Introduction. Sevda Aydin Kurna, Ahmet Altun, Aynur Oflaz and Aysu Karatay Arsan. Acta Ophthalmologica 2015

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1 Evaluation of the imact of ersistent subeithelial corneal infiltrations on the visual erformance and corneal otical quality after eidemic keratoconjunctivitis Sevda Aydin Kurna, Ahmet Altun, Aynur Oflaz and Aysu Karatay Arsan Fatih Sultan Mehmet Education and Research Hosital, Ohthalmology Clinics, Istanbul, Turkey ABSTRACT. Purose: Aim was to measure the effect of ersistent subeithelial corneal infiltrates (SEIs) after eidemic keratoconjunctivitis (EKC) on visual erformance and corneal otical quality. Methods: We examined 53 atients divided into two grous. Patients with revious EKC constituted the study grou (Grou 1, n: 27). Healthy age matched subjects constituted the control grou (Grou 2, n: 26). Study grou was subdivided into eyes with SEI (Grou 1A, 40 eyes) and healthy fellow eyes (Grou 1B, 14 eyes). Patients were submitted to a comlete examination including high- and low-contrast visual acuities (HCVA, LCVA), corneal toograhy and aberrometry. Results: The mean interval between eidemic conjunctivitis and examination was months. Mean number of corneal infiltrates was The mean HCVA and LCVA were significantly lower in the eyes with SEI than fellow eyes and control grou ( = 0.001). LCVA value was also worse in the fellow eyes when comared to control ( = 0.048). Corneal toograhy values were significantly higher in the eyes with SEI from both fellow eyes and control grou. During corneal aberrometry, the mean root mean square value of sheric aberration, irregular astigmatism and total aberration were significantly higher in SEI grou when comared to fellow eyes and control grou ( < 0.05). Total aberrations were higher than control subjects in the fellow eyes. Trefoil aberration was higher in SEI grou only when comared to control subjects, while there was no significant difference in coma aberration values between the grous ( > 0.05). Conclusion: Results of this study suggested that visual erformance is comromised in atients with EKC by aberrations and changes in toograhic variables. Key words: corneal aberrometry corneal toograhy eidemic keratoconjunctivitis low-contrast visual acuity subeithelial corneal infiltrations None of the authors has conflict of interest with the submission. Acta Ohthalmol. 2015: 93: ª 2014 Acta Ohthalmologica Scandinavica Foundation. Published by John Wiley & Sons Ltd doi: /aos Introduction Eidemic keratoconjunctivitis (EKC) is an adenoviral infection with a clinical sectrum ranging from subclinical cases to severe keratoconjunctivitis (Gordon et al. 1998; Hillenkam et al. 2002). The corneal disease usually starts 2 or 3 days after onset of symtoms with a diffuse eithelial keratitis, followed from the seventh day on by unctuate focal areas of eithelial oacities, gradually fading but often leaving subeithelial corneal infiltrates (SEIs) in a manner of 1 3 weeks. Corneal SEIs are small, round and greyish lesions (Dawson et al. 1972). Histoathology of the cornea with oacities due to EKC reveals the collection of lymhocytes, histiocytes and fibroblasts, which can be accomanied by disrution of the collagen fibres of Bowman layer (Lund & Stefani 1978; Tabery 2000). The athogenesis of SEI involves a ersisting viral relication in subeithelial keratocytes, which triggers an immunologic host reaction (Dawson et al. 1972). SEIs are associated with significant atient morbidity, including symtomatic distress with visual disturbances (Ford et al. 1987; Hillenkam et al. 2001). Visual imairment because of SEIs and irregular astigmatism can ersist for months (Bohringer et al. 2008; Meyer-Rusenberg et al. 2011). Corneal defects may roduce severe aberrations in the eye and have been described as corneal wavefront aberrations and mathematically decomosed 377

2 to a series of Zernike aberrations. Wavefront aberrations can be defined as any deviation from the wavefront that would be exected through a erfect otical system in which a wavefront emerging from a oint in the object lane converges on a single oint in the image lane (Cervino et al. 2007; Mello et al. 2012). From analysis of the corneal aberrations, the anterior cornea has been found to have most classical aberrations, including astigmatism, coma and sherical aberration and many other higher-order aberrations (Alegate et al. 2000). They are a result of the lack of homogeneity of the ocular media as well as local irregularities of the otical surfaces (Cervino et al. 2007). Corneal wavefront analysis imroved our comrehension of the otical effects of corneal disorders such as keratoconus (Alio & Shabayek 2006; Barbero et al. 2007), laser-assisted corneal incisional surgeries (Oshika et al. 1999), collagen cross-linking theray with riboflavin (Vinciguerra et al. 2009), corneal translantation (McLaren et al. 2009), customized intraocular