Evaluation of bilateral minimum thickness of normal corneas based on Fourier-domain optical coherence tomography

ARTICLE

Evaluation of bilateral minimum thickness of normal corneas based on Fourier-domain optical coherence tomography Gaurav Prakash, MD, Dhivya Ashok Kumar, MD, Amar Agarwal, MS, FRCS, RCOphth, Yoga Sarvanan, ME, Soosan Jacob, MS, DNB, FRCS, Athiya Agarwal, MD, DO

PURPOSE: To determine the normative ranges and various aspects of the relationship between the minimum corneal thicknesses (MCT) in fellow eyes and the location of the MCT in relation to the central cornea using Fourier-domain optical coherence tomography (OCT). SETTING: Tertiary care ophthalmic hospital, Chennai, India. METHODS: In this cross-sectional observational trial, both eyes of consecutive healthy young subjects with a low refractive error and no clinical or topographic evidence of corneal disorders had bilateral pachymetric assessment with a Fourier-domain OCT platform (RTVue). The MCT, central corneal thickness (CCT), and x–y coordinates of the MCT location were noted. RESULTS: The CCT and MCT followed a normal distribution with a good correlation. The difference between CCT and MCT was approximately 5 mm in right eyes and left eyes (P<.05 for both). The difference in CCT was the best predictor of the difference in MCT. The mean distance from the center (0.63 mm G 0.13 [SD], right eyes; 0.66 G 0.17 mm, left eyes) was well correlated. The MCT points in fellow eyes tended to be symmetrical along the vertical midline. The mean angular distance between mirror-superimposed MCT points was 20.54 G 17.6 degrees and the mean linear distance, 0.25 G 0.17 mm. CONCLUSIONS: The findings establish normative MCT pachymetry data and location using Fourierdomain OCT. The MCT and CCT points, although symmetrical, differed significantly in location and magnitude and should be evaluated separately in normal eyes and eyes with disease. Financial Disclosure: No author has a financial or proprietary interest in any material or method mentioned. Additional financial disclosures are found in the footnotes. J Cataract Refract Surg 2010; 36:1365–1372 Q 2010 ASCRS and ESCRS

A tendency toward structural symmetry has been observed in fellow eyes of humans. The retinal nerve fiber layer, retinal capillary perfusion, astigmatic axis, higher-order aberrations (HOAs), and overall corneal thickness, as well as the epithelial thickness, have similar patterns, mirror-symmetric patterns, or both.1–11 Minimum corneal thickness (MCT) is an important parameter in surgical planning and in the detection of pathology in certain corneal and refractive surgery procedures, in which accurate assessment of MCT and its location is crucial.12–16 Errors in pachymetric measurement are factors in poor surgical outcomes, including ectasia after laser in situ keratomileusis.17–19 Corneal topographic assessment can be inaccurate in the presence of motion artifacts. Fourier-domain Q 2010 ASCRS and ESCRS Published by Elsevier Inc.

optical coherence tomography (OCT), also known as frequency-domain tomography, overcomes this problem to a large extent because of its high acquisition speed.21,22,A In Fourier-domain OCT, the light from the reference arm interferes with the reflected light, generating spectral interference fringes that are eventually analyzed using Fourier transformation.20–22 Therefore, information in an entire A-scan area can be acquired by a charge-coupled device camera simultaneously. This increases the acquisition rate many times without physical movement.20–22 Recently, we found that Fourier-domain OCT has better repeatability than time-domain OCT (Visante, Carl Zeiss) for minimum, central, and paracentral corneal thickness measurements.23 A previous study24 0886-3350/$dsee front matter doi:10.1016/j.jcrs.2010.02.023

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found that time-domain OCT pachymetry correlates better with the gold standard (ultrasound pachymetry) than with Orbscan pachymetry (Bausch & Lomb). The aim of the current study was to determine the normative ranges and various aspects of the relationship between the minimum corneal thicknesses (MCT) in fellow eyes and the location of the MCT in relation to the central cornea using Fourier-domain optical coherence tomography (OCT). To our knowledge, no similar study using the Fourier-domain OCT platform has been published.

