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Optometry & Vision Science:
doi: 10.1097/OPX.0b013e318281980f
Original Articles

Higher Order Aberrations After Keratoplasty for Keratoconus

Salvetat, Maria Letizia*; Brusini, Paolo*; Pedrotti, Emilio*; Zeppieri, Marco; Miani, Flavia*; Marcigaglia, Mattia*; Passilongo, Mattia*; Marchini, Giorgio*

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Author Information

*MD

MD, PhD

Department of Ophthalmology, S. Maria della Misercordia Hospital, Udine, Italy (MLS, PB, MZ, FM); and Eye Clinic, Department of Neurological and Visual Sciences, University of Verona, Verona, Italy (EP, MM, MP, GM).

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s Web site (www.optvissci.com).

Paolo Brusini Department of Ophthalmology Azienda Ospedaliero-Universitaria Santa Maria della Misericordia 15 33100 Udine Italy e-mail: brusini@libero.it

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Abstract

Purpose: To compare higher order aberrations (HOAs) caused by the anterior and posterior corneal surfaces after conventional penetrating keratoplasty (PK), deep anterior lamellar keratoplasty (DALK), and automated lamellar therapeutic keratoplasty (ALTK) in patients undergoing corneal transplantation for keratoconus (KC).

Methods: This retrospective, observational, cross-sectional study included one eye of the following subjects: 40 patients with KC, 23 KC patients after PK, 17 KC patients after DALK, 18 KC patients after ALTK, and 38 healthy controls. All underwent imaging with a rotating Scheimpflug camera (at least 6 months after complete suture removal in grafted subjects) to assess the HOAs from the anterior and posterior corneal surfaces within the central 4-mm and 6-mm zones. The conversion of the corneal elevation profile into corneal wavefront data was performed using Zernike polynomials. Total and third- and fourth-order HOAs were considered. The root mean square of the Zernike vector magnitude, expressed in micrometers, was used. Differences among groups were assessed using the Kruskal-Wallis and Duncan multiple range tests. Statistical significance was defined as p < 0.05.

Results: In both 4-mm and 6-mm central zones, the total HOAs from the anterior corneal surfaces were significantly lower in DALK than in ALTK and PK groups (p < 0.05). The total HOAs from the posterior corneal surface were comparable amongst postoperative groups (p > 0.05). The aberration components that were significantly greater included coma in the KC and ALTK eyes, trefoil and coma in the DALK eyes, and trefoil in the PK eyes.

Conclusions: The corneal anterior surface optical quality appeared significantly better after DALK than after ALTK and PK.

Keratoconus (KC) is a noninflammatory corneal disorder characterized by the progressive thinning of the central stroma and asymmetric anterior corneal protrusion.1 These pathologic processes induce a great amount of irregular astigmatism, also known as higher order aberrations (HOAs),2–5 and in later stages, corneal scarring, which all lead to impaired visual function.

Nowadays, deep anterior lamellar keratoplasty (DALK) is considered as the first surgical option for KC.6–10 The aim of this technique involves reshaping the corneal profile by selectively removing and replacing most of the anterior corneal stroma while preserving the host’s healthy endothelium. The main advantages of DALK compared with penetrating keratoplasty (PK) include the reduced risk of endothelial immunologic rejection and graft failure.8–12 Several studies have reported comparable postoperative visual outcomes after DALK and PK7–10; however, others have shown reduced or unsatisfactory visual performances after lamellar procedures despite graft transparency, especially in cases in which a significant amount of pre-Descemet stroma is left on the recipient bed.6,13 Some authors have suggested that residual stromal scarring and increased irregularities at the corneal surfaces and/or donor-host interface can induce enhanced HOAs and light scattering,14 thus limiting the quality of vision after DALK surgery.