lenses (Nochez et al. 2010) and contact lenses (Gemoules & Morris 2007) in the literature. The uroses of this article were to measure the effect of ersistent SEIs on high- and low-contrast visual acuities (HCVA, LCVA) and corneal otical quality (corneal higher-order aberrations and toograhic changes) and to comare these measurements with the data obtained from healthy fellow eyes and control atients. Materials and methods The study rotocol was in adherence to the tenets of the Declaration of Helsinki and aroved by the Ethics Committee of Fatih Sultan Mehmet Education and Research Hosital. Informed, written consent was obtained from each articiant. Study included 53 atients examined between March 2013 and Setember Patients with revious eidemic kerato-conjunctivitis constituted the study grou (Grou 1, n: 27). The inclusion criterion was to have ersistent SEIs in the cornea due to revious eidemic kerato-conjunctivitis at least 3 months before the examination. Patients between 18 and 65 years old were included. Patients with corneal athologies that can affect the results of corneal toograhy such as revious ocular surgery, corneal scar or dry eye were excluded from the study. Healthy age matched subjects constituted the control grou (Grou 2, n: 26). Corneal oacities were bilateral in 13 atients while it was unilateral in 14 atients. Study grou was subdivided in to eyes with SEIs as Grou 1A (40 eyes) and healthy fellow eyes as Grou 1B (14 eyes). We erformed a comlete ohthalmic examination on all of the subjects including best corrected visual acuity (BCVA) testing with logarithm of the minimum angle of resolution (log- MAR), slit lam biomicroscoy and fundoscoy. We evaluated monocular logmar visual acuity with best sectacle correction using high contrast (96%) and low contrast (10%) using Bailey Lovie logmar letter charts at a distance of 4 m. Each letter read correctly on each line was given a score of 0.02 log units. In this chart, a loss of one line of letters corresonded to a logmar increase of 0.1 (Lovie-Kitchin 1989). All atients corneal toograhy measurement and simulated (sim) K, surface asymmetry index (SAI), otential visual acuity (PVA), surface regularity index (SRI) values were recorded. Corneal toograhy was measured with Magellan Maer (Nidek Technologies SRL, Padova, Italy). Magellan Maer features a streamlined 30-ring rojector, dual-edge ring finder with an astounding 60 rings detected, data oints and a high-resolution camera ( ixels) that analyses corneal aberrometry through the ZERNIKE decomosition software (Nidek Technologies SRL). Corneal aberrations were measured with corneal aberrometer and sheric aberration; coma, trefoil, irregular astigmatism and total high-order root mean square (RMS) values were recorded. All the data obtained were measured according to the 5-mm uilla diameter at dark environment, and uilla was not dilated. Corneal haze due to infiltrates was scored with bio-microscoic examination according to the Fantes grading scale as stage 0: clear cornea or no haze; stage 1: trace haze of minimal density seen with difficulty using direct illumination; stage 2: moderate haze easily visible with direct slit illumination; stage 3: marked haze artly obscuring anterior chamber observation or iris details; and stage 4: severe haze obscuring anterior chamber or iris details (Fantes et al. 1990). Statistical analyses Statistical analyses were made with NCSS (Number Cruncher Statistical System) 2007 and PASS (Power Analysis and Samle Size) 2008 Statistical Software (NCSS, LCC, UT, USA) on the comuter. While evaluating the arameters other than definitive statistical methods (mean, median, standard deviation, median and ratio), Student s t-test and Kruskal Wallis test were used for the comarison of the grous and ostgrou comarison was made with Tukey HDS and Mann Whitney U-tests. Correlations between the arameters were comared with Searman s correlation analysis. For the comarison of quantitative arameters, Pearson s chi-square test and Yates continuity correction test was used. Data were exressed as mean standard deviation. Results at < 0.05 were evaluated as significance level. Results Eidemiologic characteristics of the subjects (age and gender) according to the grous are shown in Table 1. There was no statistically significant difference for age and gender between the grous ( = 0.332; = 0.424, Student s t-test, chi-square test). The mean interval between eidemic conjunctivitis and examination was months. Mean number of corneal infiltrates was and mean score of haze due to infiltrates was in Grou 1A. All the atients in Grou 1 had used toical antibiotic and nonsteroid antiinflammatory or corticosteroid dros during their conjunctivitis eriods. Five atients had also used toical cyclosorine A after their conjunctivitis eriod in Grou 1. The mean HCVA and LCVA were significantly lower in the eyes with SEIs than fellow eyes and control grou ( = 0.001, Kruskal Wallis test; Table 2). There was no difference between the fellow eye and control eyes for HCVA ( = 0.885, Mann Whitney U-test), while LCVA value was lower in the fellow eyes when comared to control ( = 0.048). The mean values of sheric refraction, cylinder and sheric equivalent 378

