Seminars in Ophthalmology, Early Online, 1–7, 2013 ! Informa Healthcare USA, Inc. ISSN: 0882-0538 print / 1744-5205 online DOI: 10.3109/08820538.2013.833264
ORIGINAL ARTICLE
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Comparison of Central Corneal Thickness Measurements with a Rotating Scheimpflug Camera, a Specular Microscope, Optical Low-Coherence Reflectometry, and Ultrasound Pachymetry in Keratoconic Eyes Yasin Cinar1, Abdullah Kursat Cingu1, Fatih Mehmet Turkcu1, Tuba Cinar2, Alparslan Sahin1, Harun Yuksel1, and Seyhmus Ari1 1
Department of Ophthalmology, Faculty of Medicine, Dicle University, Diyarbakir, Turkey and 2 Diyarbakir Children Hospital, Ophthalmology Clinic, Diyarbakir, Turkey
ABSTRACT Objective: To compare central corneal thickness (CCT) measurements with a rotating Scheimpflug camera (RSC), noncontact specular microscopy (SM), optical low-coherence reflectometry (OLCR), and ultrasonic pachymetry (UP) in keratoconus (KC) patients. Method: In this prospective study, four CCT measurements taken with an RSC, SM, OLCR, and UP were compared in 81 eyes of 44 consecutive KC patients. The KC patients were divided into four subgroups according to Amsler-Krumeich’s KC classification. Results: The RSC and UP measurements of the CCT were not statistically significant in all the groups. Comparison of the SM vs. the OLCR measurements yielded statistically significant differences in all the KC patients and in all KC stages. In all the KC patients, RSC and OLCR showed a high correlation coefficient factor (r = 0.87, p = 0.000). Conclusion: CCT measurements with RSC are comparable to those achieved with UP. Compared with the other devices, according to SM measurements, the central cornea is thicker in all keratoconic eyes and in all KC grades, and it is thinner according to OLCR. RSC, UP, SM, and OLCR should not be used interchangeably in keratoconic eyes. Keywords: Central corneal thickness, keratoconus, pachymetry, scheimpflug camera, reflectometry
INTRODUCTION
Various techniques are available to measure the central corneal thickness (CCT), including ultrasonic pachymetry (UP), optical pachymetry,1 ultrasound biomicroscopy,2 slit scanning corneal topography,3–4 optical coherence tomography (OCT),5 confocal microscopy,6 optical low-coherence reflectometry (OLCR),7 contact or noncontact specular microscopy (SM),8 and dual-beam partial coherence interferometry.9 UP measures corneal thickness using the reflection of sound waves, whereas SM and OLCR utilize light reflection. OLCR measurements provide CCT, details on the axial length, and keratometric readings. SM provides information on the endothelium and CCT.
Keratoconus (KC) is a bilateral noninflammatory disorder characterized by progressive corneal thinning and steepening that results in induced myopia and astigmatism. The diagnosis of KC in patients with classical biomicroscopic findings or retinoscopic signs is not difficult. However, it is challenging in early KC or subclinical KC patients with good visual acuity and delicate signs on examination. In progressive KC, early detection of corneal thinning might be important for patients who could be considered for collagen crosslinking treatment or intracorneal ring segment implantation.
Received 12 April 2013; accepted 26 July 2013; published online 19 September 2013 ¨ niversitesi Tip Fakultesi, Goz Hastaliklari A.D.,21280 Kampus, Diyarbakir, Turkey. E-mail: Correspondence: Yasin Cinar, Dicle U [email protected]
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The rotating Scheimpflug camera (RSC) system yields information on the anterior and posterior corneal topography, corneal volume, corneal pachymetry, and anterior chamber depth. The most widely used method of measuring corneal thickness is UP, which is considered to be the gold standard because of its ease of use, portability, and cost-effectiveness.10–11 As UP is a contact method, topical anesthesia is required. Touching the cornea during the procedure may cause patients discomfort and lead to epithelial erosion and the transmission of infections.12 Indentation of the cornea13 or tear film displacement by the probe14 may produce inaccurate (thinner) measurements. Inappropriate probe placement and tissue hydration may cause observer bias. Thus, UP measurements require some experience.9,15 Many comparisons of different pachymetric techniques have been performed in healthy corneas,5,13,16 and there are few studies of keratoconic eyes.17–19 In this prospective study, we aimed to compare CCT measurements using RSC and SM, OLCR, and UP in keratoconic eyes.
