Seminars in Ophthalmology
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Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy Nicola Rosa MD, Maddalena De Bernardo MD, Stefania Iaccarino MD & Michele Lanza MD To cite this article: Nicola Rosa MD, Maddalena De Bernardo MD, Stefania Iaccarino MD & Michele Lanza MD (2014): Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy, Seminars in Ophthalmology, DOI: 10.3109/08820538.2013.874478 To link to this article: http://dx.doi.org/10.3109/08820538.2013.874478
Published online: 07 Feb 2014.
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Date: 05 November 2015, At: 19:36
Seminars in Ophthalmology, Early Online, 1–7, 2014 ! Informa Healthcare USA, Inc. ISSN: 0882-0538 print / 1744-5205 online DOI: 10.3109/08820538.2013.874478
ORIGINAL ARTICLE
Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy Nicola Rosa, MD1, Maddalena De Bernardo, MD1, Stefania Iaccarino, MD2, and Michele Lanza, MD2,3 1
Department of Medicine and Surgery, University of Salerno, Salerno, Italy, 2Multidisciplinary Department of Medical, Surgical and Dental Specialities, Seconda Universita` di Napoli, Napoli, Italy, and 3Centro Grandi Apparecchiature, Seconda Universita` di Napoli, Napoli, Italy
Seminars in Ophthalmology
ABSTRACT Purpose: To study the corneal biomechanical and morphological changes after photorefractive keratectomy (PRK) and the correlation with morphological parameters. Methods: 119 eyes of 75 subjects with a refraction ranging between 0.50 D and 14.50 D (mean = 4.7 ± 2.3 D) were included in this study. The differences in corneal hysteresis (CH) and corneal resistance factor (CRF) one, three, and six months after PRK have been correlated with effective treatment, central corneal thickness (CCT), and corneal volume (CV) variations at any follow-up utilizing the Pearson Index. Differences between preoperative and postoperative values of the analyzed parameters have been checked with Student T test. Results: Both CH and CRF showed a significant (p50.01) decrease at one, three, and six months’ follow-up. Conclusion: Our findings suggest that after myopic PRK there is a significant decrease of CH and CRF immediately after treatment that remains stable over the follow-up. Keywords: Corneal hysteresis, corneal resistance factor, corneal thickness, myopia, photorefractive keratectomy
INTRODUCTION
Thus far, measuring these parameters has been a difficult task, Pallikaris et al.13 measured the ocular rigidity in living human eyes, increasing IOP by injecting a saline solution into the anterior chamber. Grabner et al.14 used the dynamic corneal imaging method by central indentation to assess the individual elastic properties of the eyes. An Ocular Response Analyzer (ORA), a device able to measure corneal biomechanical parameters, has been described.15,16 It gives in-vivo measurements of two corneal characteristics: (1) the static resistance component (the corneal resistance factor), for which deformation is proportional to applied force; and (2) the dynamic resistance component (corneal hysteresis), in which the relationship between applied force and deformation depends on time.
It has long been suspected that corneal biomechanical properties influence the results and outcome of various ocular measurements and procedures and may influence the diagnosis and the management of ocular diseases. For example, it has been shown that excimer laser ablation affects the postoperative measurement of intraocular pressure (IOP) by Goldmann applanation tonometry (GAT), and various conversion formulas have been proposed to correct IOP measurements as a function of central corneal thickness (CCT) or/and amount of treatment.1–12 However, the difference in IOP measurements before and after photorefractive keratectomy (PRK) could also be related to the changes in biomechanical properties induced by this kind of surgery.
Received 4 July 2013; accepted 8 December 2013; published online 31 January 2014 Correspondence: Nicola Rosa, MD, Department of Medicine and Surgery, University of Salerno, Salerno, Italy. E-mail: [email protected]
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The changes of corneal biomechanical properties in patients undergoing refractive surgery have been studied in different papers17–28 but, among the few that analyzed patients that underwent PRK, none of them evaluated the relations between biomechanical and morphologic corneal parameters in a large population with a wide range of myopic treatments.
