Central and peripheral corneal thickness measured with optical coherence tomography, Scheimpflug imaging, and ultrasound pachymetry in normal, keratoconus-suspect, and post–laser in situ keratomileusis eyes

ARTICLE

Central and peripheral corneal thickness measured with optical coherence tomography, Scheimpflug imaging, and ultrasound pachymetry in normal, keratoconus-suspect, and post–laser in situ keratomileusis eyes Claudia Maria Prospero Ponce, MD, Karolinne Maia Rocha, MD, PhD, Scott D. Smith, MD, MPH, Ronald R. Krueger, MD, MSE

PURPOSE: To compare central (CCT) and peripheral corneal thickness (PCT) using Scheimpflug imaging (Pentacam), high-speed optical coherence tomography (Visante OCT), and ultrasound (US) pachymetry (Sonogage Corneo-Gage Plus) in normal, keratoconus-suspect, and post–laser in situ keratomileusis (LASIK) eyes. SETTING: Department of Refractive Surgery, Cole Eye Institute, Cleveland Clinic, Cleveland, Ohio, USA. METHODS: The CCT and PCT were retrospectively measured using US pachymetry, Scheimpflug imaging, and high-speed OCT from January 2006 to March 2008. The influence of age and absolute magnitude of corneal thickness were also analyzed. Analysis was by multivariate generalized estimating equations, multivariate linear regression, and linear regression plots. RESULTS: One hundred sixty-three eyes were analyzed. Ultrasound pachymetry CCT measurements were consistently higher than Scheimpflug and OCT measurements (mean difference 6.5 mm G 1.8 [SD] and 7.5 G 1.4 mm, respectively) (both P<.0005) in normal eyes; the difference was statistically similar and not greater with keratoconus suspicion, age, or absolute magnitude of corneal thickness (P>.05). Scheimpflug measurements were significantly lower than US pachymetry in post-LASIK eyes (P<.0005). There was no statistically significant difference (mean 0.9 G 1.4 mm) in Scheimpflug and OCT CCT measurements (P>.5), although Scheimpflug measurements were significantly lower in post-LASIK eyes (P<.0005). Scheimpflug PCT measurements were higher than OCT measurements, showing more agreement with increasing age (P Z .017). CONCLUSIONS: Scheimpflug and OCT CCT measurements were reproducible but always thinner than US pachymetry in normal and keratoconus-suspect eyes. In post-LASIK eyes, OCT pachymetry maps were more accurate than Scheimpflug maps. The influence of age on PCT requires further study. J Cataract Refract Surg 2009; 35:1055–1062 Q 2009 ASCRS and ESCRS

Anterior segment imaging has gone through several advances in the past decade. New imaging devices now provide accurate measurements of corneal power, corneal elevation, iridocorneal angle, anterior segment biometry, corneal wavefront, and corneal pachymetry.1 The latter is essential in refractive surgery in evaluating eyes suspected of having ectasia and in determining the residual stromal bed in candidates for retreatment.2,3 Ultrasound (US) pachymetry has been described to be more precise than optical pachymetry and is Q 2009 ASCRS and ESCRS Published by Elsevier Inc.

currently considered the gold standard for measuring central corneal thickness (CCT). Moreover, the pachymetry maps of Pentacam Scheimpflug imaging (Oculus Inc.) and Visante anterior segment high-speed optical coherence tomography (OCT) (Carl Zeiss Meditec Inc.) have been shown to be comparable to US pachymetry maps.3,4 Both systems also overcome some disadvantages of ultrasound such as in-fluid immersion requirements (US biomicroscopy),1 uncontrolled gaze, probe placement error, and sound transmission variability due to dryness.3,4 0886-3350/09/$dsee front matter doi:10.1016/j.jcrs.2009.01.022