SUBJECTS AND METHODS This trial was performed at a tertiary care ophthalmic hospital and approved by the institutional review board. The research followed the tenets of the Declaration of Helsinki. After receiving an explanation of the nature of the study, all subjects provided informed consent. The participants in the study were normal young volunteers with no previously documented ocular morbidity other than a myopic error less than or equal to 3.00 diopters (D). Slitlamp evaluation was performed to rule out corneal disorders, including ectatic disorders, scarring, or thinning. Orbscan IIz topographic evaluation was also performed in all cases. The KISA% index25 and the Melki and Azar Massachusetts Eye and Ear Infirmary index26 were used to rule out cases of keratoconus and cases suspected of keratoconus. Fellow eyes with unilateral forme fruste or more severe keratoconus were excluded from the study. No subject wore contact lenses. To minimize the effect of diurnal variation in corneal thickness,27,28 all tests were performed between 2 PM and 5 PM by the same experienced examiner. The sequence of examination (right, left–left, right) was randomized by a computer-generated sequence of 100 randomly selected options using the numbers 1 and 2 (1 Z right eye examined first; 2 Z left eye examined first). Corneal assessment was performed using the RTVue OCT systemA (Optovue, Inc.), which takes 26 000 A-scans per second, a much higher acquisition speed than with most other available anterior segment assessment devices. The optional cornea anterior module was used for anterior segment imaging. The scan beam wavelength is 840 nm G 10 (SD) and the exposure power at the pupil, 750 mW.A The L lens of the module can acquire 6.0 mm  6.0 mm scans of the cornea for pachymetric analysis. The frame rate is 256 to 4096 A scans/frame. The resolution depth is 5.0 mm and the

transverse resolution, 15.0 mm. The scan beam wavelength is 840 G 10 nm and the exposure power at the pupil, 750 W. The subject’s head was positioned on the headrest. The examiner observed the infrared (IR) image of the cornea on the examination screen. All scans were performed with the subject’s eye wide open by his or her own effort. Scanning was performed on visualization of a centered bright IR image of the central cornea. No topical anesthesia or lubricating drops were used. The scan was repeated if the first was decentered or had a poor corneal apex reflection. The output screen of the OCT system shows an IR image of the cornea in the upper right followed by, in clockwise direction, keratoconus analysis data, an axial scan of the cornea, a color-coded corneal pachymetry map, and a numerical data map divided into zones (Figure 1). The 2.0 mm central zone is surrounded by a 2.0 to 5.0 mm zone and a 5.0 to 6.0 mm zone divided into 45-degree subtending angles. The mean pachymetry in the respective zones is included in the output. The MCT and its relation to the center of the cornea are shown in the keratoconus analysis box. The location is also marked on the colorcoded pachymetric map.

Mathematical Calculations and Transformations The distance of the MCT from the center of the cornea was calculated as  0:5 D Z x2 þ y2 To assess symmetry, the left-eye coordinates were transformed along possible axes to match the right eye data and evaluated for patterns and symmetry. A direct symmetry model was evaluated with the original values of R(x, y) and L(x, y). Then, reflections were performed along the yaxis (vertical midline, x Z 0), along the x-axis (horizontal midline, y Z 0), and across the equivalence diagonal (y Z x). The distance between the right-eye coordinates R(x, y) and the transformed left-eye coordinates (x0 , y0 ) was calculated as h i0:5 2 2 S Z ðRx  Lx0 Þ þ ðRy  Ry0 Þ To determine the angular distance, the angle q between R and L0 was calculated as q Z cos1 fðR  L0 Þ=ðjRj jL0 jÞg where R  L0 Z ðRx  Lx0 þ Ry  LyÞ and the cross product of R is L0 h h 0:5 i 0:5 i  Lx2 þ Ly2 jRj  jL0 j Z Rx2 þ Ry2

Submitted: August 20, 2009. Final revision submitted: January 15, 2010. Accepted: February 13, 2010.

The angle was then converted from radians to degrees.

From Dr. Agarwal’s Group of Eye Hospitals, Chennai, India.

The data were analyzed using SPSS software (version 16.0, SPSS, Inc.). Paired t tests were used to analyze the differences in mean values, which are reported with the standard deviation. Correlation coefficients and best-fit linear equations were computed to assess the correlation between measurements in right eyes and measurements in left eyes. Bland-Altman plots were drawn to show the effect of corneal thickness on the difference in measurements between the 2

Statistical Analysis

Additional financial disclosures: Dr. Amar Agarwal is a consultant to Abbott Medical Optics Inc., Staar Surgical Co., and Bausch & Lomb. Corresponding author: Amar Agarwal, MS, FRCS, FRCOphth, Dr. Agarwal’s Eye Hospital and Eye Research Centre, 19, Cathedral Road, Chennai-600 086, India. E-mail: [email protected].

