CLINICAL SCIENCE
Clinical Evaluation of Corneal Biomechanical Parameters After Posterior Chamber Phakic Intraocular Lens Implantation Mohamed Ali, MD,*† Kazutaka Kamiya, MD, PhD,* Kimiya Shimizu, MD, PhD,* Akihito Igarashi, MD, PhD,* and Rie Ishii, MD, PhD*
Purpose: The aim of this study was to quantitatively assess the changes in corneal biomechanics after posterior chamber phakic intraocular lens (Visian ICL; STAAR Surgical) implantation for normal and keratoconic subjects.
Methods: We retrospectively examined 29 eyes of 16 consecutive patients (mean age 6 SD, 32.4 6 7.3 years) undergoing implantable collamer lens (ICL) implantation through a 3.0-mm temporal corneal incision. We longitudinally assessed the values of corneal hysteresis (CH) and corneal resistance factor (CRF) using an Ocular Response Analyzer. We also investigated the relationship between these biomechanical parameters and central corneal thickness (CCT) preoperatively, and at 1 week, 1 month, and 3 months postoperatively. Results: The CH was 9.2 6 1.4 mm Hg preoperatively, and 9.2 6 1.4
mm Hg, 9.3 6 1.7 mm Hg, and 8.8 6 1.3 mm Hg at 1 week, 1 month, and 3 months postoperatively, respectively. The CRF was 8.4 6 1.6 mm Hg preoperatively, and 9.0 6 1.5 mm Hg, 8.8 6 1.7 mm Hg, and 8.8 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. Multiple comparisons demonstrated no significant differences between measurements made preoperatively and postoperatively (P . 0.05, Dunnett test). Both CH and CRF were significantly correlated with CCT 3 months postoperatively [Spearman correlation coefficient (r) = 0.48, P = 0.01 for CH; r = 0.84, P , 0.001 for CRF].
Conclusions: We found no significant changes in CH or CRF after ICL implantation, not only in normal eyes but also in keratoconic eyes, suggesting that this surgical technique does not significantly affect corneal biomechanical factors. The CCT may play some role in corneal biomechanics even in eyes undergoing ICL implantation. Key Words: corneal biomechanics, corneal hysteresis, corneal resistance factor, corneal thickness, implantable collamer lens (Cornea 2014;33:470–474) Received for publication October 27, 2013; revision received December 19, 2013; accepted January 10, 2014. Published online ahead of print March 7, 2014. From the *Department of Ophthalmology, University of Kitasato School of Medicine, Kanagawa, Japan; and †Department of Ophthalmology, Faculty of Medicine, Minia University Hospitals, Minia, Egypt. K. Shimizu has received consultancy fees from the STAAR Surgical Company. The others authors have no funding or conflicts of interest to disclose. Reprints: Kazutaka Kamiya, Department of Ophthalmology, University of Kitasato School of Medicine, 1-15-1, Kitasato, Sagamihara, Kanagawa 228-8555, Japan (e-mail: [email protected]). Copyright © 2014 by Lippincott Williams & Wilkins
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hakic intraocular lens (IOL) implantation has been widely accepted now as the first surgical option in the field of refractive surgery to correct moderate-to-high myopia in patients who may not be appropriate candidates for undergoing keratorefractive procedures because of having low pachymetric values and post–laser in situ keratomileusis (LASIK) ectasia concerns.1,2 An implantation of the phakic IOL helps patients with high myopia or thin corneas to get rid of glasses or contact lenses without the risk of developing keratectasia caused by LASIK technique,3,4 and has several advantages over LASIK, in terms of fast visual recovery and rehabilitation, excellent refractive accuracy and stability, improved visual acuity, preservation of physiological accommodation, and being a largely reversible procedure.5–7 The Visian Implantable Collamer Lens (STAAR Surgical, Nidau, Switzerland), a posterior chamber phakic IOL, has been reported to be effective for the correction of moderate-tohigh ametropia with better visual performance than that of LASIK.8,9 This surgical technique requires a 3.0-mm temporal corneal incision. Hence, it is theoretically possible that the postoperative biomechanical characteristics, which may play a role not only in the refractive outcomes but also in the measurement of the intraocular pressure (IOP),10–13 might be compromised with time. However, as far as we can ascertain, the time course of corneal biomechanical parameters in implantable collamer lens (ICL)–implanted eyes has not so far been investigated either in normal eyes or in keratoconic eyes. Considering that toric ICL implantation has been reported to be effective for the correction of moderate-to-high myopic astigmatism in keratoconic eyes,14–18 it is also clinically meaningful to assess the changes in corneal biomechanics for keratoconus after ICL implantation. The purpose of this study is to retrospectively assess the time course of corneal biomechanical variables, not only in normal eyes but also in keratoconic eyes, after ICL implantation.
MATERIALS AND METHODS Study Population Twenty-nine eyes of 16 consecutive patients (8 men and 8 women), who underwent an uneventful ICL implantation at the Kitasato University Hospital, and who regularly returned for postoperative examination, were included in this retrospective observational study. The patient age at the time Cornea Volume 33, Number 5, May 2014
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of the surgery was 32.4 6 7.3 years (mean 6 SD) (95% confidence interval, 18.1–46.7 years). The preoperative manifest spherical equivalent was 29.7 6 4.9 (219.3 to 20.2) diopters (D). The preoperative manifest cylinder was 21.09 6 1.08 (23.2 to 1.0 D). The study comprised 25 normal eyes and 4 mild and nonprogressive keratoconic eyes undergoing ICL implantation. The sample size in this study offered 82.3% statistical power at 5% level to detect a 1-mm Hg difference in corneal hysteresis (CH), when the SD of the mean difference was 1.8 mm Hg. The study was approved by the Institutional Review Board of Kitasato University and followed the tenets of the Declaration of Helsinki. Informed consent was obtained from all the patients after an explanation of the nature and possible consequences of the study was given to them.