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The Pentacam device uses a rotating Scheimpflug camera. The camera creates an image by intersecting the eye plane with a slit beam, collecting 50 slit images in fewer than 2 seconds.1 Any movement of the eye is captured by another camera that controls centration and adjusts the measurements. The Scheimpflug system determines net corneal power,5 elevation maps, anterior chamber depth, and corneal wavefront.1 It is also an excellent way to detect keratoconus, both form fruste and suspect, by calculating the cornealthickness spatial profile and volume distribution.6 Optical coherence tomography, which was initially introduced for tomographic imaging of the retina,7 was recently improved for anterior segment applications with higher wavelength imaging and less image acquisition time (0.125 seconds).8 The OCT device captures the reflection of light to create a cross-sectional image in 8 meridians (128 sectional maps)9 using the same principles of reflection as for US pachymetry. Notable advantages over other imaging techniques include noncontact application, accuracy in the presence of corneal opacity, ease of use, and high-resolution profile imaging.1 In consecutive studies, the OCT pachymetry map was also shown to be comparable to US pachymetry.9,10 The aim of this study was to compare CCT and peripheral corneal thickness (PCT) using a Scheimpflug system, high-speed OCT, and US pachymetry in normal and keratoconus-suspect eyes and in eyes that have had laser in situ keratomileusis (LASIK). This is the first study comparing central pachymetry between the 3 systems in these 3 groups of eyes and to our knowledge, is the first comparison of PCT maps using the Scheimpflug and high-speed OCT systems.

Submitted: October 2, 2008. Final revision submitted: January 16, 2009. Accepted: January 20, 2009. From TEC de Monterrey (Prospero Ponce), School of Medicine, Monterrey, Mexico; the Cole Eye Institute (Prospero Ponce, Rocha, Smith, Krueger), Cleveland Clinic, Cleveland, Ohio, USA; and the Federal University of Sa˜o Paulo (Rocha), Sa˜o Paulo, Brazil. No author has a financial or proprietary interest in any material or method mentioned. Supported by a challenge grant to the Department of Ophthalmology, Cleveland Clinic Lerner College of Medicine, from Research to Prevent Blindness, New York, New York, USA. Corresponding author: Claudia Maria Prospero Ponce, MD, Cole Eye Institute, Cleveland Clinic, 9500 Euclid Avenue, Suite A31, Cleveland, Ohio 44195, USA. E-mail: [email protected].

PATIENTS AND METHODS This retrospective study analyzed the CCT and PCT in candidates for refractive surgery and patients evaluated after LASIK from January 2006 to March 2008. There were no age or sex restrictions. The protocol was in compliance with the Declaration of Helsinki. Three groups of eyes were analyzed: keratoconus suspect, those with previous LASIK, and normal (unoperated without corneal disease or topographic irregularity). The diagnosis of keratoconus suspect was based on the RabinowitzMcDonnell test and PathFinder II corneal analysis software for the Atlas corneal topography system (model 9000, Carl Zeiss Meditec). The software incorporates 3-dimensional mean curvature analysis. A vector machine algorithm analyzes multiple parameters from the mean curvature map and compares them with the software’s clinical database. The relationship between age and corneal thickness was evaluated in all 3 groups. The eyes were also grouped by thin corneas (!500 mm), normal corneas (501 to 550 mm), or thick corneas (O551 mm) based on the US pachymetry values.

Measurement Technique The CCT and PCT measurements were performed using a Scheimpflug imaging system (Pentacam), high-speed OCT (Visante), and US pachymetry (Sonogage CorneoGage Plus, Sonogage Inc.). Data were collected at 0.0 mm and 6.0 mm with the Scheimpflug system and at 0.0 to 2.0 mm and 5.0 to 7.0 mm with high-speed OCT; a single value was obtained from US pachymetry. Ultrasound pachymetry was performed first. Each patient was assigned to 1 of 3 certified technicians in the clinic. After topical anesthetic drops (proparacaine 0.5%) were instilled, the US probe was placed directly in the center of the eye, creating a 90-degree angle. The final US pachymetry value was obtained from 1 measurement by 1 technician. The US pachymetry device takes multiple, rapid, and sequential readings during a single applanation of the probe. This gives a mean US pachymetry reading with a standard deviation (SD). The reading was accepted when the SD was less than 2.0 to 3.0 mm. After US pachymetry, the high-speed OCT and Scheimpflug imaging assessments were performed by the same physician (K.M.R.). For the high-speed OCT, the patient was seated, with the face placed in the device’s chin and forehead support. Two images where taken, and the image with better quality (lowest SD) was chosen. Scheimpflug system measurements were performed using the same process. Illumination of the room was carefully established with a soft light. Inclusion criteria required the capture of all 3 CCT measurements for comparison.

