ARTICLE

Photorefractive keratectomy with mitomycin-C for the combined treatment of myopia and subepithelial infiltrates after epidemic keratoconjunctivitis

David Alevi, MD, Allon Barsam, MA, FRCOphth, Jonathan Kruh, MD, Jessica Prince, MD, Henry D. Perry, MD, Eric D. Donnenfeld, MD

PURPOSE: To report the use of photorefractive keratectomy (PRK) with mitomycin-C (MMC) to treat concomitant myopia and visually significant infiltrates associated with epidemic keratoconjunctivitis (EKC). SETTING: Ophthalmic Consultants of Long Island, Nassau University, Long Island, New York, USA. DESIGN: Interventional case series. METHODS: Consecutive patients with myopia and recalcitrant subepithelial infiltrates after EKC were treated with custom wavefront PRK (Visx S4 IR) and MMC with a target of emmetropia in all cases. RESULTS: The study evaluated 6 eyes of 3 patients. One year after treatment, all eyes attained an uncorrected distance visual acuity of 20/20 or better. There was no recurrence of infiltrates within the ablation zone in any eye. CONCLUSION: The use of topical MMC in conjunction with PRK to treat subepithelial infiltrates due to EKC provided good visual and refractive results. Financial Disclosure: No author has a financial or proprietary interest in any material or method mentioned. J Cataract Refract Surg 2012; 38:1028–1033 Q 2012 ASCRS and ESCRS

Excimer laser photoablation in the form of photother- comfort. Using a laser instead of conventional exci- apeutic keratectomy (PTK) has been used since the late sional corneal surgery may allow more controlled re- 1980s to manage and treat anterior corneal pathology.1 moval of pathological tissue by minimizing adjacent The 193 nm argon–fluoride laser photochemically tissue damage. breaks intermolecular bonds, expelling corneal tissue Phototherapeutic keratectomy is effective in superfi- in a controlled manner without thermal damage. cial corneal pathology that is present in Bowman Excimer laser photoablation can remove corneal membrane or in the anterior cornea stroma. Removing pathology, improving visual acuity and patient or reducing this corneal pathology allows a smoother and clearer cornea.2 Ablating and flattening the more central areas of the cornea with use of PTK often re- Submitted: September 13, 2011. sults in a hyperopic change in refractive error that is di- Final revision submitted: December 13, 2011. 3 Accepted: December 16, 2011. rectly related to the depth of the ablation. This hyperopic shift is unpredictable and may diminish From Ophthalmic Consultants of Long Island, Rockville Centre, over time.3 Haze, likely secondary to deposition of New York, USA. new irregular collagen fibers or from light scattering Corresponding author: Allon Barsam, MA, FRCOphth, Consultant by activated keratocytes in the wound, is another com- 4 Ophthalmic Surgeon, Luton and Dunstable University Hospital plication of PTK. Also, variations in the eye’s rate and NHS Foundation Trust, Lewsey Road, Luton LU4 0DZ, United ability to reepithelialize contribute to further compli- Kingdom. E-mail: [email protected]. cations, including irregular astigmatism and scarring.

1028 Q 2012 ASCRS and ESCRS 0886-3350/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.jcrs.2011.12.039 PRK FOR MYOPIA AND RECALCITRANT ADENOVIRAL KERATITIS 1029