Surgical Procedure The patients preoperatively underwent 2 peripheral iridotomies with a neodymium-doped yttrium aluminum garnet laser. On the day of the surgery, the patients were given dilating and cycloplegic agents. After topical anesthesia was given, a model V4 ICL was inserted through a 3-mm temporal corneal incision using an injector cartridge (STAAR Surgical) after the placement of a viscosurgical device (Opegan; Santen, Osaka, Japan) into the anterior chamber. The ICL was placed in the posterior chamber, the remaining viscosurgical device was completely washed out of the anterior chamber with balanced salt solution, and a miotic agent was instilled. For toric ICL implantation, to control for potential cyclotorsion in a supine position, the zero horizontal axis was marked preoperatively using a slit lamp. A Mendez ring was also used for intraoperatively measuring the required rotation from the horizontal axis. After that, the ICL had been placed in the posterior chamber and rotated by #22.5° using the manipulator. After the surgery, steroidal (0.1% betamethasone, Rinderon; Shionogi, Osaka, Japan) and antibiotic (levofloxacin, Cravit; Santen, Osaka, Japan) medications were administered topically 4 times daily for 2 weeks, and the dose was steadily reduced thereafter.
Measurements of Corneal Biomechanical Parameters We measured the biomechanical parameters of the cornea, characterized by CH and corneal resistance factor (CRF), using the Ocular Response Analyzer (ORA; Reichert Ophthalmic Instruments, Depew, NY) with software version 2.04, before the surgery and at 1 week, 1 month, and 3 months after the surgery. This device used a rapid air impulse to deform the cornea, and the shape changes were monitored by an electrooptical system. The air puff induced 2 corneal applanations, inward and outward, of the cornea. The air deforms the cornea through an initial applanation event (peak 1), then beyond it into a concavity, and gradually subsides, allowing the cornea to return to its original shape as the applied pressure becomes lower than the IOP, passing through a second applanation (peak 2). The CH was calculated as the difference between pressures (millimeters of mercury) where infrared peaks 1 and 2 occur.19 The CRF Ó 2014 Lippincott Williams & Wilkins
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was calculated as a linear function of P1 and P2, based on the results of a large-scale clinical data analysis, according to the manufacturer.19a We carried out this measurement at least 3 times with the patient in a sitting position with ocular fixation to ensure that there was consistent signal quality and to look for consistent signal morphology and measurement values. The value with the highest waveform score was used for the statistical analysis according to the manufacturer’s instructions. The waveform score is a composite index based on 5 mathematical aspects of the corneal deformation signal. The score ranges from 0 to 10, with a higher score indicating that the signal is closer to an ideal signal from a normal cornea. We confirmed that the waveform scores were $6.5 in all eyes. The central corneal thickness (CCT) was also measured using an ultrasound pachymeter (DGH-500; DGH Technologies, Exton), before the surgery and 1 week, 1 month, and 3 months after the surgery. Topical anesthetic was placed in each eye before the ultrasonic pachymetry.
Statistical Analysis All statistical analyses were performed using Stat View software (version 5.0; SAS Institute, Inc). One-way analysis of variance (ANOVA) was used to evaluate the changes over time course, and the Dunnett test was used for multiple comparisons. The Spearman correlation coefficient (r) was calculated to assess the relationship of CH and CRF with CCT. Unless otherwise indicated, the results are expressed as mean 6 SD, a value of P , 0.05 was considered statistically significant.
RESULTS Patient demographics of the study population are summarized in Table 1. All the surgeries were uneventful, and no significant increase in IOP occurred in any case during the observation period. The results of corneal biomechanical parameters are summarized in Table 2. In the whole study population, the CH was 9.2 6 1.4 mm Hg preoperatively, 9.2 6 1.4 mm Hg, 9.3 6 1.7 mm Hg, and 8.8 6 1.3 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.56, repeated measures ANOVA). The CRF was 8.4 6 1.6 mm Hg preoperatively, 9.0 6 1.5 mm Hg, 8.8 6 1.7 mm Hg, and 8.8 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of
TABLE 1. Preoperative Demographics of Study Population Demographic Parameter Age, yrs Gender (male:female) Manifest spherical equivalent, D Manifest cylinder, D CH, mm Hg CRF, mm Hg CCT, mm
Mean 6 SD (95% Confidence Interval) 32.4 6 7.3 (18.1–46.7) 8:8 29.7 6 4.9 (219.3 to 20.2) 21.09 6 1.08 (23.2 to 1.0) 9.2 6 1.4 (6.4 to 11.9) 8.4 6 1.6 (5.2 to 11.6) 535.1 6 48.9 (439.3 to 631.0)
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TABLE 2. Summary of the Corneal Biomechanical Parameters in Eyes Undergoing ICL Implantation Mean 6 SD (95% Confidence Interval) Study Group Whole study population Normal eyes Keratoconic eyes
Parameter CH (mm Hg) CRF (mm Hg) CH (mm Hg) CRF (mm Hg) CH (mm Hg) CRF (mm Hg)
9.2 8.4 9.3 8.6 8.4 7.1
Preoperative
1-week Postoperative
6 6 6 6 6 6
9.2 9.0 9.3 9.0 8.7 8.5
1.4 1.6 1.4 1.6 0.6 1.4
(6.4–11.9) (5.2–11.6) (6.5–12.2) (5.5–11.7) (7.2–9.6) (4.4–9.9)
6 6 6 6 6 6
the data was not statistically significant (P = 0.52, repeated measures ANOVA). We found weak, but significant, correlations between CH and CCT before the surgery [Spearman correlation coefficient (r) = 0.38, P = 0.04], 1 week after the surgery (r = 0.57, P = 0.001), 1 month after the surgery (r = 0.39, P = 0.04), and 3 months after the surgery (r = 0.48, P = 0.01) (Fig. 1). We also found weak, but significant, correlations between CRF and CCT before the surgery (r = 0.59, P = 0.001), 1 week after the surgery (r = 0.54, P = 0.002), 1 month after the surgery (r = 0.46, P = 0.01), and 3 months after the surgery (r = 0.84, P , 0.001) (Fig. 2).