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Figure 1. Pachymetric output of the Fourier-domain OCT device. Clockwise from top left: Infrared image capture, keratoconus analysis box, color-coded pachymetric map, and the zone thickness map.

eyes and the 95% limits of agreement (95% LoA). To prevent confusion from the x and y coordinates at the thinnest point, the regression fit-related linear equations in the study are presented as b Z ma C c rather than in the conventional

y Z mx C c form, where a and b are the x and y coordinates, respectively, of the regression fit line; m is the gradient of the straight-line graph; and c is the y intercept of the straight-line graph.

RESULTS Demographics The study evaluated 200 eyes of 100 subjects (52 men, 48 women) with a mean age of 25.4 G 1.8 years (range 23 to 32 years). The mean spherical equivalent was 1.02 G 0.7 D (range 3.0 to 0.0 D) in right eyes and 1.04 G 0.6 D (range 3.0 to 0.0 D) in left eyes. Corneal Pachymetry

Figure 2. Frequency distribution of CCT and MCT in right eyes and left eyes (CCT Z central corneal thickness; LE Z left eye; MCT Z minimum corneal thickness; RE Z right eye).

Central Corneal Thickness Both right-eye and left-eye pachymetric values followed a normal distribution curve (P Z .5 and P Z .3, respectively; KolmogorovSmirnov test for normality) (Figure 2). The mean central corneal thickness (CCT) was 517.3 G 35.4 mm (range 440 to 624 mm) in right eyes and 516.6 G 36.0 mm (range 450 to 636 mm) in left eyes. The mean difference between the CCT in right eyes and left eyes was 0.68 G 5.9 mm (P Z .25, paired t test). There was a statistically significant correlation between the CCT in right eyes and the CCT in left eyes (r Z 0.98, (P!.001). Figure 3, A, shows the best-fit line, suggesting an excellent linear fit (r2 Z 0.97).

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Figure 4. Overlay Bland-Altman plot showing the difference in fellow-eye pachymetry as a function of the mean pachymetry in right eyes and in left eyes.

511.7 G 35.7 mm (range 440 to 633 mm) in left eyes. The mean difference in the MCT between right eyes and left eyes was 0.29 G 5.86 mm (P Z .6, paired t test).There was a statistically significant correlation between the 2 MCT values (r Z 0.98, P!.001). Figure 3, B, shows the best-fit line, suggesting an excellent linear fit (r2 Z 0.97).

Figure 3. Linear best-fit plots between pachymetric values. A: Central corneal thickness in right eye (CCTR) and left eye (CCTL). B: Minimum corneal thickness in right eye (MCTR) and left eye (MCTL).

Minimum Corneal Thickness Both right-eye and lefteye values followed a normal distribution curve (P Z .5 and P Z .7, respectively; KolmogorovSmirnov Z test) (Figure 2).The mean MCT was 511.9 G 35.2 mm (range 435 to 624 mm) in right eyes and

Difference Between Central and Minimum Pachymetry The mean pachymetric difference between the CCT and the MCT was 5.34 G 4.48 mm in right eyes and 4.95 G 3.6 mm in left eyes (both P!.001, paired t test). Relationship Between Thicknesses in Thinner and Thicker Corneas An overlay Bland-Altman plot to determine whether the difference in fellow-eye MCT or CCT

Table 1. Symmetry analysis of the right and left eye coordinates. Original Coordinates (Mean G SD) Right Eye Transform Group I II III IV