MATERIALS AND METHOD Eighty-one eyes of 44 consecutive patients (24 female and 20 male) previously diagnosed as KC were included in the study. Patients with KC with a clear central cornea were included in the study. The exclusion criteria were as follows: use of contact lens, corneal scarring, previous ocular surgery (e.g., cataract, pterygium, corneal collagen crosslinking, intracorneal ring segment implantation), systemic connective tissue disease, atopy, and dry eye syndrome. Informed consent was obtained from all the patients in accordance with the Declaration of Helsinki before any intervention was performed, and the local ethics committee approved this study. If the patient was under 18 years, a consent form was also obtained from his/her parents. A complete ophthalmic examination was performed, including uncorrected and best corrected visual acuity, refraction for best corrected visual acuity, KC classification, and slit lamp biomicroscopy. A KC diagnosis was made if there was a scissor reflex on retinoscopy and central or paracentral steepening of the cornea on corneal topography with one of the following biomicroscopic findings: central or paracentral steepening, hemosiderin deposition, Vogt’s stria, apical scarring, or breaks in the Descement’s membrane. The eyes were classified into four groups according to the Amsler–Krumeich KC classification,20 which is based on biomicroscopic findings, keratometric readings, pachymetry at the thinnest area of the cornea, and refraction. The corneal thickness measurements were performed in the order of RSC (Pentacam HR, Oculus,
Germany), SM (Konan Noncon Robo specular microscope, Konan Medical Inc., Hyogo, Japan), OLCR (LenStar LS 900, Haag-Streit AG, Koeniz, Switzerland), and UP (US 4000, Nidek, Japan) by the same investigator on the same day. If the patients moved their eyes or blinked, the measurement was repeated to standardize the examinations. For each subject, the pachymetric measurements were performed on the same day, with a 10 min interval between the measurements with the four devices. During the measurement with the RSC, the patients were seated and asked to place their chin on a chinrest, with their forehead touching the headband. The patients were then instructed to look at the black spot in the middle of the blue fixation lamp. On the monitor, the investigator evaluated the position of the image of the eye and then focused the image. The image was then centralized in the aiming circle on the monitor. To eliminate operator-dependent variables, the automatic release mode was used. Three successive measurements of both eyes of the patients were taken over the course of a few minutes. Inappropriate measurements were indicated by a red color on the monitor and were deleted, as recommended by the manufacturer. The average of three pachymetric measurements of the center of the pupil was used for the study. For the SM, the patients were asked to look into the fixation target. The center of the cornea was adjusted by focusing on the center of the pupil on the screen until a clear image appeared on the monitor. When the alignment and focus were appropriate, the endothelial image and the CCT were measured automatically with the device. Three successive measurements were taken. The mean of these three measurements was used for statistical analysis. For the OLCR, the patients were seated and placed their chins on a chinrest with their foreheads on the headrest of the device and were asked to look at the fixation light. According to the manufacturer’s recommendations, both hands were used to adjust the position of the device (for better alignment, one hand was placed on the joystick and the other one on the cross slide), and the device was not moved between the measurements. Implausible measurements marked in a red color on the monitor were deleted, as recommended by the manufacturer. The software calculated the mean of five consecutive measurements. Three successive measurements were obtained for both eyes and the mean of these measurements was used for the analysis. The UP measurements were performed last because they require a contact method. After instillation of one drop of 0.5% proparacaine hydrochloride to the cornea for anesthesia, the patients were asked to look at a distant fixation point, and the UP probe was placed perpendicularly, touching the center of the cornea. Three consecutive measurements were Seminars in Ophthalmology
Central Corneal Thickness Measurements in Keratoconus performed for both eyes, and the mean of these measurements was used for the analysis.
were stage 4 KC). OLCR could not measure the CCT only in one eye, which was stage 2 KC.
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STATISTICAL ANALYSIS
Comparison of the Mean CCT Measurements
The Statistical Package for the Social Sciences statistical software, version 11.5 (SPSS Inc., Chicago, IL, USA) was used for the statistical analysis. To analyze the distribution of the data, a Kolmogorov-Smirnov test was performed. The data were distributed normally, and a paired t test was used to analyze the differences between the measurements of the devices. Pearson’s coefficient of correlation was used to express the strength of the relationship between the measurements of the devices. A p value less than 0.05 was considered significant.