Subgroup Analysis
In normal eyes, the CH was 9.3 6 1.4 mm Hg preoperatively, 9.3 6 1.4 mm Hg, 9.5 6 1.8 mm Hg, and 8.9 6 1.4 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.49). The CRF was 8.6 6 1.6 mm Hg preoperatively, 9.0 6 1.5 mm Hg, 9.1 6 1.7 mm Hg, and 9.0 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.67). In keratoconic eyes, the CH was 8.4 6 0.6 mm Hg preoperatively, 8.7 6 0.9 mm Hg, 8.1 6
1.4 1.5 1.4 1.5 0.9 1.2
(6.5–11.9) (6.0–11.9) (6.4–12.1) (6.0–12.1) (7.0–10.4) (6.2–10.8)
1-month Postoperative 9.3 8.8 9.5 9.1 8.1 7.4
6 6 6 6 6 6
1.7 1.7 1.8 1.7 0.7 0.6
(5.9–12.7) (5.6–12.1) (6.0–13.0) (5.8–12.3) (6.8–9.4) (6.3–8.5)
3-month Postoperative 8.8 8.8 8.9 9.0 8.4 7.8
6 6 6 6 6 6
1.3 1.6 1.4 1.6 1.2 1.3
(6.2–11.4) (5.8–11.9) (6.2–11.6) (5.9–12.0) (6.0–10.7) (5.4–10.3)
P 0.56 0.52 0.49 0.67 0.83 0.38
0.7 mm Hg, and 8.4 6 1.2 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The CRF was 7.1 6 1.4 mm Hg preoperatively, 8.5 6 1.2 mm Hg, 7.4 6 0.6 mm Hg, and 7.8 6 1.3 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively.
DISCUSSION In this study, we demonstrated that there were no significant changes in corneal biomechanical parameters after ICL implantation, not only in normal eyes but also in keratoconic eyes. Both CH and CRF have been reported to be significantly decreased after a LASIK was performed.19–24 These results indicate that ICL implantation may be a safer surgical approach than a keratorefractive surgery such as LASIK or photorefractive keratectomy, from a biomechanical viewpoint, for both normal and keratoconic eyes. We also demonstrated that both CH and CRF were significantly correlated with CCT preoperatively, and 1 week, 1 month, and 3 months postoperatively. It is suggested that the corneal thickness may play some role in these biomechanical characteristics of the cornea even after ICL implantation. Our results also indicate that CRF may reflect the overall rigidity of the cornea, depending on CCT more correctly than CH does even
FIGURE 1. A scatter plot showing a significant correlation between CH and CCT 3 months after the ICL implantation (r = 0.48, P = 0.01).
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FIGURE 2. A Scatter plot showing a significant correlation between CRF and CCT 3 months after the ICL implantation (r = 0.84, P , 0.001).
in eyes undergoing ICL implantation, as evidenced by the higher correlation coefficient of CCT. To our knowledge, this is the first published study to longitudinally assess corneal biomechanical metrics, not only in normal but also in keratoconic eyes undergoing ICL implantation. Despite the small sample size and the short duration of the follow-up period that impose limitations to our study, we believe that this information is clinically valuable because this surgical technique requiring a 3.0-mm temporal corneal incision can compromise corneal biomechanics with time. Considering that both CH and CRF have been reported to be already compromised in thin corneas and keratoconus.25,26 It is especially important to assess these postoperative parameters in such eyes in a clinical setting. To avoid the possible risk of iatrogenic keratectasia, ICL implantation may have advantages over LASIK in terms of corneal biomechanics, especially in eyes with a thin cornea and those with keratoconus. Regarding corneal biomechanics after cataract surgery, Hager et al27 reported, in a study of 101 eyes having phacoemulsification with IOL implantation through a 4.1-mm corneal incision, that the CH decreased from 10.3 6 2.5 mm Hg preoperatively to 9.2 6 1.9 mm Hg 1 day postoperatively, but that the CCT increased from 556.8 6 32.5 mm to 580.3 6 45.5 mm. In a study of 51 eyes that underwent a cataract surgery through a 2.4-mm corneal incision, Kucumen et al28 showed that CH and CRF decreased in the early postoperative period but that both parameters increased and reached the preoperative levels by 3 months postoperatively. We found a transient decrease in CH and CRF 1 day postoperatively, but this soon recovered to preoperative levels and then became stable afterward during a 3-month follow-up, not only in eyes undergoing phacoemulsification with IOL implantation using a 2.8-mm corneal incision29 but also in those with simultaneous phacoemulsification with IOL implantation and limbal relaxing incisions.30 There have been several reports on ICL implantation in eyes with mild and nonprogressive keratoconus. We first presented two cases of successful toric ICL implantation for the correction of high myopic astigmatism for keratoconic Ó 2014 Lippincott Williams & Wilkins
patients.31 Alfonso et al32 demonstrated that nontoric ICL implantation was a safe, effective, and predictable procedure for the correction of myopia associated with keratoconus. They also reported that the safety and efficacy indices were 1.16 and 1.07 after toric ICL implantation, respectively.33 We also demonstrated, in another prospective study, that toric ICL implantation was beneficial in all measures of safety, efficacy, predictability, and stability for the correction of spherical and cylindrical errors in keratoconic eyes throughout the 6-month follow-up period.34 Our findings may contribute to the prevalence of this surgical technique for mild and nonprogressive keratoconic patients for the correction of refractive errors. The limitations of this study are that the sample data were rather limited in amount and that the follow-up time is short. However, the sample size in this study offered .80% statistical power at the 5% level. Another limitation is a lack of 1-day postoperative measurements. However, the measurements of these parameters 1 day after ICL implantation were not very reliable because of the presence of superficial punctate keratitis, inflammatory responses, or a difficulty in opening the eyes, especially in eyes with keratoconus. Accordingly, we did not assess these parameters immediately after the surgery in this study. In conclusion, our study clarified that there have been no significant changes in corneal biomechanical parameters after ICL implantation in normal or keratoconic eyes. These findings may support the view that ICL implantation may be a safer surgical option for the treatment of eyes with thin corneas or those with mild and nonprogressive keratoconus having ametropia from a biomechanical viewpoint. A large cohort of patients with a longer follow-up is necessary for confirming these preliminary findings.
