Contact Lens & Anterior Eye

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1 Contact Lens & Anterior Eye 32 (2009) Contents lists available at ScienceDirect Contact Lens & Anterior Eye journal homepage: The use of the Ocular Response Analyser to determine corneal hysteresis in eyes before and after excimer laser refractive surgery Sunil Shah a,b,c, Mohammad Laiquzzaman a, *, Ian Yeung c, Xueliang Pan d, Cynthia Roberts e a Heart of England Foundation Trust, Solihull, UK b Ophthalmic Research Group, Aston University, Birmingham, UK c Midland Eye Institute, Birmingham, UK d Department of Statistics, The Ohio State University, Columbus, OH, USA e Department of Ophthalmology and Department of Biomedical Engineering, The Ohio State University, Columbus, OH, USA ARTICLE INFO ABSTRACT Keywords: CCT CH CRF IOPg IOPcc Purpose: To compare corneal biomechanical parameters and two measures of intraocular pressure (IOP) in eyes before and after excimer laser refractive surgery, with the Ocular Response Analyser (ORA). Materials and methods: Eighty normal eyes of 41 patients undergoing excimer laser refractive surgery in Birmingham, U.K. were recruited into three groups: Laser Assisted-Epithelial Keratomileusis (LASEK) (Myopes), Laser Assisted in Situ Keratomileusis (LASIK) (myopes) and LASIK (hyperopes). The preop and 3 months postop Goldmann correlated IOP (IOPg), corneal compensated IOP (IOPcc), corneal hysteresis (CH), and corneal resistance factor (CRF) were measured by the ORA. Central corneal thickness (CCT) was measured using ultrasonic pachymeter. The differences of the changes in IOPg, IOPcc, CH, CRF and CCT between the three groups were estimated. A General Linear Model was selected to investigate the influence of gender, age, initial conditions (CH, CRF, CCT, IOPcc and IOPg) and changes in CCT on the measured IOP. Results: The differences between the mean IOPg, CH and CRF after refractive surgery were statistically significant for all three groups. The hyperopic LASIK group had a significantly smaller change compared to the other groups (which had no statistical significance). The preop IOPg, preop CH and gender were significant predictors of the changes in measured pressure and biomechanical parameters after surgery in the myopic groups only. Conclusion: CH and CRF were found to decrease after both myopic and hyperopic refractive surgery. CH and CRF measurement may prove important tools to clarify the role of corneal biomechanics for refractive surgery. ß 2009 British Contact Lens Association. Published by Elsevier Ltd. All rights reserved. 1. Introduction The cornea is a largely transparent tissue that also serves as a very powerful optical lens [1] accounting for 70% of the total refractive power of the eye [2]. It forms a mechanically tough membrane. It is because of its mechanical strength and transparency that the cornea serves both as an efficient protective barrier and as a refractive lens. Various surgical procedures used for corneal refractive surgery result in substantial changes in corneal tissue structure that affect the central corneal thickness (CCT) and curvature [3 7]. Corneal refractive surgery can thus alter corneal biomechanical properties. * Corresponding author at: Midland Eye Institute, 50 Lode Lane, Solihull, West Midlands B91 2AW, UK. Tel.: ; fax: address: mohammadlaiquzzaman@hotmail.com (M. Laiquzzaman). There is evidence that the biomechanical properties of the cornea can influence the diagnosis and hence management of ocular disease(s), but the factors which influence these properties are not well understood and hence cannot be controlled without the knowledge and ability to measure the biomechanical properties in vivo [8]. An example is the validity of intraocular pressure (IOP) after refractive surgery [9]. With the ever increasing popularity of refractive surgery, the knowledge of the factors that determine the biomechanical properties of the eye and their importance in the management of disease process has gained importance. So far there has been no easy method reported to determine bio-mechanical corneal properties in vivo other than indirectly through CCT measurements. A recent addition to the armamentarium for assessing biomechanics has been the Ocular Response Analyser (ORA) [Reichert Ophthalmic Instruments, Buffalo, USA] which in addition to being a non-contact tonometer, measures new metrics referred to as corneal hysteresis (CH) which is said to be a /$ see front matter ß 2009 British Contact Lens Association. Published by Elsevier Ltd. All rights reserved. doi: /j.clae