The KC grades and the mean CCT measurements of all the patients obtained by the four devices are shown in Table 1. Table 1 also shows the p values of the binary comparisons of the four different methods used to measure the CCT. The CCT measurements obtained by the RSC and UP were not significantly different in any of the groups (Table 1). The SM vs. the OLCR measurements were significantly different in the whole cohort and also in every KC stage. There were significant differences between the CCT measurements of RSC vs. SM, RSC vs. OLCR, SM vs. OLCR, SM vs. UP, and OLCR vs. UP in the whole cohort. The RSC measures were, on average, 0.02 26.7 mm thinner than UP in all the KC patients. The CCT measurements with SM were significantly greater than those of the other devices in every stage of KC.
RESULTS Six patients had unilateral KC. One eye of a patient with facial nerve paralysis accompanying mild exposure keratopathy was excluded. The mean age of the patients was 19.0 5.33 years (range 10–32 years). The mean keratometric value (K) was 50.5 5.25 Diopter (D) according to the RSC. The mean manifest refraction spherical equivalent (MRSE) was 5.13 3.02 D. According to the Amsler-Krumeich classification, there were 25 stage 1, 35 stage 2, 13 stage 3, and eight stage 4 eyes. The mean MRSE was 3.2 1.7 D in stage 1, 4.6 1.8 D in stage 2, 7.3 2.0 D in stage 3, and 9.8 4.4 D in stage 4 KC. The CCT measurements could be performed in all the patients using RSC and UP, whereas SM could not measure the CCT in seven eyes of six patients (two eyes were stage 2, three eyes were stage 3, two eyes
Correlations between the Pachymetry Methods Table 2 represents the correlation coefficients (r values) and p values of Pearson’s correlation test, showing the agreements between the CCT measurements with RSC, SM, OLCR, and UP in the study. A scatter plot of the CCT measurements is shown in Figure 1. When all the patients were considered, the highest correlation coefficient was found between RSC and
TABLE 1. The mean CCT measurements of four instruments in the whole cohort and in the subgroups according to Amsler-Krumeich classification; at the bottom p values of CCT measurements among four devices in all patients and subgroups. RSC
UP
SM
OLCR
All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
458 45.6 478 43.6 468 30.6 441 29.0 379 39.5
458 46.5 480 40.2 465 27.8 440 38.5 389 69.2
474 38.9 487 49.6 468 22.7 456 33.3 474 58.4
448 44.6 473 36.1 457 23.2 429 24.8 357 38.7
*p Values All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
RSC vs UP 0.993 0.674 0.307 0.902 0.658
RSC vs SM 0.004 0.062 0.535 0.025 0.078
RSC vs OLCR 50.001 0.274 50.001 0.018 0.277
SM vs OLCR 50.001 0.013 0.001 0.018 0.010
SM vs UP 0.009 0.106 0.394 0.183 0.087
OLCR vs UP 0.002 0.126 0.005 0.167 0.273
UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera; CCT: Central Corneal Thickness; KC: Keratoconus. p50.05 considered as significant; *paired t test. !
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TABLE 2. Degree correlation between the CCT measurements of the devices. RSC vs UP þ
All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
RSC vs SM
RSC vs OLCR
SM vs OLCR
SM vs UP
OLCR vs UP
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
0.83 0.9 0.83 0.68 0.46
50.001 50.001 50.001 0.011 0.251
0.59 0.87 0.6 0.8 0.62
50.001 50.001 50.001 0.005 0.263
0.87 0.88 0.88 0.85 0.1
50.001 50.001 50.001 50.001 0.798
0.59 0.86 0.63 0.57 0.42
50.001 50.001 50.001 0.083 0.483
0.44 0.89 0.49 0.68 0.89
50.001 50.001 0.004 0.03 0.044
0.79 0.87 0.8 0.75 0.1
50.001 50.001 50.001 0.003 0.814
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UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera; KC: Keratoconus; CCT: Central Corneal Thickness. þPearsons correlation coefficient; *paired t test. p50.05 considered as significant.
