1040-5488/15/9205-0589/0 VOL. 92, NO. 5, PP. 589Y595 OPTOMETRY AND VISION SCIENCE Copyright * 2015 American Academy of Optometry
ORIGINAL ARTICLE
Corvis ST Tonometer for Measuring Postoperative IOP in LASIK Patients Jiaxu Hong*, Zhiqiang Yu†, Chunhui Jiang†, Xingtao Zhou†, Zuguo Liu‡, Xinghuai Sun‡, and Jianjiang Xu‡
ABSTRACT Purpose. To compare the postoperative measurements of intraocular pressure (IOP) using the Corvis ST Tonometer (CST), ocular response analyzer (ORA), and Goldmann applanation tonometry (GAT) in eyes undergoing laser in situ keratomileusis (LASIK), as well as to analyze the relationship between the corneal biomechanical parameters of the CST and the ORA. Methods. Fifty participants who had undergone LASIK to treat myopia in the previous 3 months were enrolled. Postoperative IOP measurements of these participants were obtained using the CST, ORA (corneal-compensated IOP [IOPcc], Goldmanncorrelated IOP [IOPg]), and GAT. Device agreement was calculated by Bland-Altman analysis. The metrics of corneal biomechanical properties were recorded using the ORA and the CST. Corneal biomechanical parameters were compared. Results. The Bland-Altman analysis revealed a significant bias between CST and GAT, between CST and IOPcc, and between CST and IOPg of 3.4, 1.0, and 3.8, mm Hg, respectively, with 95% limits of agreement of j0.7 to 7.5 mm Hg, j2.1 to 4.2 mm Hg, and j0.4 to 8.0 mm Hg. The ORA-derived IOP measurements, CST-derived IOP, and GAT IOP values showed good correlation with each other. The CST IOP and IOPcc were higher than the GAT IOP (all p G 0.05), whereas IOPg did not differ from the GAT IOP readings. Ocular response analyzerYderived corneal biomechanical parameters (corneal hysteresis and the corneal resistance factor) showed significant correlations with CST-derived parameters, including the maximum deformation amplitude at the corneal apex and the time from start until the first applanation. Conclusions. The CST offers an alternative method for measuring postoperative IOP in LASIK patients, and it appears to obtain higher IOP values than other tonometry techniques. The technique may facilitate the investigation of corneal biomechanical property changes in LASIK-treated eyes. (Optom Vis Sci 2015;92:589Y595) Key Words: intraocular pressure, corneal biomechanics, LASIK
A
ccurate diagnosis and follow-up of elevated intraocular pressure (IOP) in eyes that have undergone laser in situ keratomileusis (LASIK) is of great importance because increased IOP in these patients may cause progressive glaucomatous optic neuropathy and may eventually lead to impairment of the visual field. Goldmann applanation tonometry (GAT) is currently the gold standard for IOP measurement, and it has been used most
*MPA, MD, PhD † MD ‡ MD, PhD School of Life Sciences, Xiamen University, Fujian Provincial Key Laboratory of Ophthalmology and Visual Science, Xiamen, China (JH, ZL); Department of Ophthalmology, Eye, Ear, Nose, and Throat Hospital, School of Shanghai Medicine, Fudan University, Shanghai, China (JH, ZY, CJ, XZ, XS, JX); State Key Laboratory of Medical Neurobiology, Institutes of Brain Science, Shanghai, China (XS); Key Laboratory of Myopia, National Health and Family Planning Commission, Shanghai, China (XS); and Schepens Eye Research Institute and Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts (JH).
widely in clinical practice. However, measuring IOP in patients after LASIK remains a major challenge because of the inconsistency in IOP measurements owing to the reduction in corneal thickness1 and alteration of corneal biomechanics,2 both of which significantly affect the accuracy of GAT.3 As a consequence, several new devices have been used to overcome the disadvantages of GAT, including Tonopen,4 rebound tonometry,5 dynamic contour tonometry (DCT),1 and ocular response analyzer (ORA).6 Recently, the Corvis ST Tonometer (CST), a noncontact tonometer, was designed to measure IOP, provide parameters reflecting corneal biomechanical properties, and allow for investigation of the cornea’s dynamic reaction after an air impulse.7 Several CST studies have revealed acceptable repeatability and reproducibility and good correlation with other tonometers in IOP measurement in normal subjects, as well as in ocular hypertension and glaucoma patients.8 However, few reports are available on the application of this device for measuring IOP in LASIK patients. Interestingly, a case report has suggested that the CST may be more
Optometry and Vision Science, Vol. 92, No. 5, May 2015
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590 Postoperative IOP in LASIK PatientsVHong et al.
useful than the GAT in obtaining the true IOP of patients with pressure-induced stromal keratopathy after LASIK.8 We have found that IOP measurements between the CST and other tonometers may not be interchangeable.7 Therefore, it is important to assess whether this new generation of tonometer can be used for LASIK patients. The purpose of this study was to compare the postoperative IOP measurement for the first time by using the CST, ORA, and GAT on eyes that have undergone LASIK. A secondary objective was to analyze the relationship between the set of corneal biomechanical parameters using the CST and the ORA and to investigate potential factors that might account for the difference between the CST and GAT.