3 Table 1. Eidemiologic characteristics of the atients. Conjunctivitis (n = 27) Control (n = 26) Mean SD Mean SD Age (year) Conjunctivitis (n = 27) Control (n = 26) Table 2. The arameters of sheric refraction, cylinder, sheric equivalent, visual acuity, contrast sensitivity, corneal toograhy arameters of sim K1, sim K2, cylinder, SAI, PVA, SRI values and aberration values of sheric aberration, coma, trefoil, irregular astigmatism and total high-order RMS values according to the grous. Grou 1A Grou 1B Grou 2 SEI Fellow eye Control Mean SD Mean SD Mean SD Sheric (0) (0) (0) refraction Cylinder (0) (0) (0) Sheric (0.37) (0.37) (0.50) equivalent High contrast (0.1) (0.0) (0.0) 0.001** visual acuity (logmar) Low-contrast visual acuity (logmar) (0.4) (0.1) (0.0) 0.001** Corneal toograhy Sim K (43.7) (42.5) (43.7) Sim K (43.02) (41.12) (42.90) Total cylinder (0.54) (0.56) (0.63) SAI (0.48) (0.39) (0.33) 0.001** PVA (17) (14) (15) 0.001** SRI (0.66) (0.37) (0.23) 0.001** Corneal aberrations Sheric (0.19) (0.04) (0.05) 0.001** aberration Coma (0.17) (0.20) (0.14) Trefoil (0.16) (0.15) (0.09) 0.005** Irregular (0.23) (0.12) (0.11) 0.001** astigmatism Total aberration (0.42) (0.35) (0.26) 0.001** Kruskal Wallis test, ** < Sim = simulated, SAI = surface asymmetry index, PVA = otential visual acuity, SRI = surface regularity index. values did not show a significant difference between the grous ( = 0.103; = 0.911; = 0.590). Corneal toograhy values of SAI, PVA and SRI were significantly higher in the eyes with SEIs from both fellow eyes and control grou, while there was n % n % Gender Male Female Student s t-test. 2 Chi-square (Yates continuity correction test), ** < no difference between fellow eyes and control grou ( > 0.05). The mean RMS value of sherical, trefoil, irregular astigmatism and total higher-order aberrations showed significant differences between the grous ( < 0.05), while there was no significant difference in coma aberration values between the grous ( = 0.146; Table 2). Sheric aberration, irregular astigmatism and total aberration were significantly higher in the eyes with SEIs when comared to fellow eyes and control grou ( < 0.05). There was no significant difference between fellow eye and control subjects for sheric aberration and irregular astigmatism ( = 0.417; = 0.463), while total aberrations were higher than control subjects in the fellow eyes ( = 0.001). Trefoil aberration was significantly higher than control subjects in the eyes with subeithelial infiltrates ( = 0.002), while no significant difference was observed between the fellow eye and control subjects ( = 0.075) or atients with SEIs ( = 0.515; Table 3). When we evaluated the correlation of the characteristics on the arameters measured, the number of the infiltrations and infiltration score showed significant correlation with irregular astigmatism and total aberration. Number of the infiltrations also showed a correlation with sheric aberration. Cylinder value showed a correlation with irregular astigmatism ( < 0.05, Searman s Correlation coefficient). HCVA and LCVA showed significant correlation with sherical, coma, trefoil, irregular astigmatism and total higher-order aberrations ( < 0.05). While age, sheric equivalent and conjunctivitis time interval did not show significant correlation with the aberration values measured ( > 0.05; Table 4). Five atients in Grou 1 had used toical cyclosorine A after their conjunctivitis eriod for the mean of months. Use of toical cyclosorine A did not have a significant effect on the arameters measured ( > 0.05). Mean sheric aberration value was in the atients who had used cyclosorine A, while it was in the atients who had not used it. Although sheric aberration value was smaller in the atients who had used cyclosorine A, the difference was not significant ( = 0.098). Discussion Eidemic keratoconjunctivitis is a highly contagious infection of the 379