REFERENCES 1. Zaldivar R, Davidorf JM, Oscherow S. Posterior chamber phakic intraocular lens for myopia of -8 to -19 diopters. J Refract Surg. 1998;14: 294–305.
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2. Binder PS. Ectasia after laser in situ keratomileusis. J Cataract Refract Surg. 2003;29:2419–2429. 3. Espandar L, Meyer JJ, Moshirfar M. Phakic intraocular lenses. Curr Opin Ophthalmol. 2008;19:349–356. 4. Kamiya K, Igarashi A, Shimizu K, et al. Visual performance after posterior chamber phakic intraocular lens implantation and wavefrontguided laser in situ keratomileusis for low to moderate myopia. Am J Ophthalmol. 2012;153:1178–1186. 5. Colin J, Mimouni F, Robinet A, et al. The surgical treatment of high myopia: comparison of epikeratoplasty, keratomileusis and minus power anterior chamber lenses. Refract Corneal Surg. 1990;6:245–251. 6. Fechner PU, van der Heijde GL, Worst JGF. The correction of myopia by lens implantation into phakic eyes. Am J Ophthalmol. 1989;107:659–663. 7. Hoyos JE, Dementiev DD, Cigales M, et al. Phakic refractive lens experience in Spain. J Cataract Refract Surg. 2002;28:1939–1946. 8. Fink AM, Gore C, Rosen E. Cataract development after implantation of the Staar Collamer posterior chamber phakic lens. J Cataract Refract Surg. 1999;25:278–282. 9. Sanders DR, Vukich JA; ICL in Treatment of Myopia (ITM) Study Group. Incidence of lens opacities and clinically significant cataracts with the implantable contact lens: comparison of two lens designs. J Refract Surg. 2002;18:673–682. 10. Roberts C. Biomechanics of the cornea and wavefront-guided laser refractive surgery. J Refract Surg. 2002;18:S589–S592. 11. Kamiya K, Miyata K, Tokunaga T, et al. Structural analysis of the cornea using scanning-slit corneal topography in eyes undergoing excimer laser refractive surgery. Cornea. 2004;23:S59–S64. 12. Jaycock PD, Lobo L, Ibrahim J, et al. Interferometric technique to measure biomechanical changes in the cornea induced by refractive surgery. J Cataract Refract Surg. 2005;31:175–184. 13. Liu J, Roberts CJ. Influence of corneal biomechanical properties on intraocular pressure measurement: quantitative analysis. J Cataract Refract Surg. 2005;31:146–155. 14. Budo C, Bartels MC, van Rij G. Implantation of Artisan toric phakic intraocular lenses for the correction of astigmatism and spherical errors in patients with keratoconus. J Refract Surg. 2005;21:218–222. 15. Colin J, Velou S. Implantation of intacs and a refractive intraocular lens to correct keratoconus. J Cataract Refract Surg. 2003;29:832–834. 16. El-Raggal TM, Abdel Fattah AA. Sequential intacs and verisyse phakic intraocular lens for refractive improvement in keratoconic eyes. J Cataract Refract Surg. 2007;33:966–970. 17. Kamburoglu G, Ertan A, Bahadir M. Implantation of Artisan toric phakic intraocular lens following intacs in a patient with keratoconus. J Cataract Refract Surg. 2007;33:528–530. 18. Coskunseven E, Onder M, Kymionis GD, et al. Combined Intacs and posterior chamber toric implantable collamer lens implantation for keratoconic patients with extreme myopia. Am J Ophthalmol. 2007;144:387–389. 19. Luce DA. Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg. 2005;31:156–162.