METHODS Fifty eyes of 50 consecutive Chinese participants who had undergone LASIK to treat myopia in the previous 3 months at the Shanghai Eye & Ear, Nose and Throat Hospital were considered. The enrolled patients fulfilled the general criteria for LASIK: 18 years or older, stable refraction for at least 2 years, baseline logarithm of the minimum angle of resolution best spectaclecorrected visual acuity of 0.3 or better in both eyes, greater than 3.0 diopters of preoperative myopic SE with less than or equal to 1.0 diopters of myopic astigmatism, no previous ocular disease or surgery, and no connective tissue disease or systemic disease that might influence corneal wound healing. Furthermore, patients who had either anatomic limitations to undergoing LASIK surgery (suspected keratoconus, steep corneas, epithelial basement membrane dystrophy, deep-set eyes, and glaucoma-filtering blebs) or expressed a preference to undergo surface ablation for correcting their refractive error were excluded. All LASIK procedures were performed by the same surgeon. In detail, the eye scheduled for LASIK was fixed by a suction ring using a 60-mm Hg negative pressure, which was increased gradually. The corneal flap was created using a mechanical microkeratome Moria M2 (Moria, Antony, France). Laser ablation was performed using the Zeiss MEL-80 excimer laser (Carl Zeiss Meditec, Jena, Germany). The ablation was centered at the pupil center in all eyes. The LASIK procedure was completed without complication in all cases. Dexamethasone 0.1% drops were applied every 5 minutes for three times immediately after the operation and then four times per day for 3 days. Patients were given levofloxacin 0.3% drops four times per day for 2 weeks and fluorometholone 0.1% drops four times per day, which was usually tapered over 8 weeks. The Medical Ethics Committee approved this study protocol before the data collection began. The research conducted met the tenets of the Declaration of Helsinki. Written informed consent was obtained from each participant before examination. One eye of each subject was selected randomly using a random digits table for further analysis. A full ophthalmic examination was performed on each eye, including objective and subjective refraction, slit-lamp biomicroscopy, IOLMaster (Carl Zeiss Meditec), and Pentacam (Oculus Optikgera¨te GmbH, Wetzlar, Germany). To minimize the potential confounding effect of diurnal IOP variation, all measurements were obtained in the afternoon between 1:00 and 4:00 PM. All tonometers were calibrated according to the manufacturers’ guidelines. Postoperative IOP was measured in a sitting
position by the same operator, using either a CST-ORA-GAT or an ORA-CST-GAT sequence. The measurement sequence for each participant was chosen randomly using a random digits table. The instruments used for IOP measurements included a newly developed noncontact tonometer (Corvis ST, Oculus Optikgera¨te GmbH), an ORA (Reichert Inc, Depew, NY), and a Goldmann applanation tonometer (Haag-Streit, Bern, Switzerland). During a single visit, the IOP of each eye was measured two times with each device, and the mean values were used for further analysis. Participants were asked to pause for 2 minutes between each measurement taken with the same tonometer and for 5 minutes between measurements taken with different tonometers. Statistical analysis was performed using SPSS statistical software package (SPSS for Windows, version 17.0; SPSS, Inc, Chicago, IL) and MedCalc software version 12.2.1.0 (MedCalc Software, Mariakerke, Belgium). The data are shown as mean T SD. Agreement between devices was assessed using Bland-Altman analyses. Student t test and mixed-model analysis of variance with post hoc least significant difference multiple comparisons were used to compare the postoperative IOP measurements taken using different devices. The nonparametric Spearman correlation coefficient was used to assess the corneal biomechanical parameters obtained using the CST (the maximum deformation amplitude at the corneal apex [MDA] and the time from start until the first applanation [1st A-time]) and the ORA (corneal hysteresis [CH] and corneal resistance factor [CRF]) to evaluate the relationships among different tonometry techniques and to establish the potential postoperative factors affecting the postoperative IOP difference between the CST and the GAT. All p values were two sided and considered statistically significant when they were less than 0.05.
RESULTS Patient Demographics Fifty eyes of 50 participants (30 male and 20 female) were selected for this study (Table 1). Intraocular pressure was measured successfully using the CST, ORA, and GAT in all eyes. The best spectaclecorrected visual acuity was 20/20 or better in all cases after LASIK. TABLE 1.
Demographic data of LASIK participants Characteristic Age, y Male sex Axial length, mm MRSE after LASIK, D Central corneal thickness before LASIK, Km Central corneal thickness after LASIK, Km Mean K after LASIK, D ORA: CH after LASIK, mm Hg ORA: CRF after LASIK, mm Hg CST: MDA after LASIK, mm CST: 1st A-time after LASIK, ms
Value 21.8 T 5.9 30 25.9 T 1.2 0.1 T 0.3 542 T 26 447 T 46 36.5 T 3.7 7.8 T 2.0 7.5 T 2.1 1.1 T 0.1 7.1 T 0.3
Values are expressed as mean T SD (except for male sex, which is expressed as frequency [n]). MRSE, mean refractive spherical equivalent.
Optometry and Vision Science, Vol. 92, No. 5, May 2015
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Postoperative IOP in LASIK PatientsVHong et al.
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FIGURE 1. Bland-Altman scatterplot showing agreement among different postoperative IOP measurement devices. (A) Between CST and GAT: mean difference, 3.4 mm Hg; 95% limits of agreement, T4.1 mm Hg. (B) Between CST and ORA-derived IOPcc: mean difference, 1.0 mm Hg; 95% limits of agreement, T3.2 mm Hg. (C) Between CST and ORA-derived IOPg: mean difference, j1.1 mm Hg; 95% limits of agreement, T4.2 mm Hg. (D) Between IOPcc and GAT: mean difference, 2.4 mm Hg; 95% limits of agreement, T3.3 mm Hg. (E) Between IOPg and GAT: mean difference, j0.4 mm Hg; 95% limits of agreement, T3.6 mm Hg. (F) Between IOPcc and IOPg: mean difference, 2.8 mm Hg; 95% limits of agreement, T3.7 mm Hg. Optometry and Vision Science, Vol. 92, No. 5, May 2015
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592 Postoperative IOP in LASIK PatientsVHong et al. TABLE 2.
Comparison of postoperative IOP measurements among different tonometers IOP, mm Hg
Mean T SD
CST GAT* IOPcc IOPg* GAT before LASIK
16.4 T 13.0 T 15.3 T 12.5 T 14.9 T
2.2 2.3 2.4 2.1 2.5
Range 10Y20 9Y17 10Y20 8Y18 10.2Y21
*Significant difference was detected compared with GAT before LASIK, p G 0.05.
Agreement between Devices Fig. 1 shows Bland-Altman plots, illustrating agreement between devices. The analysis shows that, on average, postoperative IOP measured by the CST was about 3.4 mm Hg higher than that by the GAT with 95% limits of agreement of j0.7 to 7.5 mm Hg. In addition, its value was 1.0 mm Hg higher than that obtained using the ORA-derived IOPcc (95% limits of agreement, j2.1 to 4.2 mm Hg) and 3.8 mm Hg higher than that obtained using the ORA-derived IOPg (95% limits of agreement, j0.4 to 8.0 mm Hg) (Fig. 1A to C). Intraocular pressure measurement agreement analyses among the GAT, IOPcc, and IOPg are also shown in Fig. 1D to F.