OLCR (r = 0.87, p5.001). In the grade 1 KC group, there were high correlations between each binary comparison of the four different methods, particularly with RSC and UP (r = 0.9, p50.001). RSC vs. OLCR had the highest correlation coefficient in grade 2 KC (r = 0.88, p50.001) and grade 3 KC (r = 0.85, p50.001) patients. In the grade 4 KC group, UP vs. SM had a significant negative correlation coefficient (r = 0.89, p = 0.044) (Table 2).
DISCUSSION The measurement of the CCT is crucial in the diagnosis, follow-up, and treatment of KC. In the corneal collagen crosslinking procedure, the recommended corneal thickness is at least 400 mm to avoid damage to the corneal endothelium and deeper structures of the eye, such as the lens and the retina.21 In corneal intrastromal ring segment implantation, the thickness at the implanted site should not be less than 400 mm to prevent full thickness corneal incision or shallow placement of the ring segment.22 In recent years, new devices have been introduced to measure the CCT in a noncontact way. This study compared CCT measurements obtained by four different methods in keratoconic eyes: RSC, SM, OLCR, and UP. To the best of our knowledge, this is the first study to compare the use of these four devices to measure the CCT in KC patients. Uc¸akhan et al. reported a comparison of CCT with RSC, SM, and UP measurements in normal and keratoconic corneas.17 According to their results, RSC had better reproducibility than UP and SM in moderate keratoconic eyes. They found a very high correlation between the RSC and UP measurements in mild and severe KC, whereas SM was unable to measure the CCT in any of the eyes with severe KC and 42.9% of the eyes with moderate KC in their study population. They reported a correlation coefficient of 0.92 between the RSC and UP measurements in the keratoconic eyes. In the current study, the KC patients were staged according to the Amsler–Krumeich KC classification, and SM could not measure the CCT
only in seven eyes of six bilateral KC patients. Of these, two eyes were stage 2, three eyes were stage 3, and two eyes were stage 4 KC. In the present study, when we compared the UP and RSC measurements in all the keratoconic patients, the measurements were not statistically significant (p = 0.993), and there was a significant correlation (r = 0.83, p50.001). The measurements with UP were slightly thicker than those obtained with the RSC, a finding in agreement with some previous studies13,17,23 in which UP measured thicker than RSC. The thinnest pachymetry point measured by the RSC and the slit scan corneal topography showed no significant difference in mean deviation.19 However, Dutta et al. demonstrated that UP yielded significantly higher CCT values than slit scan corneal topography.18 This finding was attributed to the posterior reflection point of the sound waves of the UP not being identified. However, this point is supposed to be between Descement’s membrane and the anterior chamber.17 Furthermore, compression of the epithelium and displacement of a 7 to 40 mm thick tear film by the UP probe may underestimate CCT measurements.24–25 Some studies have reported that the agreement between OLCR and US pachymetry in CCT measurements is very good.12,26 Spadea et al. reported that a comparison of OLCR and US pachymetry in the measurement of the CCT before and after photorefractive keratectomy had a smaller effect on the agreement between the two devices. They also noted that these two devices could be used interchangeably in normal eyes and in the planning of refractive surgery.26 In the present study, the UP measurements were thicker than those obtained with OLCR, in agreement with a previous study.27 When all the KC patients were considered, the mean difference between the CCT measurements of these two devices was 10.5 mm. The mean difference between the UP and OLCR measurements was greater in grade 4 KC compared to grade 1 KC. The correlation coefficient between UP and OLCR was 0.79 (p50.001) in grade 1 KC and 0.1 (p = 0.814) in grade 4 KC. These two devices should not be used interchangeably in KC patients. Seminars in Ophthalmology
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Central Corneal Thickness Measurements in Keratoconus
FIGURE 1. (a) Scatterplot of CCT measurements taken by UP and RSC; (b) scatterplot of CCT measurements taken by RSC and SM; (c) scatterplot of CCT measurements taken by RSC and OLCR; (d) scatterplot of CCT measurements taken by SM and OLCR; (e) scatterplot of CCT measurements taken by UP and SM; (f) scatterplot of CCT measurements taken by UP and OLCR. UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera.
Ucakhan and associates17 reported that the mean differences between UP-SM, RSC-SM, and RSC-UP were 18.8 mm, 12.7 mm, and 11.2 mm, respectively, in keratoconic eyes. In the current study, the mean !
