Laser in situ keratomileusis (LASIK) is the most widely used

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1 CLINICAL SCIENCE Epithelial Ingrowth After LASIK: Visual and Refractive Results After Cleaning the Interface and Suturing the Lenticule Jose L. Güell, MD, PhD,* Paula Verdaguer, MD, Gloria Mateu-Figueras, PhD, Daniel Elies, MD, Oscar Gris, MD, PhD, Felicidad Manero, MD, and Merce Morral, MD, PhD Purpose: The aim was to study the visual and refractive results in patients with epithelization in the corneal interface after laser in situ keratomileusis (LASIK) who were treated by cleaning the corneal interface (epithelial cyst extraction) and suturing the corneal flap. Methods: This is a retrospective, noncomparative interventional case series. The main outcome measures were uncorrected distance visual acuity (UDVA), corrected distance visual acuity (CDVA), refractive cylinder (CYL), spherical equivalent (SE), recurrence of epithelial ingrowth, and complications. Results: From a total of 7520 LASIK refractive eyes, 13 eyes with epithelial ingrowth were treated. The mean age was 46.9 years. The mean preoperative logmar UDVA was 0.34 (SD, 0.19). At 2 months, the mean postoperative logmar UDVA was 0.18 (SD, 0.17) and at 1 year was 0.12 (SD, 0.18) (P = 0.01). The mean logmar CDVA before surgery was 0.16 (SD, 0.16). Two months and 1 year postoperatively, the mean logmar CDVA was 0.05 (SD, 0.08) and 0.03 (SD, 0.06), respectively (P = 0.03). The mean SE before surgery was 0.30 D (SD, 1.09). The mean SE 2 months and 1 year after surgery was (SD, 0.53) and (SD, 0.18), respectively (P = 0.04). The mean CYL before surgery was D (SD, 1.09); and the mean CYL 2 months and 1 year after surgery was (SD, 0.84) and (SD, 0.75), respectively (P = 0.26). No epithelial ingrowth recurrence was observed up to 1 year after epithelial removal. Conclusions: Cleaning the corneal interface and suturing the corneal flap was effective and appeared safe in treating epithelial ingrowth after LASIK, with an extremely low rate of regrowth. However, further prospective controlled studies with a longer follow-up are needed. Received for publication December 31, 2013; revision received June 11, 2014; accepted June 22, Published online ahead of print July 31, From the *Director of Cornea and Refractive Surgery Unit, Instituto Microcirugía Ocular, Barcelona, Spain, and Universitat Autònoma de Barcelona, Barcelona, Spain; Cornea and Refractive Surgery Unit, Instituto Microcirugía Ocular, Barcelona, Spain; Universitat Autònoma de Barcelona, Barcelona, Spain; Department of Mathematics at Universitat de Girona, Girona, Spain; Cornea and Refractive Surgery Unit, Instituto Microcirugía Ocular, Barcelona, Spain; and Instituto de Microcirugía Ocular, Barcelona, Spain, and Department of Cornea and Anterior Segment Diseases and Department of Refractive Surgery of the Institut Clinic d Oftalmologia, Hospital Clinic i Provincial, Barcelona, Spain. The authors have no funding or conflicts of interest to disclose. Reprints: Paula Verdaguer, MD, C/ Josep Maria Lladó no. 3, Barcelona, Spain ( paulaverdaguer@gmail.com). Copyright 2014 by Lippincott Williams & Wilkins Key Words: LASIK, myopia, astigmatism, epithelial ingrowth, corneal flap, corneal interface (Cornea 2014;33: ) Laser in situ keratomileusis (LASIK) is the most widely used refractive surgical technique because of its safety and effectiveness, quick visual recovery, and minimal side effects. However, it is not exempt from complications, both during surgery and in the years after surgery. Therefore, it is advisable to periodically monitor patients who undergo this procedure to enable early diagnosis and treatment of complications where appropriate. One significant complication of LASIK is epithelial ingrowth at the edge of the flap. Although not always severe, it can induce regular and/or irregular astigmatism or produce melting of the overlying flap. Reports of the incidence of epithelial ingrowth have ranged from 0% to 20%. 