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MATERIALS AND METHODS A total of 119 eyes of 75 (40 men, 35 women), which were consecutively treated with PRK for myopia and myopic astigmatism in our department, were included in this nonrandomized, prospective clinical study. The mean age of the patients at the time of refractive surgery was 32 ± 9 years. The spherical equivalent (SE) intended corrections ranged from 0.50 D to 14.50 D (mean 4.7 ± 2.3 D). Patients with systemic and ocular diseases that might interfere with the corneal healing process or with the refractive outcome, such as diabetes, connective tissue disorders, dry eyes, uveitis, corneal and lens opacities, and glaucoma, were excluded from the treatment. Informed consent was obtained from all patients before surgery. The investigational review board of our institution reviewed the protocol and approved the study. Patients were asked to discontinue wearing contact lenses for at least one month before undergoing the final refractive evaluation, which was performed the day the patients underwent PRK. All treatments were performed using topical anesthesia with oxybuprocaine eyedrops (Novesina, Novartis Farma, Origgio, Italy). After a lid speculum was put in place, the epithelium was debrided with a mechanical brush. The patients were treated with an ESIRIS excimer laser (Schwind, Kleinostheim, Germany). No mitomycin C was used in any patient. A bandage contact lens was applied to the treated eye under sterile conditions immediately after surgery, and it remained in place until the epithelium was completely reepithelialized. During the postoperative period, operated eyes received the following medications: diclofenac sodium 0.1% eyedrops twice daily for the first two days; netilmicin preservative-free eyedrops until the epithelialization was complete; and preservative-free artificial tears for one month. After re-epithelialization, clobetasone eyedrops were prescribed for all patients for one month in a tapered dose: one drop four times a day for the first week, one drop three times a day for the second week, one drop twice a day for the third week, and one drop once a day for the last week. The preoperative and follow-up ophthalmic examinations at one, three, and six months included,
among others, an examination with an Oculus Pentacam to obtain corneal morphological parameters and Ocular Response Analyzer (ORA) to record corneal biomechanical parameters. The Oculus Pentacam (Oculus, Wetzlar, Germany, version 1.17r20) uses a rotating Scheimpflug camera and a monochromatic slit light source (blue led at 475 nm) that rotate together around the optical axes of the eye to calculate a three-dimensional model of the anterior segment, including data from anterior and posterior corneal topography measurements of anterior chamber depth, lens opacity, and lens thickness. Within two seconds, the system rotates 180 and acquires 25 or 50 images that contain 500 measurement points on the front and back corneal surface to draw a true elevation map. For this study, 25 images per scan were acquired. Only measurements that passed the automatic quality control of the device have been included in the study. The center of the cornea is measured in each of the single images of a scan. It should be therefore possible to calculate very precise values for the CCT and corneal volume (CV) within a 10 mm circle around the central cornea. The ORA (Reichert Inc., Depew, NY, USA; version 3.01), similar to a non-contact tonometer, uses a metered collimated air pulse to applanate the cornea in the central 3.0 mm diameter and an infrared electrooptical system to record inward (P1) and outward (P2) applanation events. The two applanations take place within approximately 20 milliseconds. The difference between the inward and outward motion applanation pressures is called corneal hysteresis (CH) and is defined as the difference in pressure between P1 and P2. This device is also able to provide another value: a corneal resistance factor (CRF) that is the result of large-scale clinical data analysis, is derived from specific combinations of the inward and outward applanation values using proprietary algorithms, and is defined as a linear function of the two peaks.23 Normal CH values are between 6.1 mm Hg and 17.6 mm Hg.24 From a mathematical standpoint, CRF places more emphasis on P1, so it is more heavily weighted by the underlying corneal elastic properties. CRF is a measurement of the cumulative effects of both the viscous and elastic resistance encountered by the air jet while deforming the corneal surface. CRF exhibits the expected property of increasing at significantly elevated pressures. Normal values for CRF are similar to those for CH.15,29 Recently developed software used in this study provides an automatic analysis of the signal quality in order to reduce any bias related to measurement errors. The normality of the population study distribution has been checked with the Kolmogorov– Smirnov test. Seminars in Ophthalmology
Corneal Hysteresis and PRK 3 Linear regression analysis has been performed between CRF and CH with the refractive treatment, with the CCT difference at the pupil center and CV difference. Differences between preoperative and post-operative parameters have been performed with Student T-test. All the statistical analysis have been done using SPSS (IBM, version 19.0).
RESULTS A significant decrease in both CH and CRF after PRK that remained stable over the follow-up was found (Table 1, Figures 1 and 2). CH and CRF showed a significant difference between preoperative and postoperative values at one month (p50.001 for both), at three months (p50.001 for both), and at six months (p50.001 for both), whereas no difference was found between one and three months (p = 0.05 and 0.07, respectively) and
between three and six months (p = 0.36 and 0.53, respectively). CCT and corneal volume (CV) values before and after surgery are shown in Table 2. The difference in CH showed a good correlation with the difference in CCT, in CV, and with the effective treatment at one month, which tends to decrease over the six-month follow-up, when the correlations became very low and not significant (Table 3). The difference in CRF showed a good correlation with the difference in CCT, in CV, and with the effective treatment one month after PRK, whereas at three- and six-month follow-up correlations between CRF and CV were poor and not significant. The correlation between CRF and the other parameters remained fairly stable (Table 3). No IOP rise has been detected during topical steroid therapy. No significant corneal haze has been observed through six months’ follow-up.
Seminars in Ophthalmology
TABLE 1. Corneal biomechanical properties. Before Surgery
CH mmHg CRF mmHg
1 month
3 months
6 months
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
5.7–14.9 5.1–15.7
10.38 10.68
1.78 2.03
3.6–14.2 3.3–15.0
7.81 7.56
1.7 2.11
4.6–13.4 2.4–12.2
7.97 7.38
1.62 1.8
5.2–13.4 4.3–12.2
8.22 7.47
1.47 1.66
Changes in mmHg of corneal hysteresis (CH) and corneal resistance factor (CRF) before surgery and throughout the follow-up.
FIGURE 1. Changes in CH over the follow-up: the bars represent the mean and standard deviation values of CH at the different follow-up periods (preoperative, one, three, and six months after PRK). !
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Seminars in Ophthalmology
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FIGURE 2. Changes in CRF over the follow-up: the bars represent the mean and standard deviation values of CRF at the different follow-up periods (preoperative, one, three, and six months after PRK). TABLE 2. Corneal morphological changes. Before Surgery
CCT (mm) CV (mm3)
1 month
3 months
6 months
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
500–665 54.5–70.3
562.42 61.98
31.76 3.36
366–581 51.2–66.9
480.34 59.51
47.55 3.58
365–588 53.6–67.7
484.03 60.26
44.44 3.47
385–594 53.1–69.1
490.36 60.75
42.5 3.72
Changes in mm of central corneal thickness (CCT) and changes in mm3 of corneal volume (CV) before surgery and throughout the follow-up. TABLE 3. Correlations between corneal biomechanical properties (CH and CRF) and central corneal thickness (CCT), corneal volume (CV), and effective treatment (ET) at one, three, and six months’ follow-up.