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differences between UP-SM, RSC-SM, and RSC-UP were 14.4 mm, 13 mm, and 0.02 mm, respectively. In contrast to the results of Ucakhan and associates, SM failed to measure the CCT in only two grade 4 KC
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eyes in the current study. This may be because the anterior corneal refractive power affects noncontact specular images.28 Tai et al.29 reported CCT measurements in healthy subjects using RSC, SM, OLCR, and UP. They found that the mean CCT differences between the methods in pairwise comparisons were statistically significant except for OLCR vs. UP and OLCR vs. RSC. They found the greatest mean difference (30.57 mm) among the comparisons between the RSC and SM. The smallest mean difference was 3.54 mm. This was found between OLCR and UP in the same study. In the current study, the greatest mean difference was between SM and OLCR (21.8 mm), and the smallest mean difference was between UP and RCS (0.02 mm) in the whole cohort. Barkana and associates13 reported that the RSC system and OLCR pachymeter are convenient and provide excellent intraoperator repeatability and reproducibility in CCT measurements in healthy subjects. They found CCT values achieved by the RSC were similar to those achieved with both the OLCR pachymeter and the US pachymeter. The correlation coefficient was 0.96 between the RSC and OLCR, according to their results. In the current study, the CCT measurements with the RSC and OLCR were close to each other, and the correlation coefficient was 0.87 between these two devices. However, it was not statistically significant in all the KC patients. The current study has some limitations, such as the lack of a healthy control group, the reliability and reproducibility analyses of the devices, and the small sample size of the study population. Nevertheless, this is the first study comparing CCT measurements of SM and OLCR in keratoconic eyes. The study found that SM and OLCR measurements of the CCT are significantly different in keratoconic eyes. In conclusion, CCT measurements with the RSC seem to be comparable to those achieved with UP. Compared with the other three devices, the CCT is thicker according to SM measures and thinner according to OLCR measures in all keratoconic eyes and in all KC grades. RSC, UP, SM, and OLCR should not be used interchangeably in keratoconic eyes.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
REFERENCES 1. Salz JJ, Azen SP, Berstein J, et al. Evaluation and comparison of sources of variability in the measurement of corneal thickness with ultrasonic and optical pachymeters. Ophthalmic Surg 1983;14:750–754.
2. Avitabile T, Marano F, Uva MG, Reibaldi A. Evaluation of central and peripheral corneal thickness with ultrasound biomicroscopy in normal and keratoconic eyes. Cornea 1997;16:639–644. 3. Yaylali V, Kaufman SC, Thompson HW. Corneal thickness measurements with the Orbscan Topography System and ultrasonic pachymetry. J Cataract Refract Surg 1997;23: 1345–1350. 4. Suzuki S, Oshika T, Oki K, et al. Corneal thickness measurements: Scanning-slit corneal topography and noncontact specular microscopy versus ultrasonic pachymetry. J Cataract Refract Surg 2003;29:1313–1318. 5. Bechmann M, Thiel MJ, Neubauer AS, et al. Central corneal thickness measurement with a retinal optical coherence tomography device versus standard ultrasonic pachymetry. Cornea 2001;20:50–54. 6. Li HF, Petroll WM, Moller-Pedersen T, et al. Epithelial and corneal thickness measurements by in vivo confocal microscopy through focusing (CMTF). Curr Eye Res 1997; 16:214–221. 7. Beutelspacher SC, Serbecic N, Scheuerle AF. Assessment of central corneal thickness using OCT, ultrasound, optical low coherence reflectometry and Scheimpflug pachymetry. Eur J Ophthalmol 2011;21:132–137. 8. Modis Jr. L,, Langenbucher A, Seitz B. Corneal thickness measurements with contact and noncontact specular microscopic and ultrasonic pachymetry. Am J Ophthalmol 2001;132:517–521. 9. Rainer G, Findl O, Petternel V, et al. Central corneal thickness measurements with partial coherence interferometry, ultrasound, and the Orbscan system. Ophthalmology 2004;111:875–879. 