1,2 The cause of epithelial ingrowth remains unclear; however, it has been associated with epithelial defects at the time of surgery with or without flap edge trauma, a history of recurrent corneal erosions, hyperopic LASIK correction, repeated LASIK surgeries, flap instability, corneal epithelial basement membrane degeneration, and a history of ingrowth in the fellow eye. 3 Correct treatment and removal of the accumulation of epithelial cells in the corneal interface is the key to guaranteeing good visual acuity in patients with epithelial ingrowth. The aim of this study was to study the visual and refractive results in patients with epithelization in the corneal interface after undergoing LASIK. To avoid the recurrence of the invasion of epithelial cells in the corneal interface, patients were treated by cleaning the corneal interface (extracting the cyst) and suturing the corneal flap. SUBJECTS AND METHODS Subjects This retrospective, nonrandomized, noncomparative, interventional study included 13 eyes from 13 patients of a total of 7520 (0.17%) LASIK refractive surgery eyes that presented epithelization of the corneal interface after LASIK and required treatment. LASIK surgery was performed between January 2000 and January 2011 by the same surgeon (J.L.G.). Minimum follow-up was 1 year. The surgeon treated the epithelial ingrowth in all of the eyes that presented this Cornea Volume 33, Number 10, October 2014

2 Cornea Volume 33, Number 10, October 2014 Epithelial Ingrowth After LASIK complication by cleaning the corneal interface and by suturing the corneal flap. Only clinically significant epithelial ingrowth was treated, specifically if it extended into the pupillary zone, caused reduced vision (UDVA and CDVA) or visual disturbances such as night-time glare, or induced melting of the edge of the flap. The presence of some isolated epithelial cells at the edge of the flap was not treated, because it is a relatively common situation that is not usually classified as ingrowth. All patients were fully informed of details and possible risks of the specific procedure. Written informed consent to perform the surgical procedure was obtained from all patients before surgery, in accordance with the Declaration of Helsinki. The study was approved by our own institution s ethics committee (Instituto de Microcirugía Ocular) and by the Autonomous University of Barcelona (Universitat Autònoma de Barcelona). Preoperative Examination and Follow-up Patients underwent a complete preoperative ophthalmologic examination, including refraction, Snellen uncorrected distance visual acuity (UDVA), corrected distance visual acuity (CDVA), refractive cylinder (CYL), spherical equivalent (SE), slit-lamp examination including Goldmann applanation tonometry, corneal topography (Orbscan, Bausch and Lomb, NY), and a fundus examination. The inclusion criteria were: previous LASIK refractive surgery with a mechanical microkeratome, epithelization of the central corneal interface with alteration of UDVA and/or CDVA, induction of corneal astigmatism (regular and/or irregular) with a decrease of UDVA and/or CDVA, and a minimum follow-up of 1 year after study surgery. The exclusion criteria were: epithelization of the peripheral corneal interface without UDVA and CDVA alteration, noninduction of corneal astigmatism, and discontinuation of follow-up. Postoperative follow-up visits after epithelial removal were held 24 hours after surgery, and then at 4 weeks, 2 months, 6 months after surgery, and at yearly intervals. At each follow-up visit, manifest refraction, UDVA, CDVA, slit-lamp examination, and applanation tonometry were performed. Corneal topography was performed 4 weeks after the surgery and at yearly intervals. Fundus examination was performed at yearly intervals. Surgical Procedure The corneal interface is cleaned to improve UDVA and CDVA, and to remove or reduce corneal astigmatism; the corneal flap is sutured to avoid new migration of epithelial cells. The patient is given a mild sedative plus a topical anesthetic. The flap is lifted after a periphery dissection with an iridodialysis spatula. Once the flap is completely