Various DALK techniques have been developed with the aim of providing better postoperative visual performances. Automated lamellar therapeutic keratoplasty (ALTK) uses a microkeratome to perform the lamellar dissection,15 which was designed to provide a smoother donor-host interface of higher optical quality. Studies have shown ALTK to be an effective alternative surgical technique in treating patients with KC.15 The advantages offered by ALTK compared with other DALK techniques include simplicity, rapidity, and standardization in most of the surgical steps.

To minimize the residual scarring and graft-host interface irregularity, descemetic-DALK procedures aim at a subtotal stromal removal, thus maintaining only Descemet membrane and endothelium for transplantation.16–18 The DALK technique considered in our study, known as deep lamellar keratoplasty (DLKP) by intracorneal dissection, has been proposed by the University of Verona.19 It is based on the development of a new kit of instruments used for a manual stromal delamination, which intentionally leaves a minimal thickness of deep stroma on the host bed before the donor button is sutured to simplify the surgical technique and to reduce the risks of intraoperative Descemet membrane rupture.19

Wavefront analysis is a diagnostic method that is able to provide an objective assessment of the optical quality of the ocular refractive surfaces by means of assessment of the low- and higher order aberrations of the eye.20–22 The evaluation of the corneal wavefront errors, thus, may have a role in understanding the effect of various graft techniques on the corneal optical quality2,4,6,8,10,23 and in objectively assessing the quality of vision perceived by the patient after corneal transplant. The rotating Scheimpflug imaging system is a relatively new noncontact method able to provide highly repeatable measurements of the anterior and posterior corneal curvatures, which can be converted into corneal aberrations measurements by the built-in software.24,25

The purpose of the study was to compare the corneal optical quality after conventional PK, ALTK, and DALK in patients undergoing corneal transplantation for KC by measuring the HOAs of the anterior and posterior corneal surfaces. Measurements were taken for the 4-mm and 6-mm central optical zone to determine the optical quality for photopic and scotopic vision, respectively.

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METHODS

This retrospective, observational, comparative, cross-sectional study included one eye of the following consecutive subjects: 40 patients with KC, 23 KC patients after PK, 17 KC patients after DALK, 18 KC patients after ALTK, and 38 age-matched subjects with normal corneas (control group) (Table 1).

Table 1
Table 1
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The study was in compliance with the tenets of the Declaration of Helsinki, and informed consent was obtained from all participants before testing. Each participant underwent the following examinations on the same day: complete ophthalmologic examination, including a review of medical history, best spectacle-corrected visual acuity (BSCVA) measured using the Snellen VA chart, manifest refraction evaluation (including spherical equivalent and cylindrical error), slit lamp examination, fundus biomicroscopy, and Goldmann applanation tonometry measurement; recipient bed thickness measurement in ALTK and DALK eyes using optical coherence tomography (OCT) (Nidek RS-3000; Nidek Co, Ltd, Japan); and imaging with a Scheimpflug-based corneal topographer (Sirius 3D; CSO, Florence, Italy).

Normal subjects were recruited from staff members and volunteers. Keratoconus, PK, and ALTK patients were recruited from the Cornea Clinic of the Department of Ophthalmology at S. Maria della Misericordia Hospital, Udine, Italy. Deep anterior lamellar keratoplasty patients were recruited from the Eye Clinic of the Department of Neurological and Visual Sciences of the University of Verona, Verona, Italy. The study was in compliance with Institutional Review Board and Health Insurance Portability and Accountability Act requirements for the institute involved in the study. The study was approved by the Institutional Review Board of both the S. Maria della Misericordia Hospital and the Department of Neurological and Visual Sciences of the University of Verona.