Comparison of Postoperative IOP Measurements among Different Tonometers after LASIK Table 2 lists the mean and range of postoperative IOP obtained using each of the three tonometers. As shown in Fig. 2, there was a statistically significant difference in IOP measurements among the tonometers (p G 0.001). Furthermore, the least significant
difference multiple comparisons analysis demonstrated that both the CST and the IOPcc obtained significantly higher IOP readings than the GAT (both p G 0.001), whereas the IOPg values were similar to those of the GAT (p = 0.37). In addition, Table 3 shows that all three IOP tonometry techniques were highly correlated (all p G 0.001). The Spearman coefficient of correlation appears to be highest between CST and IOPcc (0.822) and between IOPcc and GAT (0.767). The lowest correlations were between IOPg and CST (0.544) and between IOPg and IOPcc (0.630). Of note, as listed in Table 2, it appears that postoperative IOP readings of the CST (p = 0.07) and IOPcc (p = 0.32) after LASIK are closer to that of the GAT before LASIK than to those of the GAT (p G 0.001) and IOPg (p G 0.001).
Correlation of Postoperative Corneal Biomechanical Parameters between ORA and CST The mean values of postoperative corneal biomechanical parameters obtained using the ORA and the CST are presented in Table 1. As shown in Fig. 3, significant negative correlations were found between the MDA and the ORA-derived parameters, including CH (j0.437, p = 0.002) and the CRF (j0.438, p = 0.001). The correlations between 1st A-time and CH (0.488, p G 0.001) and CRF (0.495, p G 0.001) were positive. Furthermore, we revealed significant correlations between MDA and 1st A-time (j0.849, p G 0.001) and between CH and CRF (0.850, p G 0.001).
Effect of Potential Postoperative Factors on Difference between CST and GAT in LASIK-Treated Eyes The difference in postoperative IOP values between the CST and GAT did not correlate significantly with the LASIK patients’ age (j0.182, p = 0.205), sex (0.055, p = 0.702), axial length (j0.042, p = 0.772), mean refractive spherical equivalent (0.078, p = 0.589), mean K value (0.025, p = 0.864), or any corneal biomechanical parameter (all p 9 0.05). However, it was significantly correlated with the central corneal thickness (0.793, p = 0.035).
DISCUSSION Obtaining accurate IOP of LASIK patients could be challenging for most ophthalmologists and optometrists. Previous reports have revealed a mean underestimation of IOP after LASIK procedures, particularly when the GAT is used.2,3,9,10 It should be noted that falsely low IOP readings may lead to a delay in glaucoma diagnosis, TABLE 3.
Correlations of IOP measurements among different tonometers Tonometer FIGURE 2. Comparison of IOP measurements among three tonometers. Analysis of variance indicated that there was a statistically significant difference in IOP measurements among the tonometers (p G 0.001). The post hoc least significant difference multiple comparisons further revealed that both CST and IOPcc obtained significantly higher IOP readings compared with GAT (both p G 0.001), whereas the IOPg values were similar to those of GAT (p = 0.37).
CST vs. GAT IOPcc vs. GAT IOPg vs. GAT CST vs. IOPcc CST vs. IOPg IOPcc vs. IOPg
p
Spearman Q
G0.001 G0.001 G0.001 G0.001 G0.001 G0.001
0.672 0.767 0.667 0.822 0.544 0.630
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Postoperative IOP in LASIK PatientsVHong et al.
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FIGURE 3. Correlation of different corneal biomechanical parameters between CST and ORA tonometer. Significant negative correlations were found (A) between MDA and the ORA-derived CH (j0.437, p = 0.002) and (B) between MDA and the CRF (j0.438, p = 0.001). Significant positive correlations were found (C) between 1st A-time and CH (0.488, p G 0.001) and (D) between 1st A-time and CRF (0.495, p G 0.001).
inability to detect steroid responders after LASIK, and delayed recognition of ocular hypertensive patients.11 The main source of inaccuracy in IOP measurement after LASIK is believed to be the reduction in central corneal thickness and changes in corneal biomechanics.1,2,12 The CST is the first noncontact tonometer incorporating the Scheimpflug technology to measure corneal deformation from airpuff indentation. In the current study, we compared its performance with the GAT and the ORA in eyes that had undergone LASIK. Unlike the GAT and the ORA, which have been used widely in clinical practice, the CST is still considered to be novel, and its clinical use in postoperative LASIK patients has been limited thus far.13 Our data showed statistically significant differences in postoperative IOP values of LASIK patients with all three devices, although they are highly correlated. The Bland-Altman analysis indicated that the CST has the highest readings. Interestingly, postoperative corneal biomechanical parameters determined by the CST and ORA showed
a significant correlation with each other. It appears that the greater difference between the CST and GAT in LASIK patients is associated with a thinner cornea. Our results indicated that postoperative IOP measurements taken with each device may not be interchangeable in LASIK patients. The CST readings were, on average, 3.4 mm Hg higher than the GAT readings and 1.0 mm Hg higher than the IOPcc readings. This finding is different from our previous results on normal subjects and glaucoma patients, which revealed that the CST readings were lower than those of the GAT and Topcon noncontact tonometer.7 Other researchers also indicated a trend of higher IOP readings with the CST than with the GAT when corneal thickness increases in normal subjects and glaucoma patients, suggesting that the IOP readings in the CST is dependent on corneal thickness.14 Possible reasons for the controversial findings included different participants, ethnic differences, and changes in biomechanical properties in LASIKtreated eyes. Furthermore, our data found that central corneal
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594 Postoperative IOP in LASIK PatientsVHong et al.