open and deflected, both stromal surfaces are cleaned carefully with a golf club-shaped blunt tip and microsponges. This is because, previous modes of dissection using a hockey-stick knife used to cut epithelial cysts, leading to leakage of epithelial cells. It is important to clean the entire flap properly, identifying the entrance area, which is usually wide. In some cases, it is helpful to use indirect instead of coaxial lighting. After this, the corneal flap is repositioned and the edges are sutured using several interrupted 10-0 nylon sutures (6 10). Postoperatively, tobramycin and dexamethasone drops every 6 hours and dexamethasone-plus-chloramphenicol eye ointment at night were prescribed for 3 weeks, as well as preservative-free artificial tears several times per day. If there were peripheral areas with focal absence or irregular epithelium 1 day after the surgery, a bandage contact lens was placed on this eye. The patient was informed that it would remain on the eye until the cornea reepithelialized, usually 2 or 3 days later. Sutures were removed between 4 to 6 weeks postoperatively. Statistical Analysis Microsoft Excel (Redmond, WA) was used for data collection and to perform descriptive statistics. Continuous variables were described with mean and standard deviation (SD). The results were analyzed using SPSS software version 17.0 (SPSS, Inc, Chicago, IL). Comparison between preoperative and postoperative data was performed using Wilcoxon signed-rank tests for nonparametric data (UDVA, CDVA, SE, and CYL). The tests were performed before the surgery (epithelial ingrowth removal and suturing of the corneal flap), 1 day, 1 month (when the corneal sutures were removed), 1 month after the removal of the corneal sutures (2 months after surgery), and 1 year postoperatively. A P value lower than 0.05 was considered statistically significant. Epithelial ingrowth recurrence was analyzed at 1 year of follow-up. RESULTS Baseline Characteristics and Follow-up Thirteen eyes of 13 patients were treated: 7 (53.85%) were right eyes; and 6 (46.15%) were left eyes. The mean age was 46.9 years (range, years). Minimum follow-up after the epithelial cleaning was 1 year. Previous ophthalmic surgical history included: 2 (15.4%) anterior chamber intraocular lens implantation (IOL) (Artiflex IOL, Ophtec BV, the Netherlands) to correct a myopic refractive error, and 3 (23.1%) clear lens extraction with monofocal IOL implantation to correct hyperopia and presbyopia. These 2 groups of patients were treated again for the residual refractive error from the first surgery with LASIK. The rest of the cases were patients who had undergone LASIK as primary refractive correction. Visual Acuity Table 1 summarizes logmar UDVA, logmar CDVA, SE, and CYL at each follow-up point. The mean preoperative logmar UDVA was 0.34 (SD, 0.19). The mean logmar UDVA was 0.65 (SD, 0.26) and 0.18 (SD, 0.17) 1 day after surgery and 1 month after the removal of the corneal suture (2 months after surgery), respectively. One year after surgery, the mean logmar UDVA was 0.12 (SD, 0.18). There was a statistically significant improvement in mean logmar UDVA, that continued throughout the follow-up period (P, 0.01) (Fig. 1A). Ó 2014 Lippincott Williams & Wilkins

3 Güell et al Cornea Volume 33, Number 10, October 2014 TABLE 1. Preoperative and Postoperative Uncorrected Visual Acuity, Best-Spectacle Corrected Visual Acuity, Spherical Equivalent, and Cylinder Before LASIK Before Cleaning the Lenticule and Corneal Suture 24 Hours Postoperatively 1 Month After Removal of the Suture (2 Months After the Surgery) After 1 Year P* logmar UDVA Mean ,0.01 SD ,0.01 logmar CDVA Mean SD SE Mean SD CYL Mean SD *Wilcoxon signed rank test for SE and CDVA: statistically significant differences (P, 0.05) when preoperative was compared with any postoperative follow-up period. The mean logmar CDVA before LASIK surgery was 0.06 (SD, 0.07), and 0.16 (SD, 0.16) before epithelial cleaning and corneal suture surgery. The mean logmar CDVA was 0.54 (SD, 0.26) and 0.05 (SD, 0.08) 1 day and 1 month