Normal eyes were defined as absence of ocular disorders except for refractive errors, normal cornea appearance, normal corneal topography results, no history of ocular surgery and no previous corneal or conjunctival disease that is likely to affect the corneal HOAs, and no family history of ocular pathologies. Keratoconus was diagnosed by experienced clinicians based on slit lamp findings (corneal ectasia, stromal thinning, Fleischer ring, and/or Vogt striae) and keratometry, which was confirmed by conventional corneal topography.1

Corneal diseases requiring keratoplasty included moderate (mean keratometry between 46 and 55 diopters [D]) to advanced keratoconus (mean keratometry >55 D or immeasurable keratometry) with apex opacity or poor spectacle-corrected visual acuity, rigid gas-permeable contact lens intolerance, or unsuccessful contact lens fit. The indications for PK included central corneal pachymetry measurements less than 400 μm, coexistence of other corneal pathologies, and presence or history of acute corneal hydrops. Penetrating keratoplasty,26 ALTK,15 and DALK19 techniques have extensively been described elsewhere and have briefly been described in the Appendix (available at http://links.lww.com/OPX/A113). All PK and ALTK surgeries were performed by a single surgeon (P.B.) from March 2006 to January 2008 at the Department of Ophthalmology of the S. Maria della Misericordia Hospital. In each case, local anesthesia and akinesia were achieved with a peribulbar injection of 10 cm3 of a 1:1 mixture of bupivacaine 0.75% and lidocaine 2%. All DALK surgeries were performed under general anesthesia by a single surgeon (G.M.) from December 2005 to May 2008 at the Department of Neurological and Visual Sciences of the University of Verona. Donor corneas in the form of a sclerocorneal button stored in organ culture at 31°C were provided by the Fondazione Banca degli Occhi del Veneto (Venezia-Mestre, Italy) Eye Bank. In PK and ALK eyes, the running suture was removed 12 and 6 months after surgery, respectively.

Inclusion criteria were keratoconus at various stages; absence of ocular pathology other than keratoconus; no family history of ocular pathologies other than keratoconus; previous PK, DALK, or ALTK for keratoconus in grafted subjects (at least 6 months after complete suture removal); reliable rotating Scheimpflug camera measurements; and willingness to provide informed written consent.

Exclusion criteria included:

* for KC eyes: corneal scarring, history of acute hydrops, other disorders that prevented reliable wavefront measurements

* for postkeratoplasty eyes: corneal scar or opacity of the graft, history of postoperative ocular infection or trauma, persistent epithelial defect, severe dry eye or ocular cicatricial diseases, graft rejection, presence of ocular diseases other than KC or keratoplasty for KC, systemic diseases or medications that could affect the ocular surface, and history of intraocular surgery other than keratoplasty.

The Sirius 3D rotating Scheimpflug camera (CSO) was used for all corneal measurements. This noncontact instrument combines a rotating Scheimpflug camera with a Placido disk technique, providing high-resolution images of the anterior segment, anterior and posterior corneal topography, and pachymetry of the entire cornea. The system uses a rotating Scheimpflug camera and a monochromatic slit-light source that rotate together around the optical axis of the eye for 180 degrees and acquires 25 to 50 images from the anterior segment. By means of the device software, the conversion of the corneal elevation profile into corneal wavefront data is performed using the Zernike vector terms27 with an expansion up to the 10th order. The root mean square of the Zernike vector magnitude is calculated and expressed in micrometers. Data from an area of up to 10 mm in diameter are provided by the instrument. The automatic release mode was used, which achieves correct focus and alignment with the corneal apex before starting scanning. Three measurements were taken by the same experienced examiner (L.P.) from each eye, and the best scan with the least distorted Scheimpflug image was used for analysis. All measurements were collected at the last visit and at least 6 months after complete suture removal for postkeratoplasty eyes. The following measurements were considered: simulated keratometric (simK1 and simK2) values in the 3-mm central zone and root mean square of the Zernike vector magnitude of the total HOAs and third- and fourth-order aberrations of the anterior and posterior corneal surfaces within the central 4-mm and 6-mm zones. Total HOAs were defined as the sum of the magnitude of the Zernike vector terms of the third to seventh order.