Statistical Analysis Multivariate generalized estimating equations were used to analyze the correlation between the 3 measurements; these equations accounted for correlation between 2 eyes obtained from the same patient. A P value less than 0.05 was considered statistically significant. The difference in mean CCT between devices was obtained for each patient group using multivariate linear regression. The difference in mean CCT was further analyzed within each corneal-thickness category to determine thickness-dependent changes. Analysis of the difference in mean PCT between high-speed

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OCT and Scheimpflug imaging was performed for each patient group and each thickness subgroup in a similar fashion. The Pearson coefficient (r) was used for correlations. Analysis was performed using the Stata statistical package (version 8.1, StataCorp LP). Linear regression plots were created with Statistical Package for the Social Sciences software (version 15.0, SPSS, Inc.).

RESULTS This study evaluated 163 eyes of 83 patients; 53 were women. The mean age was 39 years (range 22 to 66 years). The mean spherical equivalent and keratometric reading, respectively, were 4.17 diopters (D) G 3.03 (SD) and 44.63 G 1.31 D in the normal group (n Z 103 eyes), 4.09 G 3.75 D and 46.04 G 2.60 D in the keratoconus-suspect group (n Z 40 eyes), and 0.78 G 2.29 D and 42.2 G 2.40 D in the post-LASIK group (n Z 17 eyes). Table 1 shows the mean CCT and PCT measurements by group. The mean difference between US pachymetry and Scheimpflug imaging CCT measurements in the normal group was 6.5 G 1.8 mm; the difference was statistically significant (P!.0005). The mean difference was statistically similar in the keratoconussuspect group (P Z .224). In the post-LASIK group, the difference between devices was approximately 25.0 mm (P!.0005). The mean difference in CCT measurements between US pachymetry and high-speed OCT was 7.5 G 1.4 mm in the normal group, which was statistically significant (P!.0005); the difference was not statistically increased in the keratoconus-suspect or post-LASIK group (P Z .190 and P Z .575, respectively). The mean difference in CCT measurements between Scheimpflug imaging and high-speed OCT was not statistically significant in the normal group (P Z .52) or keratoconus-suspect group (P Z .935). However, in the post-LASIK group, Scheimpflug imaging gave lower measurements than high-speed OCT that were statistically significantly different (mean 15.6 G 3.7 mm) from measurements in normal eyes (P!.0005). Peripheral corneal thickness measurements were statistically significantly higher with the Scheimpflug system than with high-speed OCT in the normal group (mean difference 33.4 G 2.7 mm) (P!.0005). The difference was similar whether the patient had keratoconus or LASIK surgery. (P Z .812 and P Z .530, respectively) (Figure 4). With increasing age, however, the difference in PCT between Scheimpflug imaging and high-speed OCT was less, with a 4.3 mm change for every 10 years of increasing age (P Z .017). Absolute corneal thickness did not affect the difference between means in any group (PO.05) (Table 1). In all 3 groups, there was a strong positive correlation between US pachymetry, Scheimpflug imaging,

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Table 1. Mean CCT and PCT values by group. Group Parameter Mean CCT (mm) GSD US pachymetry Scheimpflug imaging High-speed OCT Mean PCT (mm) GSD Scheimpflug imaging High-speed OCT

Normal

Keratoconus Post-LASIK

523.0 G 28.0 523.0 G 41.6 526.1 G 66.7 516.3 G 31.6 513.6 G 44.0 501.7 G 73.7 515.4 G 29.2 512.7 G 42.3 516.4 G 66.1 597.4 G 34.2 609.0 G 42.8 628.8 G 46.9 564.3 G 34.8 575.1 G 45.3 600.0 G 49.8

CCT Z central corneal thickness; LASIK Z laser in situ keratomileusis; OCT Z optical coherence tomography; PCT Z peripheral corneal thickness; US Z ultrasound

and high-speed OCT in CCT and PCT measurements (Figures 1 to 4). However, in PCT measurements, the correlation between Scheimpflug imaging and highspeed OCT showed a weak positive association in the post-LASIK group (Figure 4). Figures 1 to 4 give the r values to indicate correlations between 2 measurement devices. A positive correlation is evidence of a general tendency toward large values of the first measurement to be associated with large values of the second measurement; the same is true for low values. An r value between 0.7 and 0.9 implies a strong association. DISCUSSION Highly specialized imaging devices are essential in the ocular diagnosis and treatment of patients, especially when screening them for refractive surgery. Because corneal pachymetry gives important information on the magnitude and profile of central and peripheral corneal thinning, we sought to assess the agreement in pachymetry measurements using 3 measurement devices. The high-speed OCT system we used expands on first-generation OCT for retinal imaging by achieving greater resolution with a longer wavelength (1310 nm versus 820 nm).8 The device acquires pachymetry maps along with other readings (angle visualization, angle estimation) with an optical axial resolution of 18 mm.1 After the device emits a low-coherence luminescent light, the distance and time of light scattering are obtained from the interference signal between 2 biological tissues, allowing 2-dimensional imaging.11,12 The image-acquisition system provides a video image of the examined zone and stores the last 7 images at a rate of 8 frames per second. At the end of the examination,