Left Eye

Rx

Ry

Lx

Ly

Transform Along Line

0.51 G 0.20 0.51 G 0.20 0.51 G 0.20 0.51 G 0.20

0.28 G 0.43 0.28 G 0.43 0.28 G 0.43 0.28 G 0.43

0.51 G 0.28 0.51 G 0.28 0.51 G 0.28 0.51 G 0.28

0.21 G 0.33 0.21 G 0.33 0.21 G 0.33 0.21 G 0.33

None xZ0 yZ0 xZy

Transform Z transformation *Analysis of variance, Tukey HSD

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was more or less in thinner or thicker corneas (difference in pachymetry as a function of mean pachymetry for MCT and CCT separately) showed a 95% LoA range of 23.5 mm and 25.8 mm for MCT and CCT, respectively. Both measures showed a poor statistically nonsignificant linear fit (Figure 4). Location of Minimum Corneal Thickness The Cartesian location of the point of MCT was given in the output screen as x and y coordinates (in millimeters), with the center of the cornea being 0.0. Therefore, the right-eye and left-eye coordinates were denoted as R(x,y) and L(x,y). The mean value of the x coordinate was 0.51 G 0.21 mm (range 0.91 to 0.06 mm) in right eyes (Rx) and 0.46 G 0.32 mm (range 0.30 to 1.09 mm) in left eyes (Lx). The mean value of the y coordinate was 0.24 G 0.23 mm (range 0.82 to 0.40 mm) in right eyes (Ry) and 0.30 G 0.28 mm (1.06 to 0.74 mm) in left eyes (Ly). Therefore, the position of the thinnest point (r2 Z 0.68 and r2 Z 0.47 for x coordinate and y coordinate, respectively) was not as highly correlated between eyes as the pachymetric value (r2 Z 0.97). The location (x and y coordinates) of the thinnest points in right eyes and in left eyes was statistically significantly different from the location of the center of the cornea (0, 0) (P!.001; 1-sample t test with test value of zero).

Symmetry Table 1 shows the transformations along the direct symmetry model (Figure 5, A), the vertical midline (Figure 5, B), the horizontal midline (Figure 5, C), and the across-the-equivalence diagonal (y Z x) (Figure 5, D). The distance between the right-eye coordinates and the transformed left-eye coordinates was significantly lower for the reflection along the y-axis (vertical mirror symmetry) than the original position (direct symmetry) and the other 2 transformations along the x-axis and along the y Z x (analysis of variance with Tukey HSD, Table 1). Therefore, the location of the thinnest points in right eyes and in left eyes tended to have symmetry along the vertical midline. Normal Range of Symmetry of Linear and Angular Distances The finding that there was symmetry along x Z 0 helped establish the normal range of the minimum linear and angular distances between the locations’ 2 corresponding MCT points. This analysis used the original right-eye coordinates (Rx, Ry) and transformed left-eye coordinates (Lx0 , Ly), where Lx0 Z Lx  (1). The mean scalar (linear) distance was 0.25 G 0.17 mm (range 0.1 to 0.79 mm) (Figure 6). The mean angular distance between the points of MCT was 20.54 G 17.6 degrees (range 0.06 to 74.2 degrees). DISCUSSION

Distance of Minimum Corneal Thickness from Center The mean distance between the MCT and the center of the cornea was 0.63 G 0.13 mm (range 0.46 to 0.98 mm) in right eyes and 0.66 G 0.17 mm (range 0.38 to 1.11 mm) in left eyes. The mean difference in the distance between right eyes and left eyes was 0.03 G 0.08 mm (P!.001, paired t test). There was a good linear correlation between the 2 eyes (r Z 0.87, P!.001).

Accurate noncontact analysis of corneal structure has been difficult. Previous studies have evaluated scanning-slit, rotating Scheimpflug imaging, and time-domain OCT platforms for such analysis. In a recent study,23 we found that repeated Fourier-domain OCT corneal pachymetry measurements were highly consistent and, in contrast to time-domain OCT, did not seem to underestimate normal corneal thickness. The variability in MCT and CCT measurements has been a recent area of interest. Ru¨fer et al.29 used

Table 1. (continued)

Change in Coordinates of L

Mean Lx0 G (SD)

Mean Ly0 G (SD)

Mean Distance (mm) Between R(x,y) and L(x0 ,y0 )

Difference from Smallest Distance (II) (mm)

P Value*

L(x,y) / L(x, y) L(x,y) / L(x, y) L(x,y) / L(x, y) L(x,y) /L(x, y)