4 Table 3. Results of the arameters that were significantly different between the grous according to ost hoc evaluation. Corneal infiltration (+)- Fellow eye ocular surface. Corneal SEIs are a sequel of the EKC and may stay dormant in the cornea for months or years (Lund & Stefani 1978). They may cause symtoms such as decrease in visual acuity, halo, glare and hotohobia (Hillenkam et al. 2002). In the resent study, we evaluated the visual erformance for the atients with SEIs by measuring the logmar of HCVA and LCVA. The mean HCVA and LCVA was significantly lower in the eyes with SEIs than fellow eyes and control grou, while LCVA was also worse in the fellow eyes when comared to control. Measurement of LCVA (10%) involves a horizontal movement at contrast sensitivity of aroximately 10. The difference in visual acuity between the HCVA and LCVA charts is an indicator of the sloe of the right hand ortion of the contrast sensitivity function and hence indicators of changes in medium satial Corneal infiltration (+)- Control Fellow eye- Control Visual acuity 0.001** 0.001** Contrast 0.001** 0.001** 0.048* SAI 0.043* 0.001** PVA 0.001** 0.001** SRI 0.009** 0.001** Sheric aberration 0.003** 0.001** Trefoil ** Irregular Astigmatism 0.002** 0.001** Total aberration 0.028* 0.001** 0.025* Mann Whitney U-test, * < 0.05; ** < SAI = surface asymmetry index, PVA = otential visual acuity, SRI = surface regularity index. frequency contrast sensitivity (Woods & Wood 1995). In our study, the difference between HCVA and LCVA was 2.4 lines in SEI grou, 1.7 lines in fellow eyes and 0.8 lines in control atients. The cornea is the most owerful refractive element of the eye. Thus, it has a fundamental role in retinal image quality. Imerfections in the corneal shae revent light rays from a distant oint source from converging into a single image oint on the retina. These focusing errors are known as otical aberrations (Maloney et al. 1993; Oliveira et al. 2012). In normal human eyes, high-order aberrations had significant negative correlations with visual erformance and coma-like aberration of the eye significantly influences contrast sensitivity function (Alegate et al. 2000; Oshika et al. 2006). In our study, HCVA and LCVA showed significant correlation with sherical, coma, trefoil, irregular astigmatism and total higher-order aberrations ( < 0.05). Corneal wavefront analysis is an imortant tool in clinical ractice for evaluating the ocular otical quality because the first refractive interface is the most imortant contributor to the total ower of the eye. Particularly in highly aberrated corneas, corneal aberrations amount to the most relevant otical errors in the organ. Another advantage of corneal wavefront analysis is that it rovides data that are not only richer but also is less affected by generic variables, such as accommodation and uil size (Oliveira et al. 2012). To our knowledge, the resent series is the first descrition of the effect of SEIs associated with EKC on corneal higher-order aberrations. We measured the corneal toograhy and corneal aberrations with Magellan Maer using a lacido disk system, which analyses corneal aberrometry through the Zernike decomosition software. Our results showed that corneal toograhy values of SAI, PVA and SRI were significantly higher in the eyes with SEIs from both fellow eyes and control grou, while there was no difference between fellow eyes and control grou ( > 0.05). During corneal aberrometry, the mean RMS value of sheric aberration, irregular astigmatism and total aberration was significantly higher in SEI grou when comared to fellow eyes and control grou ( < 0.05). Total aberrations were higher than control subjects in the fellow eyes. Trefoil aberration was higher in SEI grou only when Table 4. Correlation of the characteristics (age, infiltration number and score, cylinder, sheric equivalent, conjunctivitis time interval and high and low-contrast visual acuity) on the aberration arameters measured. Sheric aberration Coma Trefoil Irregular astigmatism Total aberration r r r r r Age Infiltration number * ** ** Infiltration score ** * Cylinder ** Sheric equivalent Conjunctivitis time interval HCVA ** * * ** ** LCVA ** ** ** ** ** r: Searman s Correlation coefficient, ** < 0.01; * < Sim = simulated, SAI = surface asymmetry index, PVA = otential visual acuity, SRI = surface regularity index, HCVA = high-contrast visual acuity, LCVA = low-contrast visual acuity. 380

5 comared to control subjects. While no significant difference was observed in coma aberration values between the grous ( > 0.05). During the correlation analysis the number of the infiltrations showed significant correlation with irregular astigmatism, sheric aberration and total aberration. Previous studies with corneal oacities such as corneal subeithelial haze after hotorefractive keratectomy (PRK) showed similar results with our data. Hayashida et al. (2006) has showed that the sub eithelial stromal oacity or haze that can develo in the visual axis after PRK can affect the atient s ostoerative visual acuity. Tanabe et al. (2004) showed that increases in higher-order aberrations layed a major role in the reduction of LCVA in eyes with mild to moderate corneal subeithelial haze after PRK. LCVA significantly correlated with total higher-order aberrations. Moreover, third-order (coma-like) and fourth-order (sherical-like) aberrations also showed significant correlations with LCVA. Our results showed similar results and HCVA and LCVA showed significant correlation with sherical, coma, trefoil, irregular astigmatism and total higher-order aberrations ( < 0.05). Jimenez et al. (2009) measured