CH versus CCT CH versus CV CH versus ET CRF versus CCT CRF versus CV CRF versus ET
1 MONTH FOLLOW-UP
3 MONTHS FOLLOW-UP
6 MONTHS FOLLOW-UP
R2 = 0.304 p = 0.001 R2 = 0.504 p50.001 R2 = 0.26 p = 0.003 R2 = 0.504 p50.001 R2 = 0.355 p50.001 R2 = 0.441 p50.001
R2 = 0.256 p = 0.009 R2 = 0.168 p = 0.062 R2 = 0.131 p = 0.116 R2 = 0.387 p50.001 R2 = 0.166 p = 0.064 R2 = 0.410 p50.001
R2 = 0.188 p = 0.53 R2 = 0.116 p = 0.16 R2 = 0.005 p = 0.483 R2 = 0.379 p50.001 R2 = 0.165 p = 0.79 R2 = 0.279 p = 0.008
DISCUSSION The changes induced by corneal refractive surgery, in particular LASIK, have been widely studied, but most of the papers deal with the changes in corneal power and/or in corneal thickness30–44; only a few authors have compared the changes in corneal biomechanical
properties after corneal refractive surgery with the entity of treatment and none with change in CV. Thus far, to the best of our knowledge, this is the first study that investigates the relationship between the corneal biomechanical parameters, central corneal thickness, and corneal volume in a group of patients with a very wide range of myopic correction. Luce,29 in 10 patients after LASIK, found a general decrease of CH a few days after the treatment (the Seminars in Ophthalmology
Seminars in Ophthalmology
Corneal Hysteresis and PRK 5 follow-up was seven days), but no information was given on the amount of treatment or on the correlation with the effective treatment. Ortiz et al.16 studied 65 eyes of 39 patients who underwent LASIK with a mean refractive error of 4.25 to ± 3.00 D (range 13.00 to 1.25 D). The authors found a decrease in CH, CRF, and corneal compensated IOP (IOPcc), and observed a good correlation between the corrected refractive defect and change in biomechanical properties. They hypothesized that the flap creation and the corneal thinning, caused by the ablation, weaken the cornea, inducing a change in CH and CRF. As this weakness could be responsible for corneal ectasia after refractive surgery, the authors suggested considering a corneal biomechanical measurement as a new indicator in the screening of candidates for refractive surgery. Pepose et al.17 measured IOP with GAT, dynamic contour tonometer (DCT), and ORA before and after myopic LASIK in 66 eyes of 33 patients (19 women and 14 men), with a mean refraction of 5.1 ± 2.8 D and found a significant decrease in CH and CRF after the refractive treatment. Kirwan et al.18 studied 63 eyes that had undergone LASIK and 21 eyes that had undergone LASEK. They found a statistically significant decrease in hysteresis following LASIK (p50.01) and LASEK (p50.01), with similar decrements observed in both treatment groups, a moderate correlation between postoperative hysteresis and postoperative CCT in LASIK (r = 0.7) and LASEK (r = 0.7) treated eyes, and a weak correlation between postoperative decrease in hysteresis and the parameters examined. Wallau et al.19 compared two groups of patients undergoing corneal refractive surgery with PRK and mitomycin C and LASIK. The authors found CH and CRF to be lower in the PRK group compared to the LASIK one but, unfortunately, they did not perform ORA examination on the patients before surgery. Hamilton et al.20 studied changes in eyes that underwent PRK, LASIK with femtosecond laser and with microkeratome, comparing the refractive results. They also evaluated the corneal biomechanical properties of the two groups of patients before and after surgery, and femtosecond laser LASIK eyes had a very good correlation between difference in CH and ablation depth. They hypotized that PRK could have less effect then LASIK on biomechanical properties of the cornea. Qazi et al.21 evaluated IOP in patients who underwent LASEK and LASIK, finding a not significant difference in IOP measured with dynamic contour tonometry before and after surgery. GAT and ORA provided different IOP measurements before and after surgery. After surgery, they found lower CH values in the LASIK group. Reductions in CH, CRF, !
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and CCT were moderately correlated with ablation depth. Kamiya et al.22 compared the biomechanical property changes after LASIK (31 eyes) and after PRK (27 eyes) in myopic eyes. They found a reduction of CH and CRF, but the differences at three months’ follow-up were higher in LASIK eyes. The authors found a correlation between the difference in CH and CRF and the amount of myopic correction both in LASIK and in PRK eyes. Slade et al.,25 in a prospective randomized study, analyzed 100 eyes of 50 patients whoi underwent PRK in one eye and sub-Bowman keratomileusis (SBK) in the fellow eye for myopia or myopic astigmatism. Analyzing the biomechanical parameters, they found a reduction of both CH and CRF postoperatively after PRK and SBK. De Medeiros et al.26 investigated 13 eyes of 13 myopic patients that underwent LASIK and 11 eyes of 11 hyperopic patients. In the myopic group, one week after treatment, they found a significant decrease of both CH and CRF; moreover, they showed the CRF reduction to be correlated with the number of excimer laser pulses delivered, whereas the CH change was related to the preoperative CH value. Shah et al.27 examined 41 patients divided into three groups: LASEK for myopia, LASIK for myopia, and LASIK for hyperopia. They evaluated biomechanical parameters before and three months after treatment. Mean IOPg, CH, and CRF decreased after treatment in each group, whereas mean IOPcc increased. They found no influence of age, ablation, pre-op CCT values on IOPg, IOPcc, CH and CRF differences. Shah et al.28 conducted another prospective comparison of 110 eyes divided into two groups: LASIK and LASEK. CH, CRF, and CCT were analyzed before and after treatment, showing a significant reduction of all three examined parameters in both groups. Our findings seem to be similar to those obtained by Kirwan et al.18 because we could not find a correlation between CH and with the difference in CCT six months after refractive surgery, but they didn’t analyze the CRF change correlations. CRF is defined as a parameter with an intrinsic relation to CCT.15 This could be the reason we observed a good correlation between CRF differences with CCT changes and effective treatment six months after PRK. We observed a decrease in the correlation between CRF and CV over the six-month follow-up. In our opinion, there are two reasons for this finding: first, after PRK, the retraction of the cut lamellae, increasing the peripheral thickening, does not reflect the effective tissue ablation; second, ORA is not able to properly measure this parameter. Instead, CH showed a correlation with the other three parameters (CCT difference, CV difference, and effective