after corneal suture removal (2 months after surgery), respectively. One year after surgery, the mean logmar CDVA was 0.03 (SD, 0.06). The mean logmar CDVA significantly improved after surgery, and remained stable throughout the follow-up period (P =0.03)(Fig.1B). Refractive Outcome The mean preoperative SE before LASIK surgery was (SD, 2.29). The mean SE before epithelial ingrowth cleaning and lenticule suture surgery was 0.30 D (SD, 1.09). The mean postoperative SE was D (SD, 0.80) and (SD, 0.53) 1 day and 1 month after corneal suture removal (2 months after surgery), respectively. One year after the surgery, the mean SE was (SD, 0.18). The SE significantly and progressively decreased after all the surgeries (P = 0.043) (Fig. 1C). The mean CYL before LASIK surgery was D (SD, 1.13). The mean CYL before epithelial ingrowth cleaning and lenticule suture was D (SD, 1.09). The mean postoperative CYL was D (SD, 2.30) and (SD, 0.84) 1 day and 1 month after corneal suture removal (2 months after the surgery), respectively. One year after surgery, the mean CYL was (SD, 0.75). CYL FIGURE 1. A, Preoperative and postoperative uncorrected visual acuity (UDVA) (mean 6 SD at each follow-up point). Mean values for the UDVA variable are indicated. Error bars indicate SD. B, Evolution of the bestspectacle corrected visual acuity (CDVA) (mean 6 standard deviation at each follow-up point). Mean values for the CDVA variable are indicated. Error bars indicate SD. C, Preoperative and postoperative SE (mean 6 SD at each follow-up point). Mean values for the SE variable are indicated. Error bars indicate SD. D, Preoperative and postoperative cylinder (CYL) (mean 6 SD at each follow-up point). Mean values for the CYL variable are indicated. Error bars indicate SD Ó 2014 Lippincott Williams & Wilkins

4 Cornea Volume 33, Number 10, October 2014 Epithelial Ingrowth After LASIK progressively, though not statistically significant, decreased throughout the follow-up period (P = 0.256) (Fig. 1D). Complications There were no associated complications during or after treatment. No incidence of epithelial regrowth was reported. None of the eyes lost any line in CDVA. No epithelial defects, diffuse lamellar keratitis, or infections were observed. DISCUSSION Epithelialization of the interface, which can occur after flap creation with a mechanical or laser microkeratome, is caused by the proliferation of epithelial cells between the stromal bed and the lenticule. It is considered that, if the layer of epithelialization reaches a thickness of 40 to 60 mm and its diameter is greater than 2 mm, it can also be compounded by flap keratolysis or corneal melting. 3 Epithelialization of the interface occurs because of an invasion of the interface by the peripheral corneal epithelium, probably secondary to poor sealing of the lenticular edge or because of migration of epithelial cells under the lenticule. 4 6 It is more frequent in patients with seborrheic blepharitis, those who have an epithelial defect at the time of the intervention, and in patients who require retreatment by lifting the previous lenticulereoperation or re-lasik. 5 It affects between 1% and 20% of eyes treated with LASIK. 1,2,4 6 In our experience, the incidence of epithelial ingrowth requiring treatment is 0.17% because it was clinically significant. It has been suggested that placing a bandage contact lens on the eye after surgery can reduce the incidence of epithelial ingrowth in patients with a higher risk of this complication. These are not used in regular LASIK cases unless an obvious epithelial defect is observed, or when the epithelium is clearly detached. Epithelial ingrowth can occur many months after LASIK even in the absence of predisposing factors such as trauma or recurrent erosion syndrome. 7 In the present case series, we did not observe any epithelial defect after original LASIK surgery. The rate of epithelial growth when femtosecond LASIK is used as primary treatment after LASIK is extremely low, possibly because of the vertical side-cut incision. 