Data were analyzed using the statistical analysis software SPSS for Windows, version 20.0 (SPSS Inc, Chicago, IL). Normality of the data distribution was assessed with the Kolmogorov-Smirnov test. Data were described by medians (SD) and 95% confidence interval, which showed a non-normal distribution. Intragroup differences were assessed using the Wilcoxon and Friedman tests. Intergroup differences were calculated using the Mann-Whitney U and Kruskal-Wallis tests. The Duncan multiple range test was used for multiple comparisons. To avoid bias related to patient age, the intergroup comparison was analyzed with a multivariate general linear model using the variable age as a covariant. Correlations were tested using the Spearman rank correlation coefficient. Statistical significance was defined as p < 0.05.

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RESULTS

Detailed demographic, functional, and refractive characteristics of the five groups of subjects are listed in Table 1.

The wavefront analysis of corneal HOAs of the five groups is summarized in Table 2.

Table 2
Table 2
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Table 2
Table 2
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Anterior Corneal Surface

Considering the intergroup comparison results, the total HOAs within the 4-mm zone appeared highest in the KC eyes, followed by the ALTK and PK groups, then DALK eyes, and lowest in controls. The total HOAs within the 6-mm zone were higher in the KC, ALTK, and PK eyes; intermediate in the DALK eyes; and the lowest in controls. Trefoil and tetrafoil were significantly higher in the PK eyes; intermediate in the KC, ALTK, and DALK eyes; and lowest in controls. Coma appeared significantly higher in the KC and ALTK eyes, intermediate in the DALK and PK eyes, and the lowest in controls. Spherical aberration and secondary astigmatism were significantly lower in controls than in other groups. The intragroup comparison revealed that the aberration components that were significantly higher included coma and spherical aberration in controls, coma in the KC and ALTK eyes, trefoil and coma in the DALK eyes, and trefoil in the PK eyes.

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Posterior Corneal Surface

The intergroup comparison showed that the total HOAs, trefoil, spherical aberration, and secondary astigmatism appeared significantly lower in controls than in the other groups. Within the 4-mm zone, coma appeared highest in KC and ALTK eyes, followed by the DALK eyes, then less in the PK eyes, and lowest in controls. Within the 6-mm zone, coma was higher in the KC, ALTK, and DALK eyes; intermediate in PK eyes; and the lowest in controls. Tetrafoil was significantly lower in controls than in the other groups within the 4-mm zone; whereas, it appeared higher in the PK eyes, intermediate in the KC, ALTK, and DALK eyes, and the lowest in controls within the 6-mm zone. The intragroup comparison indicated that the aberration components that were significantly higher within the 4-mm zone were trefoil in the control, DALK, and PK eyes and trefoil and coma in the KC and ALTK groups. With regard to those within the 6-mm zone, they included trefoil in the control and PK eyes and trefoil and coma in the KC, ALTK, and DALK eyes.

Representative wavefront maps of anterior and posterior corneal surfaces in normal, KC, ALTK, DALK, and PK eyes are shown in Fig. 1. The correlations between the BSCVA and the magnitude of the HOAs of both corneal surfaces were not statistically significant in any of the five groups (p > 0.05).

Figure 1
Figure 1
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DISCUSSION

Irregularities of the refractive surfaces of the eye cause irregular astigmatism, which is not correctable by conventional spectacles or soft contact lenses.20,22 Great amounts of HOAs have been shown to decrease the optical quality of the retinal image, thus reducing the optical performance of the eye by inducing halos, glare, monocular diplopia, and decreased contrast sensitivity and visual acuity,28,29 especially under mesopic or scotopic conditions.30 The cornea is the main contributor of HOAs in the eye, and regardless of cause, corneas with increased wavefront error show significant decreases in visual performances that is pupil size dependent.31,32

In agreement with previous authors,5 our results showed that, in normal eyes, the amount of the corneal HOAs within both 4-mm and 6-mm central zones was minimal, suggesting that only a small part of the variance in visual performance of normal eyes both under photopic and scotopic conditions can be attributed to wavefront error variations.29

Aberrometric studies conducted with both ocular or corneal wavefront sensors have demonstrated that KC eyes show a great amount of HOAs2–5 because of both corneal surfaces5,33 and that corneal HOAs can be useful for early detection,34 grading,35 and predicting visual performance of KC eyes.36 In agreement with previous authors,5,33 our results showed a higher amount of total HOAs from both corneal surfaces in the KC eyes as compared with normal eyes.