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treatment) one month after surgery, whereas at three and six months’ follow-up it become very low (Table 3). The possible explanation for this finding could be, as we stated earlier, that the cornea undergoes a more complex re-organization of its own structure after PRK that ORA is not able to detect.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
Seminars in Ophthalmology
REFERENCES 1. Montes-Mico R, Charman WN. Intraocular pressure after excimer laser myopic refractive surgery. Ophthalmic Physiol Opt 2001;21:228–235. 2. Rosa N, Cennamo G, Breve M, La Rana A. Goldmann applanation tonometry after myopic photorefractive keratectomy. Acta Ophthalmol Scand 1998;76:550–554. 3. Munger R, Hodge WG, Mintsioulis G, et al. Correction of intraocular pressure for changes in central corneal thickness following photorefractive keratectomy. Can J Ophthalmol 1998;33:159–165. 4. Emara B, Probst LE, Tingey DP, et al. Correlation of intraocular pressure and central corneal thickness in normal myopic eyes and after laser in situ keratomileusis. J Cataract Refract Surg 1998;24:1320–1325. 5. Duch S, Serra A, Castanera J, et al. Tonometry after laser in situ keratomileusis treatment. J Glaucoma 2001;10:261–265. 6. Cheng AC, Fan D, Tang E, Lam DS. Effect of corneal curvature and corneal thickness on the assessment of intraocular pressure using noncontact tonometry in patients after myopic LASIK surgery. Cornea 2006;25:26–28. 7. Rashad KM, Bahnassy AA. Changes in intraocular pressure after laser in situ keratomileusis. J Refract Surg 2001;17: 420–427. 8. Arimoto A, Shimizu K, Shoji N, et al. Underestimation of intraocular pressure in eyes after laser in situ keratomileusis. Jpn J Ophthalmol 2002;46:645–649. 9. Svedberg H, Chen E, Hamberg-Nystro¨m H. Changes in corneal thickness and curvature after different excimer laser photorefractive procedures and their impact on intraocular pressure measurements. Graefes Arch Clin Exp Ophthalmol 2005;243:1218–1220. 10. Chihara E, Takahashi H, Okazaki K, et al. The preoperative intraocular pressure level predicts the amount of underestimated intraocular pressure after LASIK for myopia. Br J Ophthalmol 2005;89:160–164. 11. Kohlhaas M, Spoerl E, Boehm AG, Pollack K. A correction formula for the real intraocular pressure after LASIK for the correction of myopic astigmatism. J Refract Surg 2006; 22:263–267. 12. Chatterjee A, Shah S, Bessant DA, et al. Reduction in intraocular pressure after excimer laser photorefractive keratectomy: Correlation with pretreatment myopia. Ophthalmology 1997;104:355–359. 13. Pallikaris IG, Kymionis GD, Ginis HS, et al. Ocular rigidity in living human eyes. Invest Ophthalmol Vis Sci 2005;46: 409–414.
14. Grabner G, Eilmsteiner R, Steindl C, et al. Dynamic corneal imaging. J Cataract Refract Surg 2005;31:163–174. 15. Luce DA. Determining in vivo biomechanical properties of the cornea with an ocular response analyzer. J Cataract Refract Surg 2005;31:156–162. 16. Ortiz D, Pin˜ero 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. 17. 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. 18. Kirwan C, O’Keefe M. Corneal hysteresis using the Reichert ocular response analyzer: Findings pre and post LASIK and LASEK. Acta Ophthalm 2008;86: 215–218. 19. Wallau AD, Campos M. One-year outcomes of a bilateral randomised prospective clinical trial comparing PRK with mitomycin C and LASIK. Br J Ophthalmol 2009;93: 1634–1638. 20. Hamilton DR, Johnson RD, Lee N, Bourla N. Differences in the corneal biomechanical effects of surface ablation compared with laser in situ keratomileusis using a microkeratome or femtosecond laser. J Cataract Refract Surg 2008;34:2049–2056. 21. Qazi MA, Sanderson JP, Mahmoud AM, et al. Postoperative changes in intraocular pressure and corneal biomechanical metrics: Laser in situ keratomileusis versus laser-assisted subepithelial keratectomy. J Cataract Refract Surg 2009;35:1774–1788. 22. 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. 23. Touboul D, Roberts C, Ke´rautret J, et al. Correlations between corneal hysteresis, intraocular pressure, and corneal central pachymetry. J Cataract Refract Surg 2008; 34:616–622. 24. Shah S, Laiquzzamann M, Cunliffe I, Mantry S. The use of Reichert Ocular Response analyzer to establish the relationship between corneal hysteresis, corneal resistance factor and central corneal thickness in normal eyes. Contact Lens and Anterior Eyes 2006;29: 257–262. 25. Slade S, Durrie DS, Binder PS. A prospective, contralateral eye study comparing thin-flap LASIK (sub-Bowman keratomileusis) with photorefractive keratectomy. Ophthalmology 2009;116:1075–1082. 26. de Medeiros FW, Sinha-Roy A, Alves MR, et al. Differences in the early biomechanical effects of hyperopic and myopic laser in situ keratomileusis. J Cataract Refract Surg 2010;36: 947–949. 27. Shah S, Laiquzzaman M, Yeung I, et al. The use of the Ocular Response Analyser to determine corneal hysteresis in eyes before and after excimer laser refractive surgery. Cont Lens Anterior Eye 2009;32:123–128. 28. Shah S, Laiquzzaman M. Comparison of corneal biomechanics in pre and post-refractive surgery and keratoconic eyes by Ocular Response Analyser. Cont Lens Anterior Eye 2009;32:29–32. 29. Luce D, Taylor D. Reichert ocular response analyzer measures corneal biomechanical properties and IOP provides new indicators for corneal specialties and glaucoma management. Depew, NY: Reichert Ophthalmic Instruments, March 2006. 30. Cantera E, Cantera I, Olivieri L. Corneal topographic analysis of photorefractive keratectomy in 175 myopic eyes. Refract Corneal Surg 1993;9:S19–S22. Seminars in Ophthalmology