8 Treatment of epithelialization has been controversial, because there has not been an ideal treatment until now. Even therapeutic abstention has been suggested, mainly because of the surgical risks associated with reoperations, including a higher incidence of epithelialization, irregular astigmatism, and small tears in the lenticule Therefore, treatment is not required if there are isolated nests of epithelial cells in the lamellar interface, but they do not progress and do not affect vision. However, if the epithelium progresses toward the visual axis, causing a decrease in the visual acuity and/or inducing regular or irregular astigmatism, or if it triggers progressive melting of the overlying flap, it must be removed by lifting the flap, cleaning both stromal surfaces, and repositioning the flap. Some authors have suggested the use of Nd:YAG laser treatment for epithelial ingrowth, because this shows an improvement in 100% of patients. 12 However, this may be due to the fact that it was mostly used in cases that were not significantly advanced. Severe progressive epithelial ingrowth may also be treated successfully with a combination of mechanical debridement, flap suturing, and fibrin glue application. 13 At the same time, some surgeons also remove the peripheral corneal epithelium out from the flap edge to facilitate adherence of the flap before the epithelial edge progresses to the edge of the flap. 11 Other surgeons correct recurrent epithelial ingrowth by repeatedly lifting and scraping, with or without a flap sectorial suture, or with fibrin glue at the edge of the flap. 14,15 Some other surgeons have used cytotoxic drugs such as alcohol or mitomycin C alone or in conjunction with mechanical debridement or phototherapeutic keratectomy with very positive results. 16,17 We do not favor use of this group of substances because of the possible local toxicity. Rojas et al assessed the efficacy and safety of mechanical debridement and suturing the LASIK flap in the treatment of 20 clinically significant cases of epithelial ingrowth after LASIK. None of eyes experienced recurrence of clinically significant epithelial ingrowth. After treatment of the epithelial ingrowth, the UDVA improved although there was no decrease in SE. 18,19 In our study, cleaning both stromal surfaces and suturing the corneal flap resulted in a statistically significant improvement in the UDVA and CDVA. A statistically significant decrease in induced positive (hyperopia) SE and FIGURE 2. Right eye. A, View of the anterior segment after LASIK. Epithelization of the corneal interface has reached the edge of the pupillary area. B, View of the anterior segment after cleaning epithelial cells from the lenticule, and corneal suture. When removing the suture, the cornea was transparent and the lenticule was well positioned without signs of epithelial growth in the interface. Ó 2014 Lippincott Williams & Wilkins

5 Güell et al Cornea Volume 33, Number 10, October 2014 CYL brought on by the accumulation of cells in the interface was also noted in most cases, without any case of recurrence up to 1 year after surgery. In our opinion, suturing the LASIK flap in addition to mechanical debridement of epithelial ingrowth in both stromal surfaces is the safest and most effective treatment for clinically significant epithelial ingrowth after LASIK. Although we cannot rule out any case of late-onset epithelial ingrowth, there is only 1 report in the literature of its occurrence in the absence of trauma or recurrent erosion syndrome. 