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19a.Luce D. Methodology for cornea compensated IOP and CRF for Reichert ORA. ARVO abstract 2266. Invest Ophthalmol Vis Sci. 2006. 20. Ortiz D, Pinero D, Shabayek MH, et al. Corneal biomechanical properties in normal, post-laser in situ keratomileusis and keratoconic eyes. J Cataract Refract Surg. 2007;33:1371–1375. 21. Pepose JS, Feigenbaum SK, Qazi MA, et al. Changes in corneal biomechanics and intraocular pressure following LASIK using static, dynamic, and noncontact tonometry. Am J Ophthalmol. 2007;143: 39–47. 22. Chen MC, Lee N, Bourla N, et al. Corneal biomechanical measurements before and after laser in situ keratomileusis. J Cataract Refract Surg. 2008;34:1886–1891. 23. Kamiya K, Shimizu K, Ohmoto F. Time course of corneal biomechanical parameters after laser in situ keratomileusis. Ophthalmic Res. 2009;42: 167–171. 24. Kamiya K, Shimizu K, Ohmoto F. Comparison of the changes in corneal biomechanical properties after photorefractive keratectomy and laser in situ keratomileusis. Cornea. 2009;28:765–769. 25. Shah S, Laiquzzaman M, Bhojwani R, et al. Assessment of the biomechanical properties of the cornea with the ocular response analyzer in normal and keratoconic eyes. Invest Ophthalmol Vis Sci. 2007;48: 3026–3031. 26. Rabinowitz YS. Keratoconus. Surv Ophthalmol. 1998;42:297–319. 27. Hager A, Loge K, Fullhas MO, et al. Changes in corneal hysteresis after clear corneal cataract surgery. Am J Ophthalmol. 2007;144:341–346. 28. Kucumen RB, Yenerel NM, Gorgun E, et al. Corneal biomechanical properties and intraocular pressure changes after phacoemulsification and intraocular lens implantation. J Cataract Refract Surg. 2008;34: 2096–2098. 29. Kamiya K, Shimizu K, Ohmoto F, et al. Time course of corneal biomechanical parameters after phacoemulsification with intraocular lens implantation. Cornea. 2010;29:1256–1260. 30. Kamiya K, Shimizu K, Ohmoto F, et al. Evaluation of corneal biomechanical parameters after simultaneous phacoemulsification with intraocular lens implantation and limbal relaxing incisions. J Cataract Refract Surg. 2011;37:265–270. 31. Kamiya K, Shimizu K, Ando W, et al. Phakic toric implantable collamer lens implantation for the correction of high myopic astigmatism in eyes with keratoconus. J Refract Surg. 2008;24:840–842. 32. Alfonso JF, Palacios A, Montés-Micó R. Myopic phakic STAAR collamer posterior chamber intraocular lenses for keratoconus. J Refract Surg. 2008;24:867–874. 33. Alfonso JF, Fernández-Vega L, Lisa C, et al. Collagen copolymer toric posterior chamber phakic intraocular lensin eyes with keratoconus. J Cataract Refract Surg. 2010;36:906–916. 34. Kamiya K, Shimizu K, Kobashi H, et al. Clinical outcomes of posterior chamber toric phakic intraocular lens implantation for the correction of high myopic astigmatism in eyes with keratoconus: 6-month follow-up. Graefes Arch Clin Exp Ophthalmol. 2011;249:1073–1080.
Ó 2014 Lippincott Williams & Wilkins
Clinical Evaluation of Corneal Biomechanical Parameters After Posterior Chamber Phakic Intraocular Lens Implantation Mohamed Ali, MD,*† Kazutaka Kamiya, MD, PhD,* Kimiya Shimizu, MD, PhD,* Akihito Igarashi, MD, PhD,* and Rie Ishii, MD, PhD*
Purpose: The aim of this study was to quantitatively assess the changes in corneal biomechanics after posterior chamber phakic intraocular lens (Visian ICL; STAAR Surgical) implantation for normal and keratoconic subjects.
Methods: We retrospectively examined 29 eyes of 16 consecutive patients (mean age 6 SD, 32.4 6 7.3 years) undergoing implantable collamer lens (ICL) implantation through a 3.0-mm temporal corneal incision. We longitudinally assessed the values of corneal hysteresis (CH) and corneal resistance factor (CRF) using an Ocular Response Analyzer. We also investigated the relationship between these biomechanical parameters and central corneal thickness (CCT) preoperatively, and at 1 week, 1 month, and 3 months postoperatively. Results: The CH was 9.2 6 1.4 mm Hg preoperatively, and 9.2 6 1.4
mm Hg, 9.3 6 1.7 mm Hg, and 8.8 6 1.3 mm Hg at 1 week, 1 month, and 3 months postoperatively, respectively. The CRF was 8.4 6 1.6 mm Hg preoperatively, and 9.0 6 1.5 mm Hg, 8.8 6 1.7 mm Hg, and 8.8 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. Multiple comparisons demonstrated no significant differences between measurements made preoperatively and postoperatively (P . 0.05, Dunnett test). Both CH and CRF were significantly correlated with CCT 3 months postoperatively [Spearman correlation coefficient (r) = 0.48, P = 0.01 for CH; r = 0.84, P , 0.001 for CRF].
Conclusions: We found no significant changes in CH or CRF after ICL implantation, not only in normal eyes but also in keratoconic eyes, suggesting that this surgical technique does not significantly affect corneal biomechanical factors. The CCT may play some role in corneal biomechanics even in eyes undergoing ICL implantation. Key Words: corneal biomechanics, corneal hysteresis, corneal resistance factor, corneal thickness, implantable collamer lens (Cornea 2014;33:470–474) Received for publication October 27, 2013; revision received December 19, 2013; accepted January 10, 2014. Published online ahead of print March 7, 2014. From the *Department of Ophthalmology, University of Kitasato School of Medicine, Kanagawa, Japan; and †Department of Ophthalmology, Faculty of Medicine, Minia University Hospitals, Minia, Egypt. K. Shimizu has received consultancy fees from the STAAR Surgical Company. The others authors have no funding or conflicts of interest to disclose. Reprints: Kazutaka Kamiya, Department of Ophthalmology, University of Kitasato School of Medicine, 1-15-1, Kitasato, Sagamihara, Kanagawa 228-8555, Japan (e-mail: [email protected]). Copyright © 2014 by Lippincott Williams & Wilkins
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hakic intraocular lens (IOL) implantation has been widely accepted now as the first surgical option in the field of refractive surgery to correct moderate-to-high myopia in patients who may not be appropriate candidates for undergoing keratorefractive procedures because of having low pachymetric values and post–laser in situ keratomileusis (LASIK) ectasia concerns.1,2 An implantation of the phakic IOL helps patients with high myopia or thin corneas to get rid of glasses or contact lenses without the risk of developing keratectasia caused by LASIK technique,3,4 and has several advantages over LASIK, in terms of fast visual recovery and rehabilitation, excellent refractive accuracy and stability, improved visual acuity, preservation of physiological accommodation, and being a largely reversible procedure.5–7 The Visian Implantable Collamer Lens (STAAR Surgical, Nidau, Switzerland), a posterior chamber phakic IOL, has been reported to be effective for the correction of moderate-tohigh ametropia with better visual performance than that of LASIK.8,9 This surgical technique requires a 3.0-mm temporal corneal incision. Hence, it is theoretically possible that the postoperative biomechanical characteristics, which may play a role not only in the refractive outcomes but also in the measurement of the intraocular pressure (IOP),10–13 might be compromised with time. However, as far as we can ascertain, the time course of corneal biomechanical parameters in implantable collamer lens (ICL)–implanted eyes has not so far been investigated either in normal eyes or in keratoconic eyes. Considering that toric ICL implantation has been reported to be effective for the correction of moderate-to-high myopic astigmatism in keratoconic eyes,14–18 it is also clinically meaningful to assess the changes in corneal biomechanics for keratoconus after ICL implantation. The purpose of this study is to retrospectively assess the time course of corneal biomechanical variables, not only in normal eyes but also in keratoconic eyes, after ICL implantation.