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31. Chen S, Hu FR. Correlation between refractive and measured corneal power changes after myopic excimer laser photorefractive keratectomy. J Cataract Refract Surg 2002;28:603–610. 32. Hersh PS, Schwartz Goldstein BH. Corneal topography of phase III excimer laser photorefractive keratectomy: Characterization and clinical effects. Ophthalmology 1995; 102:963–978. 33. Hersh PS. A standardized classification of corneal topography after laser refractive surgery. J Refract Surg 1997;13: 571–578. 34. Rosa N, Lanza M, Capasso L, et al. Anterior chamber depth measurement before and after photorefractive keratectomy: Comparison between IOL Master and Orbscan II. Ophthalmology 2006;113:962–969. 35. Hugger P, Kohnen T, La Rosa FA, et al. Comparison of changes in manifest refraction and corneal power after photorefractive keratectomy. Am J Ophthalmol 2000;129: 68–75. 36. Lin DT. Corneal topographic analysis after excimer photorefractive keratectomy. Ophthalmology 1994;101:1432–1439. 37. Maeda N, Klyce SD, Smolek MK, McDonald MB. Disparity between keratometry-style readings and corneal power within the pupil after refractive surgery for myopia. Cornea 1997;16:517–524.
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38. Peter R, Hazeghi M, Job O, et al. Manual keratometry and videokeratography after photorefractive keratectomy. J Cataract Refract Surg 2000;26:1748–1752. 39. Rosa N, Cennamo G, Pasquariello A, et al. Refractive outcome and corneal topographic studies after photorefractive keratectomy with different sized ablation zones. Ophthalmology 1996;103:1130–1338. 40. Rosa N, Cennamo G, Rinaldi M. Correlation between refractive and corneal topographic changes after photorefractive keratectomy for myopia. J Refract Surg 2001;17: 129–133. 41. Rosa N, Furgiuele D, Lanza M, et al. Correlation of changes in refraction and corneal topography after photorefractive keratectomy. J Refract Surg 2004;20:478–483. 42. Wilson SE, Klyce SD, McDonald MB, et al. Changes in corneal topography after excimer laser photorefractive keratectomy for myopia. Ophthalmology 1991;98: 1338–1347. 43. Smith RJ, Chan WK, Maloney RK. The prediction of surgically induced refractive change from corneal topography. Am J Ophthalmol 1998;125:44–53. 44. Cennamo G, Rosa N, Guida E, et al. Evaluation of corneal thickness and endothelial cells before and after excimer laser photorefractive keratectomy. J Refract Corneal Surg 1994;10:137–141.
ISSN: 0882-0538 (Print) 1744-5205 (Online) Journal homepage: http://www.tandfonline.com/loi/isio20
Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy Nicola Rosa MD, Maddalena De Bernardo MD, Stefania Iaccarino MD & Michele Lanza MD To cite this article: Nicola Rosa MD, Maddalena De Bernardo MD, Stefania Iaccarino MD & Michele Lanza MD (2014): Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy, Seminars in Ophthalmology, DOI: 10.3109/08820538.2013.874478 To link to this article: http://dx.doi.org/10.3109/08820538.2013.874478
Published online: 07 Feb 2014.
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Date: 05 November 2015, At: 19:36
Seminars in Ophthalmology, Early Online, 1–7, 2014 ! Informa Healthcare USA, Inc. ISSN: 0882-0538 print / 1744-5205 online DOI: 10.3109/08820538.2013.874478
ORIGINAL ARTICLE
Corneal Biomechanical Changes After Myopic Photorefractive Keratectomy Nicola Rosa, MD1, Maddalena De Bernardo, MD1, Stefania Iaccarino, MD2, and Michele Lanza, MD2,3 1
Department of Medicine and Surgery, University of Salerno, Salerno, Italy, 2Multidisciplinary Department of Medical, Surgical and Dental Specialities, Seconda Universita` di Napoli, Napoli, Italy, and 3Centro Grandi Apparecchiature, Seconda Universita` di Napoli, Napoli, Italy
Seminars in Ophthalmology
ABSTRACT Purpose: To study the corneal biomechanical and morphological changes after photorefractive keratectomy (PRK) and the correlation with morphological parameters. Methods: 119 eyes of 75 subjects with a refraction ranging between 0.50 D and 14.50 D (mean = 4.7 ± 2.3 D) were included in this study. The differences in corneal hysteresis (CH) and corneal resistance factor (CRF) one, three, and six months after PRK have been correlated with effective treatment, central corneal thickness (CCT), and corneal volume (CV) variations at any follow-up utilizing the Pearson Index. Differences between preoperative and postoperative values of the analyzed parameters have been checked with Student T test. Results: Both CH and CRF showed a significant (p50.01) decrease at one, three, and six months’ follow-up. Conclusion: Our findings suggest that after myopic PRK there is a significant decrease of CH and CRF immediately after treatment that remains stable over the follow-up. Keywords: Corneal hysteresis, corneal resistance factor, corneal thickness, myopia, photorefractive keratectomy
INTRODUCTION
Thus far, measuring these parameters has been a difficult task, Pallikaris et al.13 measured the ocular rigidity in living human eyes, increasing IOP by injecting a saline solution into the anterior chamber. Grabner et al.14 used the dynamic corneal imaging method by central indentation to assess the individual elastic properties of the eyes. An Ocular Response Analyzer (ORA), a device able to measure corneal biomechanical parameters, has been described.15,16 It gives in-vivo measurements of two corneal characteristics: (1) the static resistance component (the corneal resistance factor), for which deformation is proportional to applied force; and (2) the dynamic resistance component (corneal hysteresis), in which the relationship between applied force and deformation depends on time.