In comparison with the postkeratoplasty groups, the magnitude of the total HOAs from the anterior corneal surface was higher in the KC group within the 4-mm zone and comparable within the 6-mm zone; however, the magnitude of the total HOAs from the posterior corneal surfaces was comparable between KC and postkeratoplasty eyes. These data are indicative of higher visual impairment under photopic conditions in the KC eyes. These differences can obviously vary based on the severity of KC.

In accordance with our results, the most significant aberration component found by previous studies in the KC eyes was an increased coma from both anterior2–5 and posterior5,33 corneal surfaces, the cause of which can be due to the characteristic cone-shaped development on the KC cornea as it degenerates.

Considering the postkeratoplasty eyes, the results of our study showed that, in comparison with controls, the grafted eyes showed a significantly higher magnitude of the total and third- and fourth-order corneal HOAs within both 4-mm and 6-mm central zones. In agreement with our data, both PK2,4,6,8,10,23,37 and DALK6,8,10,23 for KC have been associated with considerable amounts of ocular and/or corneal HOAs. These results suggest the important role of irregular astigmatism after corneal grafting, which may cause visual distortions and limit the visual rehabilitation under both photopic and scotopic conditions in these postoperative patients.37

Previous studies have reported that ocular HOAs were either comparable6,10 or significantly higher8 after descemetic-DALK when compared with PK for KC patients. Our data regarding the corneal HOAs showed, however, that although the magnitude of the total HOAs from the posterior corneal surface was comparable among postkeratoplasty eyes, those arising from the anterior corneal surface within both 4-mm and 6-mm central zones were significantly lower in DALK eyes when compared with both the PK and ALTK groups, thus suggesting an overall better optical quality of the anterior surface in the DALK group. These results could be explained by a better recipient-donor match and a higher interface regularity in our DALK eyes that all underwent the “DLKP by intrastromal dissection” procedure, in which the donor button tends to neatly position into alignment over the minimal pre–descemetic layer.

The aberration components greatly differed among postkeratoplasty groups. The most dominant aberration components from the anterior corneal surface, that is the most both within the 4-mm and 6-mm zones, were coma in the ALTK eyes, trefoil in the PK eyes, and both coma and trefoil in DALK eyes that were equally represented and appeared significantly lower when compared with those of the other postkeratoplasty groups.

The prevalence of trefoil after PK for KC has been already reported,4,37 which can be attributed to the wound malapposition caused by irregular wound incision profiles and differences in diameter, which can cause peripheral local deformations of the transplanted cornea. Coma and spherical aberration, also found in PK eyes,4 have been attributed to slight decentration of the donor cornea and mid-peripheral steepening induced by the wound, respectively.

Considering that coma is the dominant HOAs component in KC eyes,2–5,33 its prevalence after ALTK for KC could be caused by the standardized lamellar cut provided by the microkeratome on KC corneas, which are characterized by a wide range of corneal curvatures and stromal thickness irregularities. It is possible to speculate that the automatized cut is likely to leave an inhomogeneous recipient bed, which tends to be thinner at the cone apex and thicker in the periphery; thus, the apposition of the donor lamella on this irregular bed could partially reproduce the typical keratoconic anterior corneal profile postoperatively.