otical image quality and the contrast sensitivity function to enable the characterization of the otical quality and visual erformance in atients with keratitis. Ocular higher order, sherical and coma aberrations in keratitis eyes were significantly higher than those in healthy fellow eyes. After the resolution of the disease, a significant increase in the otical function and visual erformance was observed but, after treatment, significant imairment in the otical quality of the affected eyes continued to suffer comared with the healthy fellow eyes. They also roosed that the otical deterioration during keratitis could be because of the inflammatory changes occurring in the cornea that affected its otical roerties, such as variations in the trajectory of the light reaching the cornea (because of changes in corneal thickness) and/or the refraction index in different zones of the cornea affected by keratitis. They notified that these changes in otical roerties modify both the aberrations and the ocular scattering (Jimenez et al. 2009). The same mechanisms may exlain our findings in the atients with SEIs. Changes in otical aberrations created by tear-film break u may also contribute to the reduction in retinal image quality of the atients with SEI. Any local change in tear-film thickness and regularity will introduce aberrations into the otical system (Montes-Mico et al. 2010). Studies of the distribution of anterior corneal high-order aberrations in young and healthy oulations show large individual variability (Oliveira et al. 2012). The otical erformance of the eye has been shown to decrease with age due to the increase in high-order aberrations. Anterior corneal coma has been shown to increase with age, whereas sherical aberration generally did not change in revious studies (Guirao et al. 2000; Oshika et al. 2006), while in our study, age, sheric equivalent and conjunctivitis time interval did not show significant correlation with the aberration values measured. Currently, no secific anti-adenoviral drug is available for the treatment of EKC. The treatment remains urely symtomatic, with artificial teardros and antibiotics to revent or treat suer infection (Kinchington et al. 2005; Meyer-Rusenberg et al. 2011). Antiviral cidofovir was found to lower the frequency of severe corneal oacification in comarison to the control grou but dose-deendent toxicity has been observed on the conjunctiva, lid tissue and lacrimal duct (Hillenkam et al. 2002). The treatment of ersistent SEIs remains a major roblem. Steroid eye dros are effective for the suression of the symtoms and findings of EKC; however, side effects such as cataract, glaucoma and suer infections may occur on long term with high rate of steroid deendence and recurrence (Laibson 1984). Moreover, return of the oacities may be seen after discontinuation of corticosteroids, after re-infection or uer resiratory infection (Hodge et al. 1995). Chronic SEIs that do not resolve sontaneously over time can be treated locally with cyclosorine A eye dros (Levinger et al. 2010; Jeng & Holsclaw 2011). Okumus et al. (2012) reorted statistically significant imrovements in BCVA (logmar from before to after), and reduction of corneal SEI scores (from before to ) after the toical cyclosorine A treatment in the atients with corneal SEIs that have ersisted for more than 3 months due to adenoviral EKC. On the other hand, Hillenkam et al. (2001) did not find a difference in the frequency of corneal SEIs at the end of treatment with 1% cyclosorine A and 0.2% cidofovir eyedros. In our study, five atients in Grou 1 had used toical cyclosorine after their conjunctivitis eriod for the mean of months. Usage of toical cyclosorine did not have a significant effect on the arameters measured ( > 0.05). This study has several limitations. In the resent study, we only evaluated the anterior corneal surface and not the osterior corneal surface. Placido disk systems are limited in that they do not directly comute the elevation; they measure only the anterior corneal shae and the measurement axis is not the line of sight (Mandell 1992; Oliveira et al. 2012). Another limitation of our study is that we have included both eyes of each atient, which may induce statistical bias. We referred to include both eyes, because there may be an advantage in using both eyes in diseases which may be monocular then the fellow eye essentially healthy, one eye can be regarded as the diseased eye and the other as the control (Armstrong 2013). The small number of the atients and the cross-sectional design of the study are the other limitations of this study. As a result, our data for corneal toograhy and aberrometry revealed significant differences ( < 0.05) between results for the SEIs eyes with resect to values for the healthy fellow eyes and control atients reflecting comromised visual erformance and otical quality. 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