Several case reports document elimination of corneal been reports of myopic photorefractive keratectomy opacities followed by a recurrence in the pathology.5 (PRK) without MMC used with partial success to per- Finally, in certain cases in which recurrence does oc- manently remove the infiltrates in patients with sube- cur, multiple treatments of PTK are necessary to re- pithelial infiltrates.18 To our knowledge, the present duce corneal pathology and improve patient series is the first description of the use of PRK with satisfaction. Despite these potential complications, MMC to treat myopia and visually significant infil- PTK has been used with much success to reduce and trates associated with EKC. eliminate corneal pathology, delaying and avoiding more invasive methods including lamellar and pene- PATIENTS AND METHODS 6,7 trating keratoplasty. Patients with myopia and recalcitrant subepithelial infil- Epidemic keratoconjunctivitis (EKC) is caused by trates after EKC were treated with custom wavefront PRK multiple adenovirus strains and is associated with (Visx S4 IR, Abbott Medical Optics); the target was emmetro- infection and inflammation of the cornea and conjunc- pia in all cases. Approximately 10 to 15 subepithelial infil- tiva. Adenovirus is a nonenveloped double-stranded trates were observed in each patient. After informed consent and extensive discussion, each patient elected to DNA virus. The virus is extremely stable, being have PRK to treat the myopia and to remove the corneal resistant to most solvents and detergents. The more opacities. virulent serotypes, such as serotypes 8 or 19, were Manual epithelial debridement was performed followed found to be viable for up to 4 to 5 weeks on inert ma- by excimer ablation. After PRK with the laser, MMC 0.02% terial.8,9 Ophthalmology offices are prone to epidemics was applied for 30 seconds before the cornea was fully irri- – gated with a cooled balanced salt solution. Each patient due to contamination of instruments or hand eye had a bandage contact lens placed and was treated with ga- contact by ocular secretions from the infected pa- tifloxacin 0.3% 4 times a day for 6 days; ketorolac 0.5% 4 tient.10 In addition, EKC has been found in hospital times a day for 2 days; and prednisolone acetate 1.0% 4 times outbreaks, public swimming pools, and upper respira- a day for 1 week, 3 times a day for 1 week, 2 times a day for 1 tory tract infections.11 week, and every day for 1 week. The bandage contact lens was removed 3 to 5 days after surgery. Patients were then ex- Epidemic keratoconjunctivitis is characterized amined 1 week and 1, 3, 6, and 12 months after treatment. by follicular conjunctivitis, papillary hypertrophy, conjunctival hemorrhage, lid edema, and chemosis. RESULTS Preauricular and submandibular adenopathy may assist in the diagnosis. In severe cases, membranes or Six eyes of 3 patients were treated. pseudomembranes may develop on the tarsal conjunc- Case 1 tiva, which may lead to conjunctival fibrosis and symblepharon formation.12 A 27-year-old myopic male ophthalmology resident The corneal findings of EKC begin with a diffuse with a refraction of À2.50 À0.50 Â 110 in the right eye epithelial keratitis that stains with fluorescein and and À2.75 in the left eye developed EKC in both eyes may coalesce into focal epithelial lesions approxi- with visually significant subepithelial infiltrates. He mately 1 week after infection. Subepithelial corneal had worn a soft contact lens for 7 years and was devel- infiltrates of 1.0 to 2.0 mm in diameter develop within oping increased contact lens wear intolerance. Seven the second or third week after conjunctival symptoms months before evaluation, the patient had a severe begin and diffuse epithelial keratitis is seen.13 These case of EKC that left him with multiple central bilateral infiltrates generally develop in the center of the cornea; subepithelial infiltrates. The patient was treated with however, they may cover the entire corneal surface. a tapering dose of prednisolone acetate 1% starting Due to the corneal infiltrates, permanent glare or at 4 times a day for 3 months without resolution of photophobia may develop; decreased visual acuity is the infiltrates. After an additional 4 months without also likely to occur as a result of irregular astigmatism corticosteroids, the patient presented for evaluation and corneal opacities occluding the visual axis.14 Some with continued central subepithelial infiltrates and of these visual effects may (in part) resolve spontane- a corrected distance visual acuity (CDVA) of 20/20 ously over several years and can be treated with in both eyes; however, he reported glare and halo low-dose topical corticosteroid agents.15 Corticoste- that had not been present before the development of roid therapy may require months of treatment and the infiltrates 40 mm beneath the epithelium. The pa- once discontinued, the infiltrates often reoccur. In tient had 8 to 10 infiltrates, mostly clustered around addition, long-term corticosteroid use is associated the central 6.0 mm of each cornea, with a few extend- with cataract formation and glaucoma. ing to the peripheral 9.0 mm point. Successful removal of adenoviral EKC corneal Wavefront analysis was obtainable in both eyes and opacities using PTK and mitomycin-C (MMC)14 or matched the patient’s refraction. The decision was PTK alone16,17 has been reported. There have also made to enlarge the custom wavefront ablation zone

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to 8.8 mm, which increased the depth of the ablation to 68 mm in the right eye and 77 mm in the left eye. By en- larging the ablation zone and depth of ablation, the in- filtrates in the midperiphery of the cornea would also be treated. This decision was made to prevent peripheral infiltrates from causing symptoms under mesopic conditions, in which the pupil may become larger. One year after PRK, the patient had 20/15 uncor- rected distance visual acuity (UDVA) in both eyes, a refraction of plano in both eyes, no glare or halo, and clear corneas with complete resolution of all infiltrates.