thickness was the only factor associated with the IOP difference between the CST and GAT in LASIK-treated eyes, indicating that the CST may be more resistant to effects of corneal thickness than the GAT in surgically thinned corneas. Based on these findings, if one considers that calibration errors of T2.0 to T3.0 mm Hg for the GAT are still regarded as clinically acceptable,10 it appears that the limits of agreement are not good enough for the devices to replace each other. However, we must point out that postoperative IOP measurement with the GAT in LASIK patients is considered inaccurate. Clinicians should take this into account in interpreting this phenomenon. The question of which tonometer obtains the most accurate IOP (e.g., by intracameral measurements of IOP) in LASIK patients requires further study. The data presented in this study suggest that the correlation of postoperative IOP measurements between the GAT and the CST is rather weak (0.672) compared with other IOP tonometers, such as DCT and ICare, whose correlation coefficients are 0.91 and 0.89, respectively.9 Similarly, another study reported the correlation coefficient between the GAT and CST IOP values to be 0.75.14 Interestingly, our previous study revealed a higher correlation between the CST and GAT (0.896),7 which is in contrast with these findings. Our data may indicate that there is good correlation between the GAT and the CST in normal patients but not in patients who underwent LASIK recently. To the best of our knowledge, this is the first study to compare postoperative corneal biomechanical parameters obtained using the CST with those obtained using the ORA. Although these results are restricted to LASIK patients and no normal subjects or glaucoma patients were observed, we found that both the MDA and 1st A-time obtained using the CST correlated well with the CH and CRF obtained by the ORA. It appears that greater CH and CRF may induce a smaller MDA but lead to a longer 1st Atime. We chose only MDA and 1st A-time for this analysis because only these two parameters have been shown to have acceptable repeatability and reproducibility in human subjects15 as well as to be helpful in assessing corneal biomechanical changes after corneal refractive surgery.13 Our findings confirm the results of previous studies that the ORA and the CST are informative in the evaluation of corneal biomechanics in normal eyes and eyes undergoing keratorefractive procedures.16,17 We believe that these data could provide better understanding of the relationship between the biomechanical corneal properties and corneal deformation during the IOP measurement and allow for greater use of this biomechanical information delivered by the CST. Our analysis showed that the postoperative IOP difference between the CST and GAT was correlated only with corneal thickness. There have been conflicting studies on the correlation between a decrease in IOP and a change in central corneal thickness. Some studies have reported that as the central corneal thickness is reduced after LASIK, GAT was underestimated after surgery.12,17 However, no significant correlation between a decrease in IOP measured by DCT and a change in corneal thickness was observed.18 In the majority of studies comparing the GAT with other IOP tonometers, it has been widely assumed that the decrease in corneal thickness is the major cause of the decrease in IOP measured with the GAT after LASIK. In a previous study, we found that there was no statistically significant difference in IOP measurement between the CST and the GAT in corneas with normal thicknesses.7 Taken
together, the greater postoperative IOP difference between the CST and the GAT for thinner corneas may indicate that IOP readings by the CST tend to be relatively immune to pachymetry changes after LASIK. Potential limitations of the current study should be mentioned. First, because most of the enrolled subjects were only measured with the GAT before LASIK, we did not investigate the change in IOP readings before and after the surgery with these three instruments; actually, this is beyond the scope of our study and is the subject of an ongoing study. Second, we did not take into account other factors that may influence postoperative IOP readings, such as flap thickness. However, the main aim of this study was to evaluate IOP measurement by the CST in eyes having undergone LASIK rather than to investigate the influence of potential factors on IOP measurement. Third, owing to financial limitations, this study did not include DCT, which is recommended as the most suitable technique for measuring postoperative IOP in LASIK patients.3 Therefore, further investigation is warranted to determine whether this tonometer is superior to the CST. Fourth, the same operator took all measurements on all subjects in a nonmasked fashion. However, because both the CST and the ORA measure the IOP and give the report automatically, and the GAT was measured last, the effect of the examination fashion on IOP measurements may be limited. Finally, the repeatability and reproducibility of all instruments were not analyzed in this study for all instruments because this issue has been well documented in previous studies.8 All IOP tonometers and corneal biomechanical parameters proved to be repeatable and reproducible. Although the new CST was found to yield higher postoperative IOP readings, its measurements correlated well with both the GAT and the ORA in patients after LASIK and remained close to the preoperative GAT readings. With regard to the increasing awareness of the effect of corneal thickness and biomechanical properties on IOP readings by applanation tonometry and the increasing number of patients with a history of corneal refractive surgery, a CST equipped with a function for measuring the corneal thickness and deformation may act as a valuable alternative to established IOP tonometers. It should be pointed out that the prospective validation of such parameters remains incomplete. Additional studies comparing the preoperative and postoperative IOP measurements obtained using these three tonometers in eyes that have undergone LASIK should be performed to address this issue.
ACKNOWLEDGMENTS The authors were supported by grants from the Key Clinic Medicine Research Program, the Ministry of Health, China (201302015); the National Science and Technology Research Program, the Ministry of Science and Technology, China (2012BAI08B01); the National Natural Science Foundation of China (81170817, 81200658, 81300735, 81270978, U1205025, and 81330022); the New Technology Joint Research Project in Shanghai Hospitals (SHDC12014114); and the Scientific Research Program, Science and Technology Commission of Shanghai Municipality, Shanghai (13441900900, 13430720400, 134119a8800, and 13430710500). The sponsor or funding organization had no role in the design or conduct of this research. Jiaxu Hong and Zhiqiang Yu contributed equally to this article. The authors have no disclosures to declare. Received July 16, 2014; accepted January 28, 2015.
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REFERENCES 1. Kaufmann C, Bachmann LM, Thiel MA. Intraocular pressure measurements using dynamic contour tonometry after laser in situ keratomileusis. Invest Ophthalmol Vis Sci 2003;44:3790Y4. 2. Pepose JS, Feigenbaum SK, Qazi MA, Sanderson JP, Roberts CJ. Changes in corneal biomechanics and intraocular pressure following LASIK using static, dynamic, and noncontact tonometry. Am J Ophthalmol 2007;143:39Y47. 3. Tsai AS, Loon SC. Intraocular pressure assessment after laser in situ keratomileusis: a review. Clin Experiment Ophthalmol 2012;40:295Y304. 4. Vakili R, Choudhri SA, Tauber S, Shields MB. Effect of mild to moderate myopic correction by laser-assisted in situ keratomileusis on intraocular pressure measurements with goldmann applanation tonometer, tono-pen, and pneumatonometer. J Glaucoma 2002; 11:493Y6. 5. Lam AK, Wu R, Wang Z, Woo V, Chan E, Tam K, Chau R, Wong KK. Effect of laser in situ keratomileusis on rebound tonometry and Goldmann applanation tonometry. J Cataract Refract Surg 2010;36: 631Y6. 6. Kirwan C, O’Keefe M. Measurement of intraocular pressure in LASIK and LASEK patients using the Reichert Ocular Response Analyzer and Goldmann applanation tonometry. J Refract Surg 2008;24:366Y70. 7. Hong J, Xu J, Wei A, Deng SX, Cui X, Yu X, Sun X. A new tonometerVthe Corvis ST tonometer: clinical comparison with noncontact and Goldmann applanation tonometers. Invest Ophthalmol Vis Sci 2013;54:659Y65. 8. Faria-Correia F, Ramos I, Valbon B, Luz A, Roberts CJ, Ambrosio R, Jr. Scheimpflug-based tomography and biomechanical assessment in pressure-induced stromal keratopathy. J Refract Surg 2013;29: 356Y8. 9. Johannesson G, Hallberg P, Eklund A, Linden C. Pascal, ICare and Goldmann applanation tonometryVa comparative study. Acta Ophthalmol 2008;86:614Y21. 10. Sandhu SS, Chattopadhyay S, Birch MK, Ray-Chaudhuri N. Frequency of goldmann applanation tonometer calibration error checks. J Glaucoma 2005;14:215Y8. 11. Bashford KP, Shafranov G, Tauber S, Shields MB. Considerations of glaucoma in patients undergoing corneal refractive surgery. Surv Ophthalmol 2005;50:245Y51.
