to measure CCT in exactly the corneal apex and at the same location every time. It is doubtful, however, whether this would produce any significant bias because multiple readings (n = 2,500) were taken each time. Furthermore, the significant increase of CCT on the first postoperative day has been shown with Orbscan pachymetry as well.12
CH
CH, in contrast, decreased significantly from before surgery, 10.35 ± 2.5 mm Hg, to 9.20 ± 1.9 mm Hg at postoperative day 1. Our preoperative values and the values of the pseudophakic control group did not differ significantly, in contrast to the group at postoperative day 1, so that we assume this change in CH to be temporary because of clear corneal surgery.
There is a range of average values of CH in a normal population found in literature so far: 9.6 mm Hg in 339 normal eyes with a mean age of 28 years,9 10.6 ± 2.29 mm Hg in 156 normal eyes,13 and in diurnal variation values between 12.2 and 12.7 mm Hg in normal eyes (n = 42).10 Therefore, the mean CH of our preoperative group and the control group seems to be within this normal range, whereas the postoperative value is clearly below normal CH values. Nevertheless, it is not as low as the mean CH of glaucoma patients, which was 8.8 ± 2.1 mm Hg in 48 eyes.14 The impact of lower CH values on clinical work is not completely understood. Congdon and associates showed that lower CH values are associated with progressive visual field worsening in glaucoma patients.15 Patients with Fuchs dystrophy as well as patients who have undergone laser in situ keratomileusis (LASIK) have lower CH values that do not depend on CCT. Those corneas are called compromised corneas; that is, the ability of those corneas of damping the pressure impulse is reduced.9 Pepose and associates demonstrated in patients with post-LASIK corneas that CH and corneal resistance factor (CRF) declined.16 Lu and associates showed that in soft contact lens wearers, CCT increased by a mean of 13.1% ± 2.2% immediately after lens removal.17 However, CH was not associated with corneal swelling induced by soft contact lens wear in this group.
The structurally altered cornea is compromised in its viscoelastic properties because of edema after cataract surgery, as demonstrated by reduced CH. Assuming that changes in CH are dependent not only on CCT, structural changes of the cornea may be better identifiable using the measurement of CH.
IOP Values
Accurate measurement of IOP is a fundamental parameter in any ophthalmologic examination. Over the past four decades, GAT has become the standard for routine measurement of IOP, because the method has proven to be robust and easy to use with low intraobserver and interobserver variability.18, 19 However, the accuracy of GAT depends on many factors, including corneal thickness, corneal curvature, and corneal structure.1, 4, 5, 6, 7, 19, 20, 21, 22 In particular, CCT has been shown to have a substantial effect on IOP readings obtained with the GAT.1, 4, 5, 20 It is recommended that not only the GAT readings but also CCT need to be recorded for a glaucoma workup to define a target IOP.1, 2, 4, 5, 6, 8, 20 However, this requires a reliable nomogram to convert GAT readings and CCT into true IOP values. Several nomograms for adjusting GAT readings in normal eyes with varying inborn CCT values1, 4, 7, 20 have been published, but so far, none seems to be satisfactory.2, 8, 23 Results of intracameral measurements are contradictory.4, 7
Furthermore, the results of different methods of IOP measurement differ significantly.16, 18, 19, 20, 22, 24 Draeger and associates showed differences between NCT and GAT readings increasing with higher IOP values.25 The difference between these two methods is even higher in patients with higher CCT, that is, inborn CCT that is not associated with structural alterations of the cornea.19, 22 Medeiros and Weinreb examined 153 subjects with ORA and GAT and showed that NCT IOP as measured by the ORA was higher than GAT.26 Martinez-de-la-casa and associates demonstrated in 48 glaucomatous eyes that both ORA pressure measurements (clear corneal IOP (IOPcc); i.e., IOP adjusted by CH measurement and NCT IOP) overestimate IOP compared with the GAT readings.14 Furthermore, they showed that the discrepancy between the two instruments became more relevant the higher the GAT IOP was and that both ORA readings seemed to be affected by CCT as well.
Interestingly, in our patients, GAT measurements did not show significant differences in the preoperative and postoperative group; that is, the statistically significant change in CCT in the preoperative and postoperative group did not influence GAT measurements. CCT rose by an average of 23 μm because of postoperative edema. Slopes between GAT and CCT show a regression between 0.19 and 0.32 mm Hg/10 μm CCT.1, 5, 6, 8, 21 However, this is valid for inborn differences of CCT. Even if these slopes also were true for structurally altered corneae, like the post–cataract surgery cornea in our group, the difference of 23 μm would be clinically negligible because the corresponding difference in pressure would not be detectable by GAT. In contrast, NCT IOP values as measured by the ORA rose significantly (P < .0001) after cataract surgery, which we assume to be because of reasons other than simply the increase of CCT after surgery.
The cornea as a viscoelastic structure contains a component of static resistance and a component of dynamic resistance. The response of the cornea to an applied force such as tonometry depends on the magnitude of the force and on the rate of change of the force. The principle of GAT has been described by Goldmann and Schmidt.19 Because of the relatively slow deformation of the cornea by the Goldmann tonometer (approximately two seconds), static resistance seems to dominate the process of GAT. Noncontact tonometers like the ORA induce corneal applanation by a very short air impulse that deforms the cornea by 4.0 μm. The change of corneal reflexes is detected by optical systems and the IOP value is generated by analyzing the time needed to applanate. Because of this very short time required (less than five milliseconds) in contrast to the much longer time needed for applanation tonometry (two seconds), dynamic resistance of the cornea may play a major role in NCT. This dynamic resistance is dominated by elastic properties of the cornea that is emphasized by reduced corneal hysteresis and also may depend on CCT more than static resistance does.
The change of viscoelastic properties of the cornea by clear corneal cataract surgery has been shown by a significant increase in CCT and a decrease in CH. Thus, structural differences and changes in the viscoelastic properties of the cornea may be brought out better by measuring CH instead of CCT.
The authors indicate no financial support or financial conflict of interest. Involved in design of study (A.H., W.W.); conduct of study and collection of the data (A.H., K.L., B.S., M.O.F.); management, analysis, interpretation of the data (A.H., M.G., B.S., W.W.); preparation, review of the manuscript (A.H., M.G., W.W.); critical revision of the article, statistical expertise (A.H., B.S., M.G., W.W.); approval of the manuscript (all authors); and administrative, technical, and logistic support (W.W.). The study was conducted in conformity with all laws, and institutional board approval was obtained. Research adhered to the tenets of the Declaration of Helsinki.
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PII: S0002-9394(07)00489-8
doi:10.1016/j.ajo.2007.05.023
© 2007 Elsevier Inc. All rights reserved.
Volume 144, Issue 3 , Pages 341-346, September 2007