Case 2 Figure 1. Case 3. Subepithelial infiltrate after EKC in the visual axis A 24-year-old myopic woman with a refraction before PRK. of À4.50 À0.25 Â 90 in the right eye and À4.75 À0.50 Â 95 in the left eye developed EKC with visually signif- Photorefreative keratectomy was performed with icant infiltrates 40 mm beneath the epithelium. The a central ablation depth of 109 mm in both eyes; the ab- infiltrates developed 2 weeks after the acute infection lation zone was 8.0 mm. The bandage contact lens was and were treated with a 5-month course of tapering removed 5 days after surgery when the epithelium prednisolone acetate 1.0% and then loteprednol 0.5%; was almost healed (Figure 2). One year after PRK, this resulted in improvement of the infiltrates and the patient had a UDVA of 20/20 in the right eye a CDVA of 20/25 in both eyes. The patient also and 20/20 in the left eye with a refraction of C0.50 reported glare and halo. She was followed for an addi- À0.25 Â 90 and C0.25 À0.25 Â 80, respectively. He tional year without topical corticosteroids and had no longer reported glare or halo; the central cornea slight improvement in the infiltrates but continued to of each eye was clear with no infiltrates. have a CDVA of 20/25 in both eyes. She had 12 to 15 infiltrates extending from the central cornea to the pe- riphery. The glare and halo remained the same. DISCUSSION Photorefractive keratectomy was performed with All 3 patients sought refractive surgery to reduce or a central ablation depth of 88 mm in the right eye and remove their dependence on glasses. However, the 90 mm in the left eye; the ablation zone was 8.0 mm. presence of subepithelial infiltrates and the glare and Two years after PRK, the patient had a UDVA of 20/ halo associated with them were also a concern. The 20 in both eyes and a refraction of C0.50 À0.25 Â 40 decision to perform PRK rather than laser in situ in the right eye and C0.25 in the left eye. She no longer reported glare or halo; the central cornea of each eye was clear with no infiltrates.

Case 3 A 30-year-old man with a refraction of À8.75 À1.25 Â 147 in the right eye and À7.75 À0.50 Â 80 in the left eye developed EKC in both eyes with visually signifi- cant infiltrates 40 mm beneath the epithelium (Figure 1). The EKC developed 7 months previously when the patient was living in Lebanon. The patient had taken several 4-week reducing courses of topical prednisolone acetate 1.0% 4 times a day since develop- ing the viral keratitis. However, he remained symp- À tomatic with glare despite a CDVA of 20/20 1 in both eyes. He had 12 to 14 infiltrates, mostly clustered around the central 5.0 mm of each cornea, with a few Figure 2. Case 3. One week after treatment, the epithelium had extending to the peripheral 10.0 mm point. healed and the opacities had resolved.