2 124 S. Shah et al. / Contact Lens & Anterior Eye 32 (2009) measure of the visco-elastic properties of the cornea and corneal resistance factor (CRF) which is said to be a measure of elasticity. CH is the difference between the inward and outward applanation pressure. The air pressure pulse which impinges on the corneal surface is a precisely, metered ramp of air. If purely elastic, it would be expected that the cornea would applanate at the same pressure in both directions i.e. inward and outward; however, due to the visco-elastic properties of the cornea two different applanation pressures are noted. The CH is described as the loss or delay of energy due to resistance of the cornea to the air puff. Reichert believes that CRF derived in this process is dominated by the elastic properties of the cornea and appears to be an indicator of the overall resistance of the cornea [10]. This study focuses on the change in three corneal parameters, CH, CRF, CCT, as well as two measures of IOP, corneal compensated IOP (IOPcc) and Goldmann correlated IOP (IOPg), 3 months following corneal refractive surgery. This is the first study to address the differences in biomechanical properties in hyperopic eyes compared to myopic eyes following refractive surgery. 2. Materials and methods Eighty eyes of 41 patients (25 females and 16 males) were recruited for this study from the Midland Eye Institute, Solihull, U.K. The mean age was SD (age range years). All had normal eyes and no history of ocular disease, surgery or trauma. IRB approval was obtained from the Local Research Ethics Committee. These patients undergoing refractive surgery were divided into three groups: Laser Assisted-Epithelial Keratomileusis (LASEK) (Myopes), Laser Assisted in Situ Keratomileusis (LASIK) (myopes) and LASIK (hyperopes) based on refractive error, corneal thickness and patient and surgeon preference i.e. these were not randomised groups. A full assessment for refractive surgery including refraction, full ocular examination, topography, abberometry and pachymetry was performed. The ORA measurements were taken while the patient was seated in a standard fashion. The IOPg, IOPcc, CH and CRF were determined by the ORA. The CCT was measured using a hand held ultrasonic pachymeter (SP-2000, Tomey Corp, Japan) after instilling a drop of topical anaesthetic Proxymethacaine (Bausch & Lomb, Rochester, New York, USA) in the eye prior to performing pachymetry. The patient was asked to fixate at a target in order to minimise any eye movement, and to avoid damage to the corneal epithelium. The pachymeter probe was gently placed onto the mid-pupillary axis in a perpendicular orientation. Upon contact with the corneal surface, the CCT value was displayed on the monitor attached to the probe. Six readings were taken and the mean value was used as the CCT. These measurements were taken before and after refractive surgery in the same order to avoid any bias in the data collection. All the patients underwent LASEK or LASIK by one surgeon (SS). All surgery was uncomplicated. For LASEK, the cornea was anaesthetised by topical proxymethacaine. The patient was made to lie on the couch and asked to focus on a flashing light. A lid speculum was inserted to open the lids. A 9.0 mm alcohol well was applied and was filled with 18% ethanol and left for 30 s. An 8 mm epithelial flap was fashioned, and then laser was applied to the bare corneal stroma. For LASIK, the cornea was anaesthetised and a lid speculum inserted. The cornea was marked with gentian violet to help realign the flap. A suction ring was applied to the limbus and IOP increased to ensure a smooth cut. A NIDEK MK2000 automated microkeratome (Gamagori, Japan) was used to create a corneal stromal flap, and all flaps were cut to a nominal depth plate of 160 mm. The hinge was made nasally. Laser was applied to ablate the corneal stroma. After laser ablation, the stromal flap was replaced. Data were collected preoperatively and 3 months postoperatively following refractive surgery. For the data analysis, several computer packages were used, including Excel (Microsoft 1 inc.) and MINITAB 1 (Minitab Inc.). The changes of IOPg, IOPcc, CH, and CRF after surgery were compared between different groups of patients. ANOVA with post hoc test was performed for statistical analysis. The level of statistical significance level was chosen at In addition, the influential predictive variables were identified based on the best subset regression and general linear models from a group of predictor variables, such as age, gender, the initial conditions (preop CCT, preop IOPg and preop CH), and ablation (CCT difference), on the IOP and CH change (IOPg difference, IOPcc difference, CH difference, and CRF difference). To count for dependence between the two eyes of the same person in this study, we analysed the data based on two models; the simple model assuming the independence of eyes in that same patient and the nested model that counted for the dependence. While the p-values for the tests are slightly different, the conclusions of the significance are the same. For simplicity, only the results based on the simple models are reported. 