MATERIALS AND METHODS Study Population Twenty-nine eyes of 16 consecutive patients (8 men and 8 women), who underwent an uneventful ICL implantation at the Kitasato University Hospital, and who regularly returned for postoperative examination, were included in this retrospective observational study. The patient age at the time Cornea Volume 33, Number 5, May 2014
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of the surgery was 32.4 6 7.3 years (mean 6 SD) (95% confidence interval, 18.1–46.7 years). The preoperative manifest spherical equivalent was 29.7 6 4.9 (219.3 to 20.2) diopters (D). The preoperative manifest cylinder was 21.09 6 1.08 (23.2 to 1.0 D). The study comprised 25 normal eyes and 4 mild and nonprogressive keratoconic eyes undergoing ICL implantation. The sample size in this study offered 82.3% statistical power at 5% level to detect a 1-mm Hg difference in corneal hysteresis (CH), when the SD of the mean difference was 1.8 mm Hg. The study was approved by the Institutional Review Board of Kitasato University and followed the tenets of the Declaration of Helsinki. Informed consent was obtained from all the patients after an explanation of the nature and possible consequences of the study was given to them.
Surgical Procedure The patients preoperatively underwent 2 peripheral iridotomies with a neodymium-doped yttrium aluminum garnet laser. On the day of the surgery, the patients were given dilating and cycloplegic agents. After topical anesthesia was given, a model V4 ICL was inserted through a 3-mm temporal corneal incision using an injector cartridge (STAAR Surgical) after the placement of a viscosurgical device (Opegan; Santen, Osaka, Japan) into the anterior chamber. The ICL was placed in the posterior chamber, the remaining viscosurgical device was completely washed out of the anterior chamber with balanced salt solution, and a miotic agent was instilled. For toric ICL implantation, to control for potential cyclotorsion in a supine position, the zero horizontal axis was marked preoperatively using a slit lamp. A Mendez ring was also used for intraoperatively measuring the required rotation from the horizontal axis. After that, the ICL had been placed in the posterior chamber and rotated by #22.5° using the manipulator. After the surgery, steroidal (0.1% betamethasone, Rinderon; Shionogi, Osaka, Japan) and antibiotic (levofloxacin, Cravit; Santen, Osaka, Japan) medications were administered topically 4 times daily for 2 weeks, and the dose was steadily reduced thereafter.
Measurements of Corneal Biomechanical Parameters We measured the biomechanical parameters of the cornea, characterized by CH and corneal resistance factor (CRF), using the Ocular Response Analyzer (ORA; Reichert Ophthalmic Instruments, Depew, NY) with software version 2.04, before the surgery and at 1 week, 1 month, and 3 months after the surgery. This device used a rapid air impulse to deform the cornea, and the shape changes were monitored by an electrooptical system. The air puff induced 2 corneal applanations, inward and outward, of the cornea. The air deforms the cornea through an initial applanation event (peak 1), then beyond it into a concavity, and gradually subsides, allowing the cornea to return to its original shape as the applied pressure becomes lower than the IOP, passing through a second applanation (peak 2). The CH was calculated as the difference between pressures (millimeters of mercury) where infrared peaks 1 and 2 occur.19 The CRF Ó 2014 Lippincott Williams & Wilkins
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was calculated as a linear function of P1 and P2, based on the results of a large-scale clinical data analysis, according to the manufacturer.19a We carried out this measurement at least 3 times with the patient in a sitting position with ocular fixation to ensure that there was consistent signal quality and to look for consistent signal morphology and measurement values. The value with the highest waveform score was used for the statistical analysis according to the manufacturer’s instructions. The waveform score is a composite index based on 5 mathematical aspects of the corneal deformation signal. The score ranges from 0 to 10, with a higher score indicating that the signal is closer to an ideal signal from a normal cornea. We confirmed that the waveform scores were $6.5 in all eyes. The central corneal thickness (CCT) was also measured using an ultrasound pachymeter (DGH-500; DGH Technologies, Exton), before the surgery and 1 week, 1 month, and 3 months after the surgery. Topical anesthetic was placed in each eye before the ultrasonic pachymetry.
Statistical Analysis All statistical analyses were performed using Stat View software (version 5.0; SAS Institute, Inc). One-way analysis of variance (ANOVA) was used to evaluate the changes over time course, and the Dunnett test was used for multiple comparisons. The Spearman correlation coefficient (r) was calculated to assess the relationship of CH and CRF with CCT. Unless otherwise indicated, the results are expressed as mean 6 SD, a value of P , 0.05 was considered statistically significant.