0.51 G 0.28 0.51 G 0.28 0.51 G 0.28 0.51 G 0.28

0.21 G 0.33 0.21 G 0.33 0.21 G 0.33 0.21 G 0.33

1.07 G 0.44 0.25 G 0.17 1.32 G 0.30 0.65 G 0.39

0.81 0.00 1.06 0.40

.001 d .001 .001

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Figure 5. Assessment of symmetry in MCT location between right eyes and left eyes. The points are mapped on a Cartesian grid with the center of the cornea being origin (0,0). The original coordinates on Fourier-domain OCT output are R(x, y) for right eyes and L(x, y) for left eyes. These points are assessed for symmetry by reflecting points along the axis by inverting the sign of Lx, Ly, or both; Lx0 Z 1  Lx and Ly0 Z 1  Ly. A: Direct symmetry, no transformation. B: Vertical midline, Lx / Lx0 . C: Horizontal midline, Ly / Ly0 . D: Along diagonal y Z x, Lx, y / Lx0 , Ly0 .

scanning-slit measurements and found that the MCT and the CCT were significantly different in right eyes and in left eyes. The mean location of the thinnest point in their study was 0.56 G 0.4 mm in right eyes and 0.69 G 0.4 mm in left eyes. The location was slightly more central than previously reported by Liu et al.30 (0.90 G 0.51 mm) using scanning-slit measurements of normal cornea. Ashwin et al.31 used rotating Scheimpflug imaging to map the thinnest point. They found the MCT was 5.57 mm thinner than the CCT. The mean distance of the thinnest point from the corneal apex was 0.62 mm in right eyes and 0.79 mm in left eyes. In a study using very-high-frequency digital ultrasound, the mean absolute stromal thickness progression from the thinnest point was governed by a quadratic equation and was independent of stromal thickness at the thinnest point.32 Our finding of a difference of approximately 5 mm in CCT and MCT tends to corroborate better with the Scheimpflug findings of Ashwin et al.31 than with

the scanning-slit studies. In addition, the location of the MCT point was more similar to that of Ashwin et al.31 and of Liu et al.30 There are many likely reasons for the differences in observations between OCT, scanning-slit, and Scheimpflug imaging platforms; they include variations in algorithms, imaging resolution, scan center, optical axis, and acquisition speed between platforms. Therefore, we recommend against extrapolating the results of one platform to another, especially during a serial follow-up of a patient. In this study, we have also evaluated the relationship between the difference in CCT and the difference in MCT and detailed the mapping of the thinnest point in terms of the scalar distance of the point from the center and the distance between the geometrically transformed thinnest points (linear and angular). The strongest predictor of a difference in MCT was a difference in CCT between 2 eyes, suggesting that normal eyes have a similarly governed architecture that

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A study with a population that includes eyes with keratoconus, forme fruste keratoconus, high myopia, and hyperopia is underway and should provide further information in this area. REFERENCES

Figure 6. Diagram of a superimposed image of fellow-eye pachymetric output showing different entities used to map the thinnest point. Terms: R(x, y) and L(x, y) Z original locations; L(x0 ,y) Z reflection of L along vertical midline; q Z angle between the 2 points with the center of the cornea as the vertex; S Z scalar distance between the 2 points; DR and DL Z the distance of the locations of the points of MCT from the central cornea for right eyes and left eyes. The difference is seen as an annular zone denoted by the circles drawn with dashed lines.

determines CCT and MCT. It will be interesting to determine whether such a relationship is disturbed in corneas with pathology. Using time-domain OCT, Li et al.14 found that a pachymetry-based diagnostic criteria of keratoconus may be as sensitive and specific as the topography-based KISA% index. Mirror symmetry that is not superimposable has been reported in refractive entities such as astigmatism axis and HOAs.1–5 We found that the location of thinnest cornea had best symmetry along the vertical midline. The relationship between the angle k, HOAs, the thinnest point, and the center of the corneal dome should be studied further. As of now, OCT platforms do not measure the angle k, and a similar study should be performed with a single, fast instrument operating at high acquisition speeds to compensate for movement errors. The current study provides normative data for MCT as well as its location in relation to the central corneal area with Fourier-domain OCT, a high-speed acquisition system. The use of Fourier-domain OCT ensured that the motion artifact was reduced to a minimum. The study confirmed that the CCT and MCT are not interchangeable and that both should be considered separately when evaluating eyes for corneal disease and surgical planning. The ranges in the normal variations in the thinnest point of the cornea in normal eyes can serve as useful parameters for ruling out pathology.

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OTHER CITED MATERIAL A. Optovue, Inc. RTVue Overview. Available at: http://www. optovue.com/products/rtvue. Accessed April 7, 2010

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First author: Gaurav Prakash, MD Tertiary care ophthalmic hospital, Chennai, India