Experimental studies have demonstrated that different HOA components have a different impact on vision. Zernike terms having a greater effect on the central portion of the wavefront, such as coma, spherical aberration, and secondary astigmatism can adversely affect visual performance much more than terms near the edge of the Zernike pyramid, such as trefoil or tetrafoil, which play an important role in retinal image quality degradation only under mesopic or scotopic conditions.28,38–40 Penetrating keratoplasty and ALTK eyes showed a comparable amount of total HOAs from both corneal surfaces, indicating that these surgical procedure induce a similar total amount of corneal surfaces irregularity. The prevalence of trefoil in PK eyes and of coma in ALTK eyes suggests a greater central corneal configuration distortion, thus giving rise to a higher optical impairment, after ALTK compared with that after PK. These results are in agreement with the lower BSCVA found in the ALTK group in comparison with that of the PK group.

The surgical treatment of choice in KC is still not clear and remains a debatable issue. The results of our study are helpful in understanding the outcomes after penetrating and lamellar keratoplasty for KC. Our data showed an overall higher anterior corneal profile regularity after descemetic-DALK procedure than after conventional PK and ALTK and a greater central anterior corneal configuration distortion after ALTK than after PK and DALK, suggesting that DALK is superior to ALTK and PK in terms of providing a better anterior surface corneal optical quality. The ALTK procedure seems limiting with regard to reshaping the corneal profile in that an irregular corneal configuration remains after surgery, especially with regard to the anterior corneal profile, which is less pronounced but similar to that found in KC eyes. Although the correlations between the corneal wavefront data and patient BSCVA were not significant, the higher amount of coma from the anterior corneal surface within both 4-mm and 6-mm zones found in ALTK eyes, as compared with those found in DALK and PK eyes, can theoretically negatively affect the quality of vision and patient satisfaction postoperatively both under photopic and scotopic conditions. The lower BSCVA found in the ALTK eyes in comparison with the DALK and PK eyes supports this hypothesis even if other factors such as residual stromal scarring or graft-host interface irregularity can be regarded as causes of visual impairment after ALTK. Our visual results are in agreement with previous studies showing that the descemetic-DALK techniques are superior in terms of visual outcomes when compared with pre–descemetic-DALK techniques6,9,12,13,19,41 and that the visual performance after ALTK is worse than that obtained with PK and descemetic-DALK procedures.41

In disagreement with previous authors,4,36,37 significant correlations were not found between BSCVA and the magnitude of the total and third- and fourth-order corneal HOAs in normal, KC, and postkeratoplasty eyes; the hypothesis that the differences in wavefront errors may be responsible for the differences in BSCVA in these patients thus cannot be proven in this study. The lack of significant relationship between BSCVA and the HOAs magnitude can partially be explained by the fact that the high-luminance, high-contrast VA has shown to be relatively insensitive to variation in wavefront errors, especially when acuity is scored to line as opposed to the letter, as done in our study.20,30

Our study has several limitations, including that it was based on retrospective data, the number of eyes considered was relatively small, and the instrument reproducibility was not assessed. Moreover, the differences among the three postoperative groups because of patient age, graft/host diameter disparity, and surgeon and suture technique may have caused a bias that needs to be taken into consideration when evaluating the intergroup differences.

In conclusion, the results of our study seem to indicate that the DALK procedure can provide a higher postoperative corneal anterior surface optical quality when compared with the ALTK and PK techniques in patients affected by KC.

Further studies evaluating the contrast sensitivity and the low-contrast visual acuity under mesopic and scotopic conditions are needed to better assess the influence of the corneal wavefront error on the visual quality after PK and ALK surgery for KC.

Paolo Brusini

Department of Ophthalmology

Azienda Ospedaliero-Universitaria

Santa Maria della Misericordia 15 33100

Udine, Italy

e-mail: brusini@libero.it

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ACKNOWLEDGMENTS

The authors have no financial or commercial interests to disclose. The study was performed without financial assistance, support, or funding.

Received August 2, 2012; accepted November 21, 2012.

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APPENDIX

The appendix is available online at http://links.lww.com/OPX/A113.

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Keywords:

keratoconus; deep anterior lamellar keratoplasty (DALK); automated lamellar therapeutic keratoplasty (ALTK); penetrating keratoplasty; corneal higher order aberrations

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© 2013 American Academy of Optometry

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