RESULTS Patient demographics of the study population are summarized in Table 1. All the surgeries were uneventful, and no significant increase in IOP occurred in any case during the observation period. The results of corneal biomechanical parameters are summarized in Table 2. In the whole study population, the CH was 9.2 6 1.4 mm Hg preoperatively, 9.2 6 1.4 mm Hg, 9.3 6 1.7 mm Hg, and 8.8 6 1.3 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.56, repeated measures ANOVA). The CRF was 8.4 6 1.6 mm Hg preoperatively, 9.0 6 1.5 mm Hg, 8.8 6 1.7 mm Hg, and 8.8 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of
TABLE 1. Preoperative Demographics of Study Population Demographic Parameter Age, yrs Gender (male:female) Manifest spherical equivalent, D Manifest cylinder, D CH, mm Hg CRF, mm Hg CCT, mm
Mean 6 SD (95% Confidence Interval) 32.4 6 7.3 (18.1–46.7) 8:8 29.7 6 4.9 (219.3 to 20.2) 21.09 6 1.08 (23.2 to 1.0) 9.2 6 1.4 (6.4 to 11.9) 8.4 6 1.6 (5.2 to 11.6) 535.1 6 48.9 (439.3 to 631.0)
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TABLE 2. Summary of the Corneal Biomechanical Parameters in Eyes Undergoing ICL Implantation Mean 6 SD (95% Confidence Interval) Study Group Whole study population Normal eyes Keratoconic eyes
Parameter CH (mm Hg) CRF (mm Hg) CH (mm Hg) CRF (mm Hg) CH (mm Hg) CRF (mm Hg)
9.2 8.4 9.3 8.6 8.4 7.1
Preoperative
1-week Postoperative
6 6 6 6 6 6
9.2 9.0 9.3 9.0 8.7 8.5
1.4 1.6 1.4 1.6 0.6 1.4
(6.4–11.9) (5.2–11.6) (6.5–12.2) (5.5–11.7) (7.2–9.6) (4.4–9.9)
6 6 6 6 6 6
the data was not statistically significant (P = 0.52, repeated measures ANOVA). We found weak, but significant, correlations between CH and CCT before the surgery [Spearman correlation coefficient (r) = 0.38, P = 0.04], 1 week after the surgery (r = 0.57, P = 0.001), 1 month after the surgery (r = 0.39, P = 0.04), and 3 months after the surgery (r = 0.48, P = 0.01) (Fig. 1). We also found weak, but significant, correlations between CRF and CCT before the surgery (r = 0.59, P = 0.001), 1 week after the surgery (r = 0.54, P = 0.002), 1 month after the surgery (r = 0.46, P = 0.01), and 3 months after the surgery (r = 0.84, P , 0.001) (Fig. 2).
Subgroup Analysis
In normal eyes, the CH was 9.3 6 1.4 mm Hg preoperatively, 9.3 6 1.4 mm Hg, 9.5 6 1.8 mm Hg, and 8.9 6 1.4 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.49). The CRF was 8.6 6 1.6 mm Hg preoperatively, 9.0 6 1.5 mm Hg, 9.1 6 1.7 mm Hg, and 9.0 6 1.6 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The variance of the data was not statistically significant (P = 0.67). In keratoconic eyes, the CH was 8.4 6 0.6 mm Hg preoperatively, 8.7 6 0.9 mm Hg, 8.1 6
1.4 1.5 1.4 1.5 0.9 1.2
(6.5–11.9) (6.0–11.9) (6.4–12.1) (6.0–12.1) (7.0–10.4) (6.2–10.8)
1-month Postoperative 9.3 8.8 9.5 9.1 8.1 7.4
6 6 6 6 6 6
1.7 1.7 1.8 1.7 0.7 0.6
(5.9–12.7) (5.6–12.1) (6.0–13.0) (5.8–12.3) (6.8–9.4) (6.3–8.5)
3-month Postoperative 8.8 8.8 8.9 9.0 8.4 7.8
6 6 6 6 6 6
1.3 1.6 1.4 1.6 1.2 1.3
(6.2–11.4) (5.8–11.9) (6.2–11.6) (5.9–12.0) (6.0–10.7) (5.4–10.3)
P 0.56 0.52 0.49 0.67 0.83 0.38
0.7 mm Hg, and 8.4 6 1.2 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively. The CRF was 7.1 6 1.4 mm Hg preoperatively, 8.5 6 1.2 mm Hg, 7.4 6 0.6 mm Hg, and 7.8 6 1.3 mm Hg, at 1 week, 1 month, and 3 months postoperatively, respectively.
DISCUSSION In this study, we demonstrated that there were no significant changes in corneal biomechanical parameters after ICL implantation, not only in normal eyes but also in keratoconic eyes. Both CH and CRF have been reported to be significantly decreased after a LASIK was performed.19–24 These results indicate that ICL implantation may be a safer surgical approach than a keratorefractive surgery such as LASIK or photorefractive keratectomy, from a biomechanical viewpoint, for both normal and keratoconic eyes. We also demonstrated that both CH and CRF were significantly correlated with CCT preoperatively, and 1 week, 1 month, and 3 months postoperatively. It is suggested that the corneal thickness may play some role in these biomechanical characteristics of the cornea even after ICL implantation. Our results also indicate that CRF may reflect the overall rigidity of the cornea, depending on CCT more correctly than CH does even
FIGURE 1. A scatter plot showing a significant correlation between CH and CCT 3 months after the ICL implantation (r = 0.48, P = 0.01).
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FIGURE 2. A Scatter plot showing a significant correlation between CRF and CCT 3 months after the ICL implantation (r = 0.84, P , 0.001).