3. Results The preop conditions of the patients from three different groups are summarised in Table 1. It is important to note that the three groups are not comparable (except for CRF) but this is to be expected as the corneal parameters were taken into account when choosing the appropriate procedure for the patients. There was no significant difference between the LASIK myopes and LASIK hyperopes (Fig. 1a and b). On average, the myopic LASIK eyes had 25 mm greater preop CCT, 0.9 mmhg higher preop CH and 0.5 mmhg higher preop CRF than the myopic LASEK eyes, as well as 0.9 mmhg lower preop IOPg, and 1.7 mmhg lower preop IOPcc. Fig. 2 shows the CCT before and after the surgery for three groups. The IOPg and CH changes after surgery for three groups of patients are shown in Fig. 3a and b. The changes of the CCT, IOPg, IOPcc, CH and CRF after refractive surgery are summarised in Table 2. The mean IOPg, CH and CRF after refractive surgery were statistically lower than their initial values for all three groups of patients. The Table 1 Initial characteristics of patients. Group n Age ** M/F Preop CCT ** (mm) Preop IOPg ** Preop CH ** Preop IOPcc ** Preop CRF 1. LASEK (myopes) / LASIK (myopes) / LASIK (hyperopes) / All / Means SDs; IOPg = (IOP1 + IOP2)/2. ** The initial value of CCT, IOPg and IOPcc are significantly different between three groups of patients (p-values are 0.006, 0.029, respectively), while age and initial value of CH are marginally different (p = 0.06 for both). The preop differences between the LASEK and the LASIK patients are statistically significant for all parameters. The preop differences between the LASIK myopes and LASIK hyperopes are not statistically significant for any parameter.

3 S. Shah et al. / Contact Lens & Anterior Eye 32 (2009) Fig. 2. Boxplot showing the CCT before and after the surgery for three groups. Fig. 1. (a) Boxplot showing the IOPg before surgery for the three groups of patients. (b) Boxplot showing the IOPcc before surgery for the three groups of patients. mean IOPcc, however, increased after surgery. While the myopic LASEK eyes and the myopic LASIK eyes have similar values in IOPg difference ( and respectively), CH difference ( mmhg and mmhg) and CRF difference ( mmhg and respectively) after surgery, the hyperopic LASIK eyes have statistically significantly smaller values of IOPg difference ( mmhg), CH difference ( mmhg) and CRF difference ( ) than the previous two myopic groups with p- values of 0.016, and respectively. There are many potential factors that may influence the IOPg difference, CH difference and CRF difference, such as surgery type (LASEK/LASIK), diagnosis (myopes/hyperopes) the initial conditions (preop IOPg, preop CCT, preop CH and preop CRF), ablation depth (CCT difference), age, and gender. Since the three groups are not comparable in terms of preop CCT, preop IOPg, preop CH and CCT difference (but were comparable for CRF), it is important to evaluate the influence of these four factors. Table 3 shows the correlation between these initial conditions that were statistically significantly Fig. 3. (a) Boxplot showing the IOPg changes after surgery for three groups of patients. (b) Boxplot showing CH changes after surgery for three groups of patients. Table 2 Changes in CCT, IOPg, hysteresis, IOPcc and CRF after surgery. Group n CCT difference ** IOP difference ** CH difference ** IOPcc difference CRF difference ** 1. LASEK (myopes) * * * * 2. LASIK (myopes) * * * * 3. LASIK (hyperopes) * * All * * Means SDs. For IOPg, CH, IOPcc and CRF, the differences are calculated as postop preop, for example, IOPg difference = postop IOP preop IOPg; for CCT, CCT difference = preop CCT postop CCT. * Denotes the value is statistically different from zero at 0.05 level. ** CCT difference, IOPg difference, CH difference, and CRF difference are significantly different among three groups (p = 0.001, 0.045, 0.006, and respectively); the differences were significant between myopes and hyperopes and insignificant between LASIK myopes and LASEK myopes, with the exception of CCT difference.