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12. Rashad KM, Bahnassy AA. Changes in intraocular pressure after laser in situ keratomileusis. J Refract Surg 2001;17:420Y7. 13. Shen Y, Chen Z, Knorz MC, Li M, Zhao J, Zhou X. Comparison of corneal deformation parameters after SMILE, LASEK, and femtosecond laser-assisted LASIK. J Refract Surg 2014;30:310Y8. 14. Reznicek L, Muth D, Kampik A, Neubauer AS, Hirneiss C. Evaluation of a novel Scheimpflug-based non-contact tonometer in healthy subjects and patients with ocular hypertension and glaucoma. Br J Ophthalmol 2013;97:1410Y4. 15. Hon Y, Lam AKC. Corneal deformation measurement using Scheimpflug noncontact tonometry. Optom Vis Sci 2013;90:E1Y8. 16. Huseynova T, Waring GO, Roberts C, Krueger RR, Tomita M. Corneal biomechanics as a function of intraocular pressure and pachymetry by dynamic infrared signal and Scheimpflug imaging analysis in normal eyes. Am J Ophthalmol 2014;157:885Y93. 17. Pedersen IB, Bak-Nielsen S, Vestergaard AH, Ivarsen A, Hjortdal J. Corneal biomechanical properties after LASIK, ReLEx flex, and ReLEx smile by Scheimpflug-based dynamic tonometry. Graefes Arch Clin Exp Ophthalmol 2014;252:1329Y35. 18. Siganos DS, Papastergiou GI, Moedas C. Assessment of the Pascal dynamic contour tonometer in monitoring intraocular pressure in unoperated eyes and eyes after LASIK. J Cataract Refract Surg 2004; 30:746Y51.
Jianjiang Xu Department of Ophthalmology and Visual Science Eye, Ear, Nose, and Throat Hospital Shanghai Medical College, Fudan University 83 Fenyang Rd Shanghai 200031 China e-mail: [email protected] Zuguo Liu Fujian Provincial Key Laboratory of Ophthalmology and Visual Science Xiamen University Xiamen, 361005 China e-mail: [email protected]
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ORIGINAL ARTICLE
Corvis ST Tonometer for Measuring Postoperative IOP in LASIK Patients Jiaxu Hong*, Zhiqiang Yu†, Chunhui Jiang†, Xingtao Zhou†, Zuguo Liu‡, Xinghuai Sun‡, and Jianjiang Xu‡
ABSTRACT Purpose. To compare the postoperative measurements of intraocular pressure (IOP) using the Corvis ST Tonometer (CST), ocular response analyzer (ORA), and Goldmann applanation tonometry (GAT) in eyes undergoing laser in situ keratomileusis (LASIK), as well as to analyze the relationship between the corneal biomechanical parameters of the CST and the ORA. Methods. Fifty participants who had undergone LASIK to treat myopia in the previous 3 months were enrolled. Postoperative IOP measurements of these participants were obtained using the CST, ORA (corneal-compensated IOP [IOPcc], Goldmanncorrelated IOP [IOPg]), and GAT. Device agreement was calculated by Bland-Altman analysis. The metrics of corneal biomechanical properties were recorded using the ORA and the CST. Corneal biomechanical parameters were compared. Results. The Bland-Altman analysis revealed a significant bias between CST and GAT, between CST and IOPcc, and between CST and IOPg of 3.4, 1.0, and 3.8, mm Hg, respectively, with 95% limits of agreement of j0.7 to 7.5 mm Hg, j2.1 to 4.2 mm Hg, and j0.4 to 8.0 mm Hg. The ORA-derived IOP measurements, CST-derived IOP, and GAT IOP values showed good correlation with each other. The CST IOP and IOPcc were higher than the GAT IOP (all p G 0.05), whereas IOPg did not differ from the GAT IOP readings. Ocular response analyzerYderived corneal biomechanical parameters (corneal hysteresis and the corneal resistance factor) showed significant correlations with CST-derived parameters, including the maximum deformation amplitude at the corneal apex and the time from start until the first applanation. Conclusions. The CST offers an alternative method for measuring postoperative IOP in LASIK patients, and it appears to obtain higher IOP values than other tonometry techniques. The technique may facilitate the investigation of corneal biomechanical property changes in LASIK-treated eyes. (Optom Vis Sci 2015;92:589Y595) Key Words: intraocular pressure, corneal biomechanics, LASIK
A
ccurate diagnosis and follow-up of elevated intraocular pressure (IOP) in eyes that have undergone laser in situ keratomileusis (LASIK) is of great importance because increased IOP in these patients may cause progressive glaucomatous optic neuropathy and may eventually lead to impairment of the visual field. Goldmann applanation tonometry (GAT) is currently the gold standard for IOP measurement, and it has been used most
*MPA, MD, PhD † MD ‡ MD, PhD School of Life Sciences, Xiamen University, Fujian Provincial Key Laboratory of Ophthalmology and Visual Science, Xiamen, China (JH, ZL); Department of Ophthalmology, Eye, Ear, Nose, and Throat Hospital, School of Shanghai Medicine, Fudan University, Shanghai, China (JH, ZY, CJ, XZ, XS, JX); State Key Laboratory of Medical Neurobiology, Institutes of Brain Science, Shanghai, China (XS); Key Laboratory of Myopia, National Health and Family Planning Commission, Shanghai, China (XS); and Schepens Eye Research Institute and Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts (JH).
widely in clinical practice. However, measuring IOP in patients after LASIK remains a major challenge because of the inconsistency in IOP measurements owing to the reduction in corneal thickness1 and alteration of corneal biomechanics,2 both of which significantly affect the accuracy of GAT.3 As a consequence, several new devices have been used to overcome the disadvantages of GAT, including Tonopen,4 rebound tonometry,5 dynamic contour tonometry (DCT),1 and ocular response analyzer (ORA).6 Recently, the Corvis ST Tonometer (CST), a noncontact tonometer, was designed to measure IOP, provide parameters reflecting corneal biomechanical properties, and allow for investigation of the cornea’s dynamic reaction after an air impulse.7 Several CST studies have revealed acceptable repeatability and reproducibility and good correlation with other tonometers in IOP measurement in normal subjects, as well as in ocular hypertension and glaucoma patients.8 However, few reports are available on the application of this device for measuring IOP in LASIK patients. Interestingly, a case report has suggested that the CST may be more
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590 Postoperative IOP in LASIK PatientsVHong et al.
useful than the GAT in obtaining the true IOP of patients with pressure-induced stromal keratopathy after LASIK.8 We have found that IOP measurements between the CST and other tonometers may not be interchangeable.7 Therefore, it is important to assess whether this new generation of tonometer can be used for LASIK patients. The purpose of this study was to compare the postoperative IOP measurement for the first time by using the CST, ORA, and GAT on eyes that have undergone LASIK. A secondary objective was to analyze the relationship between the set of corneal biomechanical parameters using the CST and the ORA and to investigate potential factors that might account for the difference between the CST and GAT.