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Figure 1. Scatterplots of CCT comparisons in normal eyes. A: Ultrasound pachymetry versus Scheimpflug imaging (r Z 0.89). B: Ultrasound pachymetry versus high-speed OCT (r Z 0.93). C: Scheimpflug imaging versus high-speed OCT (r Z 0.93) (CCT Z central corneal thickness; OCT Z optical coherence tomography; US Z ultrasound).

the software interprets the selected image and provides pachymetry information.13 In previous studies, OCT showed high repeatability in central14 and peripheral corneal9 measurements; however, when compared with US pachymetry, it underestimated CCT.4,13,15 With the OCT system we used, Ho et al.15 found the pachymetry was a mean of 11.64 G 12.87 mm lower than with US pachymetry in post-LASIK eyes (P!.01). However, Li et al.9 found the opposite, with mean values of 513.7 G 44.5 mm for OCT and 498 G 46.6 mm for US pachymetry. In our study, we found a mean reduction in pachymetry measurements with OCT of 7.5 G 1.4 mm, with no statistical variation in keratoconus-suspect or post-LASIK eyes (PO.0005). Theories that might explain our results are that higher US pachymetry values can be obtained due to corneal edema produced by anesthetic drops13 and that more accurate OCT pachymetry values might be acquired as a result of improved centration and

perpendicularity.9,13 However, some authors9,13,15 suggest that tear-film displacement by US pachymetry may lead to lower pachymetry values than those obtained by OCT, Scheimpflug imaging, or slit-scanning topography. Finally, OCT may be superior to other tomographic devices, such as Orbscan II (Bausch & Lomb), because it obtains corneal-thickness profiles in less time and is not influenced by stromal reflections or haze.9,13,15 Real-time ocular coherence pachymetry has also been used intraoperatively with good reliability, making it a versatile and promising imaging technique.16 In a study by Kim et al.,3 Scheimpflug imaging gave corneal thickness measurements that were approximately 10 mm lower than US pachymetry measurements; the difference between methods was similar before and after photorefractive keratectomy. Other studies have reported similar results in post-LASIK eyes17 and normal eyes.18,19 In our study, the mean

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Figure 2. Scatterplots of CCT comparisons in keratoconus-suspect eyes. A: Ultrasound pachymetry versus Scheimpflug imaging (r Z 0.91). B: Ultrasound pachymetry versus high-speed OCT (r Z 0.95). C: Scheimpflug imaging versus high-speed OCT (r Z 0.95) (CCT Z central corneal thickness; OCT Z optical coherence tomography; US Z ultrasound).

reduction in CCT with Scheimpflug imaging was 6.5 G 1.8 mm in normal eyes (PO.0005), which is similar to results (6.09 mm) in a study by Barkana et al.20 However, in our post-LASIK patients, Scheimpflug pachymetry measurements were even lower than US pachymetry and high-speed OCT measurements. Although the reason for the lower Scheimpflug CCT values in post-LASIK eyes is not known, the finding shows the importance of having multiple devices for testing the corneal thickness profile in suspicious eyes. Although many factors can affect its measurements, the Scheimpflug imaging system we used has otherwise been shown to have high repeatability and reproducibility in CCT measurements.1,5,15 The Scheimpflug camera captures approximately 50 slit images with 500 true elevation points per slit. Proper focus during capture is obtained because the camera automatically takes the image when alignment is achieved.20 Although the presence of dry eye after LASIK can affect

corneal pachymetry,9 the tear film does not tend to distort corneal imaging and measurements with the Scheimpflug system.20 The Scheimpflug system estimates pachymetry by gathering single points from each slit and establishing anterior and posterior surface curvatures. These surface curvatures can be displayed as anterior and posterior elevation maps, which also have value in the preoperative screening process. The system is useful in the diagnosis of subclinical keratoconus because it can measure the corneal-thickness spatial profile and volume distribution.6 Because both the Scheimpflug imaging and highspeed OCT systems we used can accurately calculate CCT and PCT in keratoconic eyes, they are valuable for diagnosing suspect or subclinical keratoconus because of the difference between the central and the conus-shaped (thinnest) portion of the cornea.21 Thus, a global form of thickness-profile imaging