4 126 S. Shah et al. / Contact Lens & Anterior Eye 32 (2009) Fig. 4. (a) Scatterplot showing the influence of initial IOPg on the IOPg difference in three groups of patients. (b) Scatterplot showing the influence of initial CH on the CH difference in three groups of patients. different and the CCT difference across all three groups. While the preop CH correlated to the preop CCT (r = 0.489), no other pair wise linear relationship was statistically significant among them. Figs. 4a, b and 5a, b show the influence of initial IOPg and CH on the IOPg difference, CH difference, IOPcc difference and CRF difference. For all three groups of patients, the IOPg difference is proportional to the preop IOPg value. The higher the preop IOPg, the larger the IOPg difference (i.e. IOPg decreased more after surgery). The preop CH had a weak influence on the CH change as one can see from Fig. 4a and b. Similar relationships can also be observed between IOPcc difference and preop IOPg and between CRF difference and preop CH (Fig. 5a and b) and CH difference and CCT difference (Fig. 6). Comparing the two groups of myopic patients, according to the models selected by the best subset regression, the influences of the type of surgery (LASEK and LASIK procedures) on IOPg difference, IOPcc difference, CH difference and CRF difference at the 3 months post-op time point are not statistically significant when other factors were considered. The factors influencing the IOPg difference are preop IOPg and preop CH. The IOPg decreases the most for those with higher preop IOPg and higher preop CH. The factors influencing the IOPcc difference are preop IOPg, preop CH Fig. 5. (a) Scatterplot showing the influence of initial CH on the CRF difference in three groups of patients. (b) Scatterplot showing the influence of initial IOPg on the IOPcc difference in three groups of patients. and gender. The IOPcc decreases the most for females with a higher preop IOPg. The factors influencing the CH difference were preop CH, preop IOPg and gender. The CH decreased the most for males with a higher preop CH and lower preop IOPg. The factors influencing the CRF difference were preop CH and gender. The CRF decreased the most for males with a higher preop CH. Age, ablation (CCT difference) and preop CCT were not influential on IOPg difference, IOPcc difference, CH difference and CRF difference. Comparing the two groups of patients who had LASIK surgery, the type of diagnosis (myopia/hyperopia) has a significant influence on the IOPg difference, IOPcc difference, CH difference and CRF difference. For IOPg difference, the additional influential Table 3 The Pearson correlation between preop CCT, preop IOPg, preop CH and CCT difference.. Preop IOPg Preop CH Preop CCT Preop CH Preop CCT a CCT difference a Denotes the value is statistically different from zero at 0.05 level. Fig. 6. Scatterplot showing the change in CCT versus change in CH in three groups of patients.

5 S. Shah et al. / Contact Lens & Anterior Eye 32 (2009) factors are gender and preop IOPg. For IOPcc difference, the additional influential factors are preop CH and preop IOPg. For CH difference, the additional influential factors are preop CH and preop IOPg. For CRF difference, the additional influential factor is preop CH. Age, ablation (CCT difference), and preop CCT are not influential on IOPg difference, IOPcc difference, CH difference and CRF difference. 4. Discussion The corneal stroma constitutes 90% of the corneal thickness and is a highly specialised tissue which is responsible for the mechanical and refractive properties of cornea [11]. The specific architecture of the most anterior part of the corneal stroma ( mm) has been suggested to be responsible for the stability of the corneal shape [12,13]. The exact mechanism which maintains the corneal shape is not known but this may be due to a passive distension of corneal tissue by IOP. This is maintained due to corneal mass, the elastic properties of the corneal tissue and the mechanical force acting on this tissue [14]. Corneal properties are different in different individuals and this is related to the structure of the corneal tissue. CCT is only one of the factors governing the corneal biomechanics [15]. To perform refractive surgery more accurately, it has been proposed that the biomechanical properties of the cornea should be taken into account [4]. Several studies have reported that when the structure of corneal tissues is altered, for example either by excimer laser ablation [3] or due to disease process such as keratoconus [16 18] corneal tissue rigidity (or elasticity) decreases. Reduced post refractive surgery IOP readings (measured IOP rather than true IOP) have also been cited as indirect evidence of a change in the biomechanical properties of the cornea [4]. Various investigators have conducted studies to measure ocular rigidity [14,16 19] but these studies used techniques that are not practical for ophthalmologists in busy clinical settings. The ORA is a new device developed by Reichert Ophthalmic Instruments which is a non-contact tonometer that measures the IOP as well as new metrics: CH (which is said to represent the visco-elastic response of the cornea) [10] and CRF represents the elastic properties of the cornea and appears to be an indicator of the overall resistance of the