METHODS Fifty eyes of 50 consecutive Chinese participants who had undergone LASIK to treat myopia in the previous 3 months at the Shanghai Eye & Ear, Nose and Throat Hospital were considered. The enrolled patients fulfilled the general criteria for LASIK: 18 years or older, stable refraction for at least 2 years, baseline logarithm of the minimum angle of resolution best spectaclecorrected visual acuity of 0.3 or better in both eyes, greater than 3.0 diopters of preoperative myopic SE with less than or equal to 1.0 diopters of myopic astigmatism, no previous ocular disease or surgery, and no connective tissue disease or systemic disease that might influence corneal wound healing. Furthermore, patients who had either anatomic limitations to undergoing LASIK surgery (suspected keratoconus, steep corneas, epithelial basement membrane dystrophy, deep-set eyes, and glaucoma-filtering blebs) or expressed a preference to undergo surface ablation for correcting their refractive error were excluded. All LASIK procedures were performed by the same surgeon. In detail, the eye scheduled for LASIK was fixed by a suction ring using a 60-mm Hg negative pressure, which was increased gradually. The corneal flap was created using a mechanical microkeratome Moria M2 (Moria, Antony, France). Laser ablation was performed using the Zeiss MEL-80 excimer laser (Carl Zeiss Meditec, Jena, Germany). The ablation was centered at the pupil center in all eyes. The LASIK procedure was completed without complication in all cases. Dexamethasone 0.1% drops were applied every 5 minutes for three times immediately after the operation and then four times per day for 3 days. Patients were given levofloxacin 0.3% drops four times per day for 2 weeks and fluorometholone 0.1% drops four times per day, which was usually tapered over 8 weeks. The Medical Ethics Committee approved this study protocol before the data collection began. The research conducted met the tenets of the Declaration of Helsinki. Written informed consent was obtained from each participant before examination. One eye of each subject was selected randomly using a random digits table for further analysis. A full ophthalmic examination was performed on each eye, including objective and subjective refraction, slit-lamp biomicroscopy, IOLMaster (Carl Zeiss Meditec), and Pentacam (Oculus Optikgera¨te GmbH, Wetzlar, Germany). To minimize the potential confounding effect of diurnal IOP variation, all measurements were obtained in the afternoon between 1:00 and 4:00 PM. All tonometers were calibrated according to the manufacturers’ guidelines. Postoperative IOP was measured in a sitting
position by the same operator, using either a CST-ORA-GAT or an ORA-CST-GAT sequence. The measurement sequence for each participant was chosen randomly using a random digits table. The instruments used for IOP measurements included a newly developed noncontact tonometer (Corvis ST, Oculus Optikgera¨te GmbH), an ORA (Reichert Inc, Depew, NY), and a Goldmann applanation tonometer (Haag-Streit, Bern, Switzerland). During a single visit, the IOP of each eye was measured two times with each device, and the mean values were used for further analysis. Participants were asked to pause for 2 minutes between each measurement taken with the same tonometer and for 5 minutes between measurements taken with different tonometers. Statistical analysis was performed using SPSS statistical software package (SPSS for Windows, version 17.0; SPSS, Inc, Chicago, IL) and MedCalc software version 12.2.1.0 (MedCalc Software, Mariakerke, Belgium). The data are shown as mean T SD. Agreement between devices was assessed using Bland-Altman analyses. Student t test and mixed-model analysis of variance with post hoc least significant difference multiple comparisons were used to compare the postoperative IOP measurements taken using different devices. The nonparametric Spearman correlation coefficient was used to assess the corneal biomechanical parameters obtained using the CST (the maximum deformation amplitude at the corneal apex [MDA] and the time from start until the first applanation [1st A-time]) and the ORA (corneal hysteresis [CH] and corneal resistance factor [CRF]) to evaluate the relationships among different tonometry techniques and to establish the potential postoperative factors affecting the postoperative IOP difference between the CST and the GAT. All p values were two sided and considered statistically significant when they were less than 0.05.
RESULTS Patient Demographics Fifty eyes of 50 participants (30 male and 20 female) were selected for this study (Table 1). Intraocular pressure was measured successfully using the CST, ORA, and GAT in all eyes. The best spectaclecorrected visual acuity was 20/20 or better in all cases after LASIK. TABLE 1.
Demographic data of LASIK participants Characteristic Age, y Male sex Axial length, mm MRSE after LASIK, D Central corneal thickness before LASIK, Km Central corneal thickness after LASIK, Km Mean K after LASIK, D ORA: CH after LASIK, mm Hg ORA: CRF after LASIK, mm Hg CST: MDA after LASIK, mm CST: 1st A-time after LASIK, ms
Value 21.8 T 5.9 30 25.9 T 1.2 0.1 T 0.3 542 T 26 447 T 46 36.5 T 3.7 7.8 T 2.0 7.5 T 2.1 1.1 T 0.1 7.1 T 0.3
Values are expressed as mean T SD (except for male sex, which is expressed as frequency [n]). MRSE, mean refractive spherical equivalent.
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Postoperative IOP in LASIK PatientsVHong et al.
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FIGURE 1. Bland-Altman scatterplot showing agreement among different postoperative IOP measurement devices. (A) Between CST and GAT: mean difference, 3.4 mm Hg; 95% limits of agreement, T4.1 mm Hg. (B) Between CST and ORA-derived IOPcc: mean difference, 1.0 mm Hg; 95% limits of agreement, T3.2 mm Hg. (C) Between CST and ORA-derived IOPg: mean difference, j1.1 mm Hg; 95% limits of agreement, T4.2 mm Hg. (D) Between IOPcc and GAT: mean difference, 2.4 mm Hg; 95% limits of agreement, T3.3 mm Hg. (E) Between IOPg and GAT: mean difference, j0.4 mm Hg; 95% limits of agreement, T3.6 mm Hg. (F) Between IOPcc and IOPg: mean difference, 2.8 mm Hg; 95% limits of agreement, T3.7 mm Hg. Optometry and Vision Science, Vol. 92, No. 5, May 2015
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592 Postoperative IOP in LASIK PatientsVHong et al. TABLE 2.