It has long been suspected that corneal biomechanical properties influence the results and outcome of various ocular measurements and procedures and may influence the diagnosis and the management of ocular diseases. For example, it has been shown that excimer laser ablation affects the postoperative measurement of intraocular pressure (IOP) by Goldmann applanation tonometry (GAT), and various conversion formulas have been proposed to correct IOP measurements as a function of central corneal thickness (CCT) or/and amount of treatment.1–12 However, the difference in IOP measurements before and after photorefractive keratectomy (PRK) could also be related to the changes in biomechanical properties induced by this kind of surgery.
Received 4 July 2013; accepted 8 December 2013; published online 31 January 2014 Correspondence: Nicola Rosa, MD, Department of Medicine and Surgery, University of Salerno, Salerno, Italy. E-mail: [email protected]
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The changes of corneal biomechanical properties in patients undergoing refractive surgery have been studied in different papers17–28 but, among the few that analyzed patients that underwent PRK, none of them evaluated the relations between biomechanical and morphologic corneal parameters in a large population with a wide range of myopic treatments.
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MATERIALS AND METHODS A total of 119 eyes of 75 (40 men, 35 women), which were consecutively treated with PRK for myopia and myopic astigmatism in our department, were included in this nonrandomized, prospective clinical study. The mean age of the patients at the time of refractive surgery was 32 ± 9 years. The spherical equivalent (SE) intended corrections ranged from 0.50 D to 14.50 D (mean 4.7 ± 2.3 D). Patients with systemic and ocular diseases that might interfere with the corneal healing process or with the refractive outcome, such as diabetes, connective tissue disorders, dry eyes, uveitis, corneal and lens opacities, and glaucoma, were excluded from the treatment. Informed consent was obtained from all patients before surgery. The investigational review board of our institution reviewed the protocol and approved the study. Patients were asked to discontinue wearing contact lenses for at least one month before undergoing the final refractive evaluation, which was performed the day the patients underwent PRK. All treatments were performed using topical anesthesia with oxybuprocaine eyedrops (Novesina, Novartis Farma, Origgio, Italy). After a lid speculum was put in place, the epithelium was debrided with a mechanical brush. The patients were treated with an ESIRIS excimer laser (Schwind, Kleinostheim, Germany). No mitomycin C was used in any patient. A bandage contact lens was applied to the treated eye under sterile conditions immediately after surgery, and it remained in place until the epithelium was completely reepithelialized. During the postoperative period, operated eyes received the following medications: diclofenac sodium 0.1% eyedrops twice daily for the first two days; netilmicin preservative-free eyedrops until the epithelialization was complete; and preservative-free artificial tears for one month. After re-epithelialization, clobetasone eyedrops were prescribed for all patients for one month in a tapered dose: one drop four times a day for the first week, one drop three times a day for the second week, one drop twice a day for the third week, and one drop once a day for the last week. The preoperative and follow-up ophthalmic examinations at one, three, and six months included,
among others, an examination with an Oculus Pentacam to obtain corneal morphological parameters and Ocular Response Analyzer (ORA) to record corneal biomechanical parameters. The Oculus Pentacam (Oculus, Wetzlar, Germany, version 1.17r20) uses a rotating Scheimpflug camera and a monochromatic slit light source (blue led at 475 nm) that rotate together around the optical axes of the eye to calculate a three-dimensional model of the anterior segment, including data from anterior and posterior corneal topography measurements of anterior chamber depth, lens opacity, and lens thickness. Within two seconds, the system rotates 180 and acquires 25 or 50 images that contain 500 measurement points on the front and back corneal surface to draw a true elevation map. For this study, 25 images per scan were acquired. Only measurements that passed the automatic quality control of the device have been included in the study. The center of the cornea is measured in each of the single images of a scan. It should be therefore possible to calculate very precise values for the CCT and corneal volume (CV) within a 10 mm circle around the central cornea. The ORA (Reichert Inc., Depew, NY, USA; version 3.01), similar to a non-contact tonometer, uses a metered collimated air pulse to applanate the cornea in the central 3.0 mm diameter and an infrared electrooptical system to record inward (P1) and outward (P2) applanation events. The two applanations take place within approximately 20 milliseconds. The difference between the inward and outward motion applanation pressures is called corneal hysteresis (CH) and is defined as the difference in pressure between P1 and P2. This device is also able to provide another value: a corneal resistance factor (CRF) that is the result of large-scale clinical data analysis, is derived from specific combinations of the inward and outward applanation values using proprietary algorithms, and is defined as a linear function of the two peaks.23 Normal CH values are between 6.1 mm Hg and 17.6 mm Hg.24 From a mathematical standpoint, CRF places more emphasis on P1, so it is more heavily weighted by the underlying corneal elastic properties. CRF is a measurement of the cumulative effects of both the viscous and elastic resistance encountered by the air jet while deforming the corneal surface. CRF exhibits the expected property of increasing at significantly elevated pressures. Normal values for CRF are similar to those for CH.15,29 Recently developed software used in this study provides an automatic analysis of the signal quality in order to reduce any bias related to measurement errors. The normality of the population study distribution has been checked with the Kolmogorov– Smirnov test. Seminars in Ophthalmology
Corneal Hysteresis and PRK 3 Linear regression analysis has been performed between CRF and CH with the refractive treatment, with the CCT difference at the pupil center and CV difference. Differences between preoperative and post-operative parameters have been performed with Student T-test. All the statistical analysis have been done using SPSS (IBM, version 19.0).