in eyes undergoing ICL implantation, as evidenced by the higher correlation coefficient of CCT. To our knowledge, this is the first published study to longitudinally assess corneal biomechanical metrics, not only in normal but also in keratoconic eyes undergoing ICL implantation. Despite the small sample size and the short duration of the follow-up period that impose limitations to our study, we believe that this information is clinically valuable because this surgical technique requiring a 3.0-mm temporal corneal incision can compromise corneal biomechanics with time. Considering that both CH and CRF have been reported to be already compromised in thin corneas and keratoconus.25,26 It is especially important to assess these postoperative parameters in such eyes in a clinical setting. To avoid the possible risk of iatrogenic keratectasia, ICL implantation may have advantages over LASIK in terms of corneal biomechanics, especially in eyes with a thin cornea and those with keratoconus. Regarding corneal biomechanics after cataract surgery, Hager et al27 reported, in a study of 101 eyes having phacoemulsification with IOL implantation through a 4.1-mm corneal incision, that the CH decreased from 10.3 6 2.5 mm Hg preoperatively to 9.2 6 1.9 mm Hg 1 day postoperatively, but that the CCT increased from 556.8 6 32.5 mm to 580.3 6 45.5 mm. In a study of 51 eyes that underwent a cataract surgery through a 2.4-mm corneal incision, Kucumen et al28 showed that CH and CRF decreased in the early postoperative period but that both parameters increased and reached the preoperative levels by 3 months postoperatively. We found a transient decrease in CH and CRF 1 day postoperatively, but this soon recovered to preoperative levels and then became stable afterward during a 3-month follow-up, not only in eyes undergoing phacoemulsification with IOL implantation using a 2.8-mm corneal incision29 but also in those with simultaneous phacoemulsification with IOL implantation and limbal relaxing incisions.30 There have been several reports on ICL implantation in eyes with mild and nonprogressive keratoconus. We first presented two cases of successful toric ICL implantation for the correction of high myopic astigmatism for keratoconic Ó 2014 Lippincott Williams & Wilkins
patients.31 Alfonso et al32 demonstrated that nontoric ICL implantation was a safe, effective, and predictable procedure for the correction of myopia associated with keratoconus. They also reported that the safety and efficacy indices were 1.16 and 1.07 after toric ICL implantation, respectively.33 We also demonstrated, in another prospective study, that toric ICL implantation was beneficial in all measures of safety, efficacy, predictability, and stability for the correction of spherical and cylindrical errors in keratoconic eyes throughout the 6-month follow-up period.34 Our findings may contribute to the prevalence of this surgical technique for mild and nonprogressive keratoconic patients for the correction of refractive errors. The limitations of this study are that the sample data were rather limited in amount and that the follow-up time is short. However, the sample size in this study offered .80% statistical power at the 5% level. Another limitation is a lack of 1-day postoperative measurements. However, the measurements of these parameters 1 day after ICL implantation were not very reliable because of the presence of superficial punctate keratitis, inflammatory responses, or a difficulty in opening the eyes, especially in eyes with keratoconus. Accordingly, we did not assess these parameters immediately after the surgery in this study. In conclusion, our study clarified that there have been no significant changes in corneal biomechanical parameters after ICL implantation in normal or keratoconic eyes. These findings may support the view that ICL implantation may be a safer surgical option for the treatment of eyes with thin corneas or those with mild and nonprogressive keratoconus having ametropia from a biomechanical viewpoint. A large cohort of patients with a longer follow-up is necessary for confirming these preliminary findings.
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19a.Luce D. Methodology for cornea compensated IOP and CRF for Reichert ORA. ARVO abstract 2266. Invest Ophthalmol Vis Sci. 2006. 20. Ortiz D, Pinero D, Shabayek MH, et al. Corneal biomechanical properties in normal, post-laser in situ keratomileusis and keratoconic eyes. J Cataract Refract Surg. 2007;33:1371–1375. 21. Pepose JS, Feigenbaum SK, Qazi MA, et al. Changes in corneal biomechanics and intraocular pressure following LASIK using static, dynamic, and noncontact tonometry. Am J Ophthalmol. 2007;143: 39–47. 22. Chen MC, Lee N, Bourla N, et al. Corneal biomechanical measurements before and after laser in situ keratomileusis. J Cataract Refract Surg. 2008;34:1886–1891. 23. Kamiya K, Shimizu K, Ohmoto F. Time course of corneal biomechanical parameters after laser in situ keratomileusis. Ophthalmic Res. 2009;42: 167–171. 24. Kamiya K, Shimizu K, Ohmoto F. Comparison of the changes in corneal biomechanical properties after photorefractive keratectomy and laser in situ keratomileusis. Cornea. 2009;28:765–769. 25. Shah S, Laiquzzaman M, Bhojwani R, et al. Assessment of the biomechanical properties of the cornea with the ocular response analyzer in normal and keratoconic eyes. Invest Ophthalmol Vis Sci. 2007;48: 3026–3031. 26. Rabinowitz YS. Keratoconus. Surv Ophthalmol. 1998;42:297–319. 27. Hager A, Loge K, Fullhas MO, et al. Changes in corneal hysteresis after clear corneal cataract surgery. Am J Ophthalmol. 2007;144:341–346. 28. Kucumen RB, Yenerel NM, Gorgun E, et al. Corneal biomechanical properties and intraocular pressure changes after phacoemulsification and intraocular lens implantation. J Cataract Refract Surg. 2008;34: 2096–2098. 29. Kamiya K, Shimizu K, Ohmoto F, et al. Time course of corneal biomechanical parameters after phacoemulsification with intraocular lens implantation. Cornea. 2010;29:1256–1260. 30. Kamiya K, Shimizu K, Ohmoto F, et al. Evaluation of corneal biomechanical parameters after simultaneous phacoemulsification with intraocular lens implantation and limbal relaxing incisions. J Cataract Refract Surg. 2011;37:265–270. 31. Kamiya K, Shimizu K, Ando W, et al. Phakic toric implantable collamer lens implantation for the correction of high myopic astigmatism in eyes with keratoconus. J Refract Surg. 2008;24:840–842. 32. Alfonso JF, Palacios A, Montés-Micó R. Myopic phakic STAAR collamer posterior chamber intraocular lenses for keratoconus. J Refract Surg. 2008;24:867–874. 33. Alfonso JF, Fernández-Vega L, Lisa C, et al. Collagen copolymer toric posterior chamber phakic intraocular lensin eyes with keratoconus. J Cataract Refract Surg. 2010;36:906–916. 34. Kamiya K, Shimizu K, Kobashi H, et al. Clinical outcomes of posterior chamber toric phakic intraocular lens implantation for the correction of high myopic astigmatism in eyes with keratoconus: 6-month follow-up. Graefes Arch Clin Exp Ophthalmol. 2011;249:1073–1080.
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