7 Therefore, it seems unlikely that spontaneous recurrence of epithelial ingrowth may occur over 1 year after interface cleaning. In fact, we do not believe that, in the absence of an open fistula at the edge of the flap, ingrowth can start later than 4 to 6 weeks after surgery. Monitoring patients periodically after LASIK enables early detection of postoperative complications that may otherwise go unnoticed, because they are virtually asymptomatic, especially in their initial stages. If epithelial ingrowth appears in the interface, causing a decrease in the visual acuity or inducing astigmatism, it must be treated by careful cleaning of epithelial cells of both stromal surfaces, and subsequent suturing, to avoid further penetration of epithelial cells. With this surgical option, after the removal of the corneal sutures, the patient s visual and refractive results as well as the slit-lamp examination were highly satisfactory (Fig. 2). The main limitations of this study are the retrospective approach, attrition of patients who were being followed up, short follow-up, and the lack of a control group or comparative group who had received another treatment. Therefore, results should be regarded with caution. Prospective comparative studies and a longer follow-up with a larger sample size are required to demonstrate the superiority of our technique over other techniques and investigating long-term safety. REFERENCES 1. Pallikaris IG, Siganos DS. Excimer laser in situ keratomileusis and photorefractive keratectomy for correction of high myopia. J Refract Corneal Surg. 1994;10: Domniz Y, Comaish IF, Lawless MA, et al. Epithelial ingrowth: causes, prevention, and treatment in 5 cases. J Cataract Refract Surg. 2001;27: Walker MB, Wilson SE. Incidence and prevention of epithelial growth within the interface after laser in situ keratomileusis. Cornea. 2000;19: Fournié PR, Gordon GM, Dawson DG, et al. Correlation between epithelial ingrowth and basement membrane remodeling in human corneas after laser-assisted in situ keratomileusis. Arch Ophthalmol. 2010;128: Saeed A, O Doherty M, O Doherty J, et al. Analysis of the visual and refractive outcome following laser in situ keratomileusis (LASIK) retreatment over a four-year follow-up period. Int Ophthalmol. 2007;27: Jun RM, Cristol SM, Kim MJ, et al. Rates of epithelial ingrowth after LASIK for different excimer laser systems. J Refract Surg. 2005;21: Todani A, Melki SA. Late-onset epithelial ingrowth after laser in situ keratomileusis. J Cataract Refract Surg. 2009;35: Güell JL, Elies D, Gris O, et al. Femtosecond laser-assisted enhancements after laser in situ keratomileusis. J Cataract Refract Surg. 2011;37: Lyle WA, Jin GJ. Interface fluid associated with diffuse lamellar keratitis and epithelial ingrowth after laser in situ keratomileusis. J Cataract Refract Surg. 1999;25: Stulting RD, Carr JD, Thompson KP, et al. Complications of laser in situ keratomileusis for the correction of myopia. Ophthalmology. 1999;106: Dawson DG, Kramer TR, Grossniklaus HE, et al. Histologic, ultrastructural, and immunofluorescent evaluation of human laser-assisted in situ keratomileusis corneal wounds. Arch Ophthalmol. 2005;123: Lindfield D, Ansari G, Poole T. Nd:YAG laser treatment for epithelial ingrowth after laser refractive surgery. Ophthalmic Surg Lasers Imaging. 2012;43: Narváez J, Chakrabarty A, Chang K. Treatment of epithelial ingrowth after LASIK enhancement with a combined technique of mechanical debridement, flap suturing, and fibrin glue application. Cornea. 2006; 25: Wang MY, Maloney RK. Epithelial ingrowth after laser in situ keratomileusis. Am J Ophthalmol. 2000;129: Asano-Kato N, Toda I, Hori-Komai Y, et al. Epithelial ingrowth after laser in situ keratomileusis: clinical features and possible mechanisms. Am J Ophthalmol. 2002;134: Haw W, Manche EE. Treatment of progressive or recurrent epithelial ingrowth with ethanol following laser in situ keratomileusis. J Refract Surg. 2001;17: Taneri S, Koch JM, Melki SA, et al. Mitomycin-C assisted photorefractive keratectomy in the treatment of buttonholed laser in situ keratomileusis flaps associated with epithelial ingrowth. J Cataract Refract Surg. 2005;31: Rojas MC, Lumba JD, Manche EE. Treatment of epithelial ingrowth after laser in situ keratomileusis with mechanical debridement and flap suturing. Arch Ophthalmol. 2004;122: Henry CR, Canto AP, Galor A, et al. Epithelial ingrowth after LASIK: clinical characteristics, risk factors, and visual outcomes in patients requiring flap lift. J Refract Surg. 2012;28: Ó 2014 Lippincott Williams & Wilkins

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