RESULTS A significant decrease in both CH and CRF after PRK that remained stable over the follow-up was found (Table 1, Figures 1 and 2). CH and CRF showed a significant difference between preoperative and postoperative values at one month (p50.001 for both), at three months (p50.001 for both), and at six months (p50.001 for both), whereas no difference was found between one and three months (p = 0.05 and 0.07, respectively) and
between three and six months (p = 0.36 and 0.53, respectively). CCT and corneal volume (CV) values before and after surgery are shown in Table 2. The difference in CH showed a good correlation with the difference in CCT, in CV, and with the effective treatment at one month, which tends to decrease over the six-month follow-up, when the correlations became very low and not significant (Table 3). The difference in CRF showed a good correlation with the difference in CCT, in CV, and with the effective treatment one month after PRK, whereas at three- and six-month follow-up correlations between CRF and CV were poor and not significant. The correlation between CRF and the other parameters remained fairly stable (Table 3). No IOP rise has been detected during topical steroid therapy. No significant corneal haze has been observed through six months’ follow-up.
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TABLE 1. Corneal biomechanical properties. Before Surgery
CH mmHg CRF mmHg
1 month
3 months
6 months
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
5.7–14.9 5.1–15.7
10.38 10.68
1.78 2.03
3.6–14.2 3.3–15.0
7.81 7.56
1.7 2.11
4.6–13.4 2.4–12.2
7.97 7.38
1.62 1.8
5.2–13.4 4.3–12.2
8.22 7.47
1.47 1.66
Changes in mmHg of corneal hysteresis (CH) and corneal resistance factor (CRF) before surgery and throughout the follow-up.
FIGURE 1. Changes in CH over the follow-up: the bars represent the mean and standard deviation values of CH at the different follow-up periods (preoperative, one, three, and six months after PRK). !
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FIGURE 2. Changes in CRF over the follow-up: the bars represent the mean and standard deviation values of CRF at the different follow-up periods (preoperative, one, three, and six months after PRK). TABLE 2. Corneal morphological changes. Before Surgery
CCT (mm) CV (mm3)
1 month
3 months
6 months
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
Range
Mean
SD
500–665 54.5–70.3
562.42 61.98
31.76 3.36
366–581 51.2–66.9
480.34 59.51
47.55 3.58
365–588 53.6–67.7
484.03 60.26
44.44 3.47
385–594 53.1–69.1
490.36 60.75
42.5 3.72
Changes in mm of central corneal thickness (CCT) and changes in mm3 of corneal volume (CV) before surgery and throughout the follow-up. TABLE 3. Correlations between corneal biomechanical properties (CH and CRF) and central corneal thickness (CCT), corneal volume (CV), and effective treatment (ET) at one, three, and six months’ follow-up.
CH versus CCT CH versus CV CH versus ET CRF versus CCT CRF versus CV CRF versus ET
1 MONTH FOLLOW-UP
3 MONTHS FOLLOW-UP
6 MONTHS FOLLOW-UP
R2 = 0.304 p = 0.001 R2 = 0.504 p50.001 R2 = 0.26 p = 0.003 R2 = 0.504 p50.001 R2 = 0.355 p50.001 R2 = 0.441 p50.001
R2 = 0.256 p = 0.009 R2 = 0.168 p = 0.062 R2 = 0.131 p = 0.116 R2 = 0.387 p50.001 R2 = 0.166 p = 0.064 R2 = 0.410 p50.001
R2 = 0.188 p = 0.53 R2 = 0.116 p = 0.16 R2 = 0.005 p = 0.483 R2 = 0.379 p50.001 R2 = 0.165 p = 0.79 R2 = 0.279 p = 0.008
DISCUSSION The changes induced by corneal refractive surgery, in particular LASIK, have been widely studied, but most of the papers deal with the changes in corneal power and/or in corneal thickness30–44; only a few authors have compared the changes in corneal biomechanical
properties after corneal refractive surgery with the entity of treatment and none with change in CV. Thus far, to the best of our knowledge, this is the first study that investigates the relationship between the corneal biomechanical parameters, central corneal thickness, and corneal volume in a group of patients with a very wide range of myopic correction. Luce,29 in 10 patients after LASIK, found a general decrease of CH a few days after the treatment (the Seminars in Ophthalmology
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Corneal Hysteresis and PRK 5 follow-up was seven days), but no information was given on the amount of treatment or on the correlation with the effective treatment. Ortiz et al.16 studied 65 eyes of 39 patients who underwent LASIK with a mean refractive error of 4.25 to ± 3.00 D (range 13.00 to 1.25 D). The authors found a decrease in CH, CRF, and corneal compensated IOP (IOPcc), and observed a good correlation between the corrected refractive defect and change in biomechanical properties. They hypothesized that the flap creation and the corneal thinning, caused by the ablation, weaken the cornea, inducing a change in CH and CRF. As this weakness could be responsible for corneal ectasia after refractive surgery, the authors suggested considering a corneal biomechanical measurement as a new indicator in the screening of candidates for refractive surgery. Pepose et al.17 measured IOP with GAT, dynamic contour tonometer (DCT), and ORA before and after myopic LASIK in 66 eyes of 33 patients (19 women and 14 men), with a mean refraction of 5.1 ± 2.8 D and found a significant decrease in CH and CRF after the refractive treatment. Kirwan et al.18 studied 63 eyes that had undergone LASIK and 21 eyes that had undergone LASEK. They found a statistically significant decrease in hysteresis following LASIK (p50.01) and LASEK (p50.01), with similar decrements observed in both treatment groups, a moderate correlation between postoperative hysteresis and