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Figure 3. Scatterplots of CCT comparisons in post-LASIK eyes. A: Ultrasound pachymetry versus Scheimpflug imaging (r Z 0.91). B: Ultrasound pachymetry versus high-speed OCT (r Z 0.94). C: Scheimpflug imaging versus high-speed OCT (r Z 0.95) (CCT Z central corneal thickness; OCT Z optical coherence tomography; US Z ultrasound).

must be used in addition to US pachymetry when screening patients with thin or suspicious corneas. Sometimes the absolute magnitude of corneal thickness can influence mean pachymetry values.3,11,13 The Orbscan II topographer has been reported to both underestimate (acoustic equivalent factor 0.94)3 and overestimate (acoustic equivalent factor 0.89)15 CCT in thinner corneas. Although the overestimation was theorized to be due to the US pachymetry probe pressure on the corneal surface in thinner corneas,13 the influence of thick and normal corneas has not been reported. In our study, we found that the Scheimpflug imaging and high-speed OCT measurements were not influenced by the absolute magnitude of CCT. With regard to PCT, Scheimpflug imaging gave a value that was approximately 30 mm greater than the high-speed OCT measurement. In the Scheimpflug system, the 6.0 mm value is the mean value of all points within a segment of the circumference of a 6.0 mm

diameter centered circle. With the high-speed OCT system, the corresponding peripheral thickness value represents the mean of all points within 1 of 8 pieshaped wedges and ranges from 5.0 to 7.0 mm. Therefore, the OCT device gathers information about PCT within a specific area while the Scheimpflug system presents the mean value along the line segment of a specific diameter. Studies have shown that the Visante OCT device underestimates the paracentral corneal thickness measurements relative to those obtained with Orbscan II.13 However, a large variation in PCT values has been reported with the Orbscan II topographer and the Topcon specular microscope.22 Orbscan II, Pentacam, and anterior segment OCT pachymetry values show less correlation in the peripheral cornea than centrally. With Visante OCT, the measurements were shown to be reliable less than 7.0 mm from the corneal center.18 Even though no general

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Figure 4. Peripheral corneal thickness correlation between Scheimpflug imaging and high-speed OCT. A: Keratoconus-suspect eyes (r Z .78). B: Normal eyes (r Z .85). C: Post-LASIK eyes (r Z .66) (OCT Z optical coherence tomography; PCT Z peripheral corneal thickness).

agreement was found between the OCT and Scheimpflug peripheral pachymetry maps, we found the peripheral pachymetry to be similar in older patients. This might be because the peripheral cornea is typically asymmetric, with the nasal and superior quadrants being thicker.22–24 In older patients, however, the peripheral cornea might become more symmetric with decreasing nasal and superior quadrant thickness.23 Although this change might not be perceived by the narrow circular line of peripheral thickness (Scheimpflug), it is averaged within only 8 broader areas in the peripheral cornea (OCT). The greater symmetry of the OCT measurement with increasing age is thus more easily perceived and shows greater agreement between devices. Khoramnia et al.24 found that age was not specifically related to pachymetry changes or the reliability of Scheimpflug imaging. In summary, the 2 relatively new tomographic imaging devices we evaluated serve to complement, not replace, the value of US pachymetry in the preoperative refractive surgery evaluation. They also

contribute specifically to keratoconus diagnosis, lens evaluation, glaucoma screening, and other emerging areas of research. Eyecare providers should become familiar with the differences in CCT measurement when using the 3 devices we studied and not use them interchangeably when establishing and meeting criteria for treatment in the preoperative evaluation. Although the Pentacam and Visante OCT instruments might be equally used for central pachymetry preoperatively, OCT may be preferable in post-LASIK eyes because the Scheimpflug pachymetry maps tend to show excessive thinning. Both of the 2 new devices have a high cost but provide benefits in patient care and integral evaluation. More studies are needed to establish the influence of age on peripheral pachymetry.

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Fitrt author: Claudia Maria Prospero Ponce, MD School of Medicine, Monterrey, Mexico, and Cole Eye Institute, Cleveland Clinic, Cleveland, Ohio, USA