cornea. The ORA been reported to provide reproducible corneal biomechanical and IOP measurements in non-operated eyes [20]. This study was performed to assess CH and CRF pre and post refractive surgery to see if there was a change in these properties. The results show that both CH and CRF values were significantly lower after refractive surgery (p < , paired t-test). This is consistent with previous reports in the literature following myopic refractive surgery [9,21]. Table 2 shows the distribution of CH and CRF and indicates these values to be lower after both myopic and hyperopic refractive surgery. This is the first paper to report on a comparison of hyperopes and myopes. The difference between the CCT values before and after refractive surgery was also statistically significant (p < , paired t-test). Fig. 2 shows the distribution of CCT indicating lower CCT readings after the refractive surgery for all three groups as one would expect. The scatter plot (Fig. 6) shows the change in CCT versus change in CH. It shows a small, but insignificant correlation between these two (r = 0.155, p = 0.170). This indicates changing the CCT does not have a predictable effect on the change in CH. Although no differences were found in the change of biomechanical properties between the myopic LASIK and myopic LASEK groups in the current study, it is important to recognize that the two groups were distinct preoperatively from a biomechanical perspective. The LASEK eyes were thinner, had higher IOP, and lower CH and CRF than the LASIK eyes, confirming a preoperative bias of the surgeon. The significant predictors of post-operative changes in measured IOP and biomechanical parameters were found to be the preoperative magnitudes of CH and IOPg, as well as gender. Therefore, any differences that might exist in the response based on type of surgery, whether LASIK or LASEK, may be hidden by the preoperative biomechanical distinctions between the populations. In fact, it is interesting that the myopic LASIK group had significantly larger ablations than the myopic LASEK group, but experienced similar changes in properties and measured IOP. The hyperopic group experienced the smallest changes in biomechanical properties and IOP post-operatively, demonstrating that this procedure is bio-mechanically distinct from a myopic procedure. The caveat in the current study is that the ablation depths were also much lower in the hyperopic group. The mean measured IOPg in this study was significantly lower (p < , paired t-test) after refractive surgery. The mean difference between the IOPg pre and post refractive surgery was 1.3 mmhg. This result is in agreement with earlier studies who also reported mean IOP readings to be lower after refractive surgery [3,4,7,22 25]. IOPcc is a corneal compensated IOP value, where the difference in the two pressure readings is calculated which is termed CH and is used to calculate the IOPcc. IOPcc is an IOP that has been claimed to be less affected by corneal biomechanical properties than other methods of measurements. It is believed to compensate for the biomechanical properties of the cornea by adjusting for hysteresis and not just the corneal thickness. Correction of IOP measurements using CCT only may result in significant errors in the adjusted IOP values if the other biomechanical properties are ignored. The results of this study revealed that the mean IOPcc was higher in post-op eyes in all the three groups. If one suggests that the true IOP should be the same following refractive surgery, then it would appear that the difference in IOPcc calculation should be zero. Refractive surgery has been shown to influence corneal biomechanics in a manner that differs from the change in CCT, however, the magnitude of effect is subject to much individual variation. Theoretically a LASIK cut of collagen fibres would induce biomechanical changes and weaken the cornea. However, subsequent healing may modify this effect. There are no available publications that the authors are aware of that have measured corneal biomechanics after a lamellar cut with no other loss of tissue. Chihara et al. [7] suggested that ablation of the collagen fibres of the cornea may lead to reduced corneal rigidity as the cut collagen fibres do have tensile force hence ablation depth per se may not be principal cause of underestimation of IOP post excimer laser refractive surgery. The biomechanical properties of the cornea are variable in different individuals and may have an influence on the treatment outcome [8]. It was shown in the current study that the preoperative properties and measured pressure are the strongest predictors of post-operative change in biomechanical properties and measured IOP. Thus, greater understanding of the biomechanical properties of cornea in terms of CH and CRF may assist in improving outcomes. Future studies of biomechanically matched populations with matched ablation depths will be important to investigate the biomechanical differences in induced response between surface ablation and LASIK. Each author states that he or his family members have no proprietary interest in the development or marketing of any instruments used. References [1] Holly FJ, Lemp MA. Tear physiology and dry eyes. Surv Ophthalmol 1977;22:69 87.

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