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keratomileusis (LASIK) offered the ability to remove These patients were candidates for PRK because of the infiltrates rather than preserve them in the LASIK their stable myopic refraction with visually significant corneal flap. In addition, LASIK can reactivate subepi- recalcitrant subepithelial infiltrates caused by EKC. In thelial infiltrates in the area of the laser ablation.19,20 In more mild cases, patients can often wait for spontane- the past, PRK treatment for residual myopia and ous resolution of symptoms to avoid the risks of PRK. subepithelial infiltrates without the use of MMC has These risks include severe corneal haze, which has had variable success, with resolution of the infiltrates been significantly reduced with the use of smoother centrally but recurrence in the periphery. In other ablation profiles and the use of MMC; however, histor- cases, significant recurrences have been seen centrally ically, haze may present in up to 15% of patients after in patients with subepithelial infiltrates after EKC. The surgery.22 In addition, patients with a high degree of recurrence is thought to be due to the natural history of myopia have less reliable refractive outcome due to the infiltrate or to the withdrawal of the corticosteroid. the cornea’s pattern of healing after the ablation. Other The decision to perform PRK rather than PTK was less common complications after PRK include pain based on the patients’ preexisting myopia and their secondary to the epithelial defect and delayed epithe- desire to treat the concomitant refractive error. lial healing.23,24 We have found that haze and scarring Photorefractive keratectomy offers greater refractive are very rare when PRK is combined with MMC; accuracy than PTK. In addition PTK in the United therefore, we do not routinely use topical steroids be- States can be performed with the Visx laser only and yond the first month unless clinical signs indicate the has a maximum ablation zone of 6.5 mm and no blend need for this. zone, which creates an oblate ablation profile. Keratocytes located within the human corneal A maximum blend zone of 0.5 mm can be added to stroma serve to organize the extracellular matrix the Visx PTK, which decreases the effective ablation (ECM) and to heal injury to the cornea. Studies zone from 6.5 mm to 6.0 mm. Performing excimer laser have shown that transforming growth factor-b in- ablation to treat myopia in a cornea with opacities is an duces transformation of keratocytes to myofibro- off-label use of the excimer laser, and our patients were blasts. During times of injury, this transformation informed of this and consented appropriately. Excimer can occur, which is critical in shaping the ECM during laser ablation does not always ablate at the same rate corneal injury.25 A capsid of adenovirus 19 can attach in a clear cornea as in a scarred cornea. Even though to a cellular binding site, activating a signal transduc- subepithelial infiltrates can be faint, they sometimes tion cascade that causes expression of interleukin-8 coalesce and create a large area of opacity; when this (IL-8) and monocyte chemoattractant protein-1 is ablated with an excimer laser, there is the potential (MCP-1). Both IL-8 and MCP-1 are chemokines that for resultant irregularity. We did not believe that the attract proinflammatory mediators to the corneal opacities in our patients were dense enough to warrant stroma.26 In our study, MMC was critical due to its ef- the use of a masking agent or transepithelial PRK to fect on keratocytes. Through the caspase pathway in prevent this potential problem. the mitochondria, MMC has been shown to induce All patients had careful evaluation of wavefront apoptosis of keratocytes by being cytotoxic to these aberrometry. By selecting a custom treatment, we cells.27 were also able to modify the ablation zone from Although MMC was originally used as a systemic 8.0 mm to 8.8 mm and ablation depth based on the chemotherapeutic agent, topical MMC is being used patients’ refractive errors, infiltrate depths, and loca- with increasing frequency in ophthalmology.28 It tions of infiltrate removal, centrally as well as in the has been used in glaucoma filtering surgery to prevent – midperiphery. However, it may not be essential to scarring,26 in pterygium surgery,28 32 in the treatment remove the peripheral infiltrates depending on the of conjunctival and corneal intraepithelial neoplasia,33 patient’s pupil size and the exact location and density and in the treatment of ocular cicatricial of the infiltrates. pemphigoid.34 At present, there is no U.S. Food and Drug Admin- Mitomycin-C is a modulator of corneal wound istration–approved treatment for EKC. In general, healing after PRK in animal models. Talamo et al.35 therapy is directed to provide symptomatic relief performed excimer laser ablation in 10 New Zealand with artificial tears and to treat the inflammation white rabbits. The eyes were randomized to receive with topical corticosteroids. Several antiviral agents topical MMC 0.05%, topical steroids and topical eryth- that have activity against adenovirus are available.21 romycin, steroids and erythromycin, or erythromycin Recently, ganciclovir was approved for use in the alone. The medications were instilled twice daily for U.S., and this antiviral has in vitro and in vivo activity 14 days. Eyes receiving topical MMC 0.05%, topical against adenovirus and may provide a treatment steroids, and topical erythromycin had little or no option that was not previously available.A subepithelial scarring. Histopathologic differences

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