Comparison of postoperative IOP measurements among different tonometers IOP, mm Hg
Mean T SD
CST GAT* IOPcc IOPg* GAT before LASIK
16.4 T 13.0 T 15.3 T 12.5 T 14.9 T
2.2 2.3 2.4 2.1 2.5
Range 10Y20 9Y17 10Y20 8Y18 10.2Y21
*Significant difference was detected compared with GAT before LASIK, p G 0.05.
Agreement between Devices Fig. 1 shows Bland-Altman plots, illustrating agreement between devices. The analysis shows that, on average, postoperative IOP measured by the CST was about 3.4 mm Hg higher than that by the GAT with 95% limits of agreement of j0.7 to 7.5 mm Hg. In addition, its value was 1.0 mm Hg higher than that obtained using the ORA-derived IOPcc (95% limits of agreement, j2.1 to 4.2 mm Hg) and 3.8 mm Hg higher than that obtained using the ORA-derived IOPg (95% limits of agreement, j0.4 to 8.0 mm Hg) (Fig. 1A to C). Intraocular pressure measurement agreement analyses among the GAT, IOPcc, and IOPg are also shown in Fig. 1D to F.
Comparison of Postoperative IOP Measurements among Different Tonometers after LASIK Table 2 lists the mean and range of postoperative IOP obtained using each of the three tonometers. As shown in Fig. 2, there was a statistically significant difference in IOP measurements among the tonometers (p G 0.001). Furthermore, the least significant
difference multiple comparisons analysis demonstrated that both the CST and the IOPcc obtained significantly higher IOP readings than the GAT (both p G 0.001), whereas the IOPg values were similar to those of the GAT (p = 0.37). In addition, Table 3 shows that all three IOP tonometry techniques were highly correlated (all p G 0.001). The Spearman coefficient of correlation appears to be highest between CST and IOPcc (0.822) and between IOPcc and GAT (0.767). The lowest correlations were between IOPg and CST (0.544) and between IOPg and IOPcc (0.630). Of note, as listed in Table 2, it appears that postoperative IOP readings of the CST (p = 0.07) and IOPcc (p = 0.32) after LASIK are closer to that of the GAT before LASIK than to those of the GAT (p G 0.001) and IOPg (p G 0.001).
Correlation of Postoperative Corneal Biomechanical Parameters between ORA and CST The mean values of postoperative corneal biomechanical parameters obtained using the ORA and the CST are presented in Table 1. As shown in Fig. 3, significant negative correlations were found between the MDA and the ORA-derived parameters, including CH (j0.437, p = 0.002) and the CRF (j0.438, p = 0.001). The correlations between 1st A-time and CH (0.488, p G 0.001) and CRF (0.495, p G 0.001) were positive. Furthermore, we revealed significant correlations between MDA and 1st A-time (j0.849, p G 0.001) and between CH and CRF (0.850, p G 0.001).
Effect of Potential Postoperative Factors on Difference between CST and GAT in LASIK-Treated Eyes The difference in postoperative IOP values between the CST and GAT did not correlate significantly with the LASIK patients’ age (j0.182, p = 0.205), sex (0.055, p = 0.702), axial length (j0.042, p = 0.772), mean refractive spherical equivalent (0.078, p = 0.589), mean K value (0.025, p = 0.864), or any corneal biomechanical parameter (all p 9 0.05). However, it was significantly correlated with the central corneal thickness (0.793, p = 0.035).
DISCUSSION Obtaining accurate IOP of LASIK patients could be challenging for most ophthalmologists and optometrists. Previous reports have revealed a mean underestimation of IOP after LASIK procedures, particularly when the GAT is used.2,3,9,10 It should be noted that falsely low IOP readings may lead to a delay in glaucoma diagnosis, TABLE 3.
Correlations of IOP measurements among different tonometers Tonometer FIGURE 2. Comparison of IOP measurements among three tonometers. Analysis of variance indicated that there was a statistically significant difference in IOP measurements among the tonometers (p G 0.001). The post hoc least significant difference multiple comparisons further revealed that both CST and IOPcc obtained significantly higher IOP readings compared with GAT (both p G 0.001), whereas the IOPg values were similar to those of GAT (p = 0.37).
CST vs. GAT IOPcc vs. GAT IOPg vs. GAT CST vs. IOPcc CST vs. IOPg IOPcc vs. IOPg
p
Spearman Q
G0.001 G0.001 G0.001 G0.001 G0.001 G0.001
0.672 0.767 0.667 0.822 0.544 0.630
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FIGURE 3. Correlation of different corneal biomechanical parameters between CST and ORA tonometer. Significant negative correlations were found (A) between MDA and the ORA-derived CH (j0.437, p = 0.002) and (B) between MDA and the CRF (j0.438, p = 0.001). Significant positive correlations were found (C) between 1st A-time and CH (0.488, p G 0.001) and (D) between 1st A-time and CRF (0.495, p G 0.001).
inability to detect steroid responders after LASIK, and delayed recognition of ocular hypertensive patients.11 The main source of inaccuracy in IOP measurement after LASIK is believed to be the reduction in central corneal thickness and changes in corneal biomechanics.1,2,12 The CST is the first noncontact tonometer incorporating the Scheimpflug technology to measure corneal deformation from airpuff indentation. In the current study, we compared its performance with the GAT and the ORA in eyes that had undergone LASIK. Unlike the GAT and the ORA, which have been used widely in clinical practice, the CST is still considered to be novel, and its clinical use in postoperative LASIK patients has been limited thus far.13 Our data showed statistically significant differences in postoperative IOP values of LASIK patients with all three devices, although they are highly correlated. The Bland-Altman analysis indicated that the CST has the highest readings. Interestingly, postoperative corneal biomechanical parameters determined by the CST and ORA showed
a significant correlation with each other. It appears that the greater difference between the CST and GAT in LASIK patients is associated with a thinner cornea. Our results indicated that postoperative IOP measurements taken with each device may not be interchangeable in LASIK patients. The CST readings were, on average, 3.4 mm Hg higher than the GAT readings and 1.0 mm Hg higher than the IOPcc readings. This finding is different from our previous results on normal subjects and glaucoma patients, which revealed that the CST readings were lower than those of the GAT and Topcon noncontact tonometer.7 Other researchers also indicated a trend of higher IOP readings with the CST than with the GAT when corneal thickness increases in normal subjects and glaucoma patients, suggesting that the IOP readings in the CST is dependent on corneal thickness.14 Possible reasons for the controversial findings included different participants, ethnic differences, and changes in biomechanical properties in LASIKtreated eyes. Furthermore, our data found that central corneal
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594 Postoperative IOP in LASIK PatientsVHong et al.