postoperative CCT in LASIK (r = 0.7) and LASEK (r = 0.7) treated eyes, and a weak correlation between postoperative decrease in hysteresis and the parameters examined. Wallau et al.19 compared two groups of patients undergoing corneal refractive surgery with PRK and mitomycin C and LASIK. The authors found CH and CRF to be lower in the PRK group compared to the LASIK one but, unfortunately, they did not perform ORA examination on the patients before surgery. Hamilton et al.20 studied changes in eyes that underwent PRK, LASIK with femtosecond laser and with microkeratome, comparing the refractive results. They also evaluated the corneal biomechanical properties of the two groups of patients before and after surgery, and femtosecond laser LASIK eyes had a very good correlation between difference in CH and ablation depth. They hypotized that PRK could have less effect then LASIK on biomechanical properties of the cornea. Qazi et al.21 evaluated IOP in patients who underwent LASEK and LASIK, finding a not significant difference in IOP measured with dynamic contour tonometry before and after surgery. GAT and ORA provided different IOP measurements before and after surgery. After surgery, they found lower CH values in the LASIK group. Reductions in CH, CRF, !
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and CCT were moderately correlated with ablation depth. Kamiya et al.22 compared the biomechanical property changes after LASIK (31 eyes) and after PRK (27 eyes) in myopic eyes. They found a reduction of CH and CRF, but the differences at three months’ follow-up were higher in LASIK eyes. The authors found a correlation between the difference in CH and CRF and the amount of myopic correction both in LASIK and in PRK eyes. Slade et al.,25 in a prospective randomized study, analyzed 100 eyes of 50 patients whoi underwent PRK in one eye and sub-Bowman keratomileusis (SBK) in the fellow eye for myopia or myopic astigmatism. Analyzing the biomechanical parameters, they found a reduction of both CH and CRF postoperatively after PRK and SBK. De Medeiros et al.26 investigated 13 eyes of 13 myopic patients that underwent LASIK and 11 eyes of 11 hyperopic patients. In the myopic group, one week after treatment, they found a significant decrease of both CH and CRF; moreover, they showed the CRF reduction to be correlated with the number of excimer laser pulses delivered, whereas the CH change was related to the preoperative CH value. Shah et al.27 examined 41 patients divided into three groups: LASEK for myopia, LASIK for myopia, and LASIK for hyperopia. They evaluated biomechanical parameters before and three months after treatment. Mean IOPg, CH, and CRF decreased after treatment in each group, whereas mean IOPcc increased. They found no influence of age, ablation, pre-op CCT values on IOPg, IOPcc, CH and CRF differences. Shah et al.28 conducted another prospective comparison of 110 eyes divided into two groups: LASIK and LASEK. CH, CRF, and CCT were analyzed before and after treatment, showing a significant reduction of all three examined parameters in both groups. Our findings seem to be similar to those obtained by Kirwan et al.18 because we could not find a correlation between CH and with the difference in CCT six months after refractive surgery, but they didn’t analyze the CRF change correlations. CRF is defined as a parameter with an intrinsic relation to CCT.15 This could be the reason we observed a good correlation between CRF differences with CCT changes and effective treatment six months after PRK. We observed a decrease in the correlation between CRF and CV over the six-month follow-up. In our opinion, there are two reasons for this finding: first, after PRK, the retraction of the cut lamellae, increasing the peripheral thickening, does not reflect the effective tissue ablation; second, ORA is not able to properly measure this parameter. Instead, CH showed a correlation with the other three parameters (CCT difference, CV difference, and effective
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treatment) one month after surgery, whereas at three and six months’ follow-up it become very low (Table 3). The possible explanation for this finding could be, as we stated earlier, that the cornea undergoes a more complex re-organization of its own structure after PRK that ORA is not able to detect.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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38. Peter R, Hazeghi M, Job O, et al. Manual keratometry and videokeratography after photorefractive keratectomy. J Cataract Refract Surg 2000;26:1748–1752. 39. Rosa N, Cennamo G, Pasquariello A, et al. Refractive outcome and corneal topographic studies after photorefractive keratectomy with different sized ablation zones. Ophthalmology 1996;103:1130–1338. 40. Rosa N, Cennamo G, Rinaldi M. Correlation between refractive and corneal topographic changes after photorefractive keratectomy for myopia. J Refract Surg 2001;17: 129–133. 41. Rosa N, Furgiuele D, Lanza M, et al. Correlation of changes in refraction and corneal topography after photorefractive keratectomy. J Refract Surg 2004;20:478–483. 42. Wilson SE, Klyce SD, McDonald MB, et al. Changes in corneal topography after excimer laser photorefractive keratectomy for myopia. Ophthalmology 1991;98: 1338–1347. 43. Smith RJ, Chan WK, Maloney RK. The prediction of surgically induced refractive change from corneal topography. Am J Ophthalmol 1998;125:44–53. 44. Cennamo G, Rosa N, Guida E, et al. Evaluation of corneal thickness and endothelial cells before and after excimer laser photorefractive keratectomy. J Refract Corneal Surg 1994;10:137–141.