thickness was the only factor associated with the IOP difference between the CST and GAT in LASIK-treated eyes, indicating that the CST may be more resistant to effects of corneal thickness than the GAT in surgically thinned corneas. Based on these findings, if one considers that calibration errors of T2.0 to T3.0 mm Hg for the GAT are still regarded as clinically acceptable,10 it appears that the limits of agreement are not good enough for the devices to replace each other. However, we must point out that postoperative IOP measurement with the GAT in LASIK patients is considered inaccurate. Clinicians should take this into account in interpreting this phenomenon. The question of which tonometer obtains the most accurate IOP (e.g., by intracameral measurements of IOP) in LASIK patients requires further study. The data presented in this study suggest that the correlation of postoperative IOP measurements between the GAT and the CST is rather weak (0.672) compared with other IOP tonometers, such as DCT and ICare, whose correlation coefficients are 0.91 and 0.89, respectively.9 Similarly, another study reported the correlation coefficient between the GAT and CST IOP values to be 0.75.14 Interestingly, our previous study revealed a higher correlation between the CST and GAT (0.896),7 which is in contrast with these findings. Our data may indicate that there is good correlation between the GAT and the CST in normal patients but not in patients who underwent LASIK recently. To the best of our knowledge, this is the first study to compare postoperative corneal biomechanical parameters obtained using the CST with those obtained using the ORA. Although these results are restricted to LASIK patients and no normal subjects or glaucoma patients were observed, we found that both the MDA and 1st A-time obtained using the CST correlated well with the CH and CRF obtained by the ORA. It appears that greater CH and CRF may induce a smaller MDA but lead to a longer 1st Atime. We chose only MDA and 1st A-time for this analysis because only these two parameters have been shown to have acceptable repeatability and reproducibility in human subjects15 as well as to be helpful in assessing corneal biomechanical changes after corneal refractive surgery.13 Our findings confirm the results of previous studies that the ORA and the CST are informative in the evaluation of corneal biomechanics in normal eyes and eyes undergoing keratorefractive procedures.16,17 We believe that these data could provide better understanding of the relationship between the biomechanical corneal properties and corneal deformation during the IOP measurement and allow for greater use of this biomechanical information delivered by the CST. Our analysis showed that the postoperative IOP difference between the CST and GAT was correlated only with corneal thickness. There have been conflicting studies on the correlation between a decrease in IOP and a change in central corneal thickness. Some studies have reported that as the central corneal thickness is reduced after LASIK, GAT was underestimated after surgery.12,17 However, no significant correlation between a decrease in IOP measured by DCT and a change in corneal thickness was observed.18 In the majority of studies comparing the GAT with other IOP tonometers, it has been widely assumed that the decrease in corneal thickness is the major cause of the decrease in IOP measured with the GAT after LASIK. In a previous study, we found that there was no statistically significant difference in IOP measurement between the CST and the GAT in corneas with normal thicknesses.7 Taken
together, the greater postoperative IOP difference between the CST and the GAT for thinner corneas may indicate that IOP readings by the CST tend to be relatively immune to pachymetry changes after LASIK. Potential limitations of the current study should be mentioned. First, because most of the enrolled subjects were only measured with the GAT before LASIK, we did not investigate the change in IOP readings before and after the surgery with these three instruments; actually, this is beyond the scope of our study and is the subject of an ongoing study. Second, we did not take into account other factors that may influence postoperative IOP readings, such as flap thickness. However, the main aim of this study was to evaluate IOP measurement by the CST in eyes having undergone LASIK rather than to investigate the influence of potential factors on IOP measurement. Third, owing to financial limitations, this study did not include DCT, which is recommended as the most suitable technique for measuring postoperative IOP in LASIK patients.3 Therefore, further investigation is warranted to determine whether this tonometer is superior to the CST. Fourth, the same operator took all measurements on all subjects in a nonmasked fashion. However, because both the CST and the ORA measure the IOP and give the report automatically, and the GAT was measured last, the effect of the examination fashion on IOP measurements may be limited. Finally, the repeatability and reproducibility of all instruments were not analyzed in this study for all instruments because this issue has been well documented in previous studies.8 All IOP tonometers and corneal biomechanical parameters proved to be repeatable and reproducible. Although the new CST was found to yield higher postoperative IOP readings, its measurements correlated well with both the GAT and the ORA in patients after LASIK and remained close to the preoperative GAT readings. With regard to the increasing awareness of the effect of corneal thickness and biomechanical properties on IOP readings by applanation tonometry and the increasing number of patients with a history of corneal refractive surgery, a CST equipped with a function for measuring the corneal thickness and deformation may act as a valuable alternative to established IOP tonometers. It should be pointed out that the prospective validation of such parameters remains incomplete. Additional studies comparing the preoperative and postoperative IOP measurements obtained using these three tonometers in eyes that have undergone LASIK should be performed to address this issue.
ACKNOWLEDGMENTS The authors were supported by grants from the Key Clinic Medicine Research Program, the Ministry of Health, China (201302015); the National Science and Technology Research Program, the Ministry of Science and Technology, China (2012BAI08B01); the National Natural Science Foundation of China (81170817, 81200658, 81300735, 81270978, U1205025, and 81330022); the New Technology Joint Research Project in Shanghai Hospitals (SHDC12014114); and the Scientific Research Program, Science and Technology Commission of Shanghai Municipality, Shanghai (13441900900, 13430720400, 134119a8800, and 13430710500). The sponsor or funding organization had no role in the design or conduct of this research. Jiaxu Hong and Zhiqiang Yu contributed equally to this article. The authors have no disclosures to declare. Received July 16, 2014; accepted January 28, 2015.
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Jianjiang Xu Department of Ophthalmology and Visual Science Eye, Ear, Nose, and Throat Hospital Shanghai Medical College, Fudan University 83 Fenyang Rd Shanghai 200031 China e-mail: [email protected] Zuguo Liu Fujian Provincial Key Laboratory of Ophthalmology and Visual Science Xiamen University Xiamen, 361005 China e-mail: [email protected]
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