10. Marsich MW, Bullimore MA. The repeatability of corneal thickness measures. Cornea 2000;19:792–795. 11. Solomon OD. Corneal indentation during ultrasonic pachometry. Cornea 1999;18:214–215. 12. Koktekir BE, Gedik S, Bakbak B. Comparison of central corneal thickness measurements with optical low-coherence reflectometry and ultrasound pachymetry and reproducibility of both devices. Cornea 2012;31:1278–1281. 13. Barkana Y, Gerber Y, Elbaz U, et al. Central corneal thickness measurement with the Pentacam Scheimpflug system, optical low-coherence reflectometry pachymeter, and ultrasound pachymetry. J Cataract Refract Surg 2005;31: 1729–1735. 14. Chakrabarti HS, Craig JP, Brahma A, et al. Comparison of corneal thickness measurements using ultrasound and Orbscan slit-scanning topography in normal and postLASIK eyes. J Cataract Refract Surg 2001;27:1823–1828. 15. Wickham L, Edmunds B, Murdoch IE. Central corneal thickness: Will one measurement suffice? Ophthalmology 2005;112:225–228. 16. Amano S, Honda N, Amano Y, et al. Comparison of central corneal thickness measurements by rotating Scheimpflug camera, ultrasonic pachymetry, and scanning-slit corneal topography. Ophthalmology 2006;113:937–941. 17. Ucakhan OO, Ozkan M, Kanpolat A. Corneal thickness measurements in normal and keratoconic eyes: Pentacam comprehensive eye scanner versus noncontact specular microscopy and ultrasound pachymetry. J Cataract Refract Surg 2006;32:970–977. 18. Dutta D, Rao HL, Addepalli UK, Vaddavalli PK. Corneal thickness in keratoconus: Comparing optical, ultrasound, and optical coherence tomography pachymetry. Ophthalmology 2013;120(3):457–463. 19. Quisling S, Sjoberg S, Zimmerman B, et al. Comparison of Pentacam and Orbscan IIz on posterior curvature topography measurements in keratoconus eyes. Ophthalmology 2006;113:1629–1632. Seminars in Ophthalmology
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Central Corneal Thickness Measurements in Keratoconus 20. Krumeich JH, Daniel J, Knulle A. Live-epikeratophakia for keratoconus. J Cataract Refract Surg 1998;24:456–463. 21. Spoerl E, Mrochen M, Sliney D, et al. Safety of UVAriboflavin cross-linking of the cornea. Cornea 2007;26: 385–389. 22. Kubaloglu A, Sari ES, Cinar Y, et al. Comparison of mechanical and femtosecond laser tunnel creation for intrastromal corneal ring segment implantation in keratoconus: Prospective randomized clinical trial. J Cataract Refract Surg 2010;36:1556–1561. 23. Prospero Ponce CM, Rocha KM, Smith SD, Krueger RR. 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. J Cataract Refract Surg 2009;35:1055–1062. 24. Tam ES, Rootman DS. Comparison of central corneal thickness measurements by specular microscopy, ultrasound pachymetry, and ultrasound biomicroscopy. J Cataract Refract Surg 2003;29:1179–1184.
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25. Nissen J, Hjortdal JO, Ehlers N, et al. A clinical comparison of optical and ultrasonic pachometry. Acta Ophthalmol (Copenh) 1991;69:659–663. 26. Spadea L, Giammaria D, Di Genova L, Fiasca A. Comparison of optical low coherence reflectometry and ultrasound pachymetry in the measurement of central corneal thickness before and after photorefractive keratectomy. J Refract Surg 2007;23: 661–666. 27. Genth U, Mrochen M, Walti R, et al. Optical low coherence reflectometry for noncontact measurements of flap thickness during laser in situ keratomileusis. Ophthalmology 2002;109:973–978. 28. Modis Jr. L,, Langenbucher A, Seitz B. Corneal endothelial cell density and pachymetry measured by contact and noncontact specular microscopy. J Cataract Refract Surg 2002;28:1763–1769. 29. Tai L-Y, Khaw K-W, Ng C-M, Subrayan V. Central corneal thickness measurements with different imaging devices and ultrasound pachymetry. Cornea 2013;32(6):766–771.
ORIGINAL ARTICLE
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Comparison of Central Corneal Thickness Measurements with a Rotating Scheimpflug Camera, a Specular Microscope, Optical Low-Coherence Reflectometry, and Ultrasound Pachymetry in Keratoconic Eyes Yasin Cinar1, Abdullah Kursat Cingu1, Fatih Mehmet Turkcu1, Tuba Cinar2, Alparslan Sahin1, Harun Yuksel1, and Seyhmus Ari1 1
Department of Ophthalmology, Faculty of Medicine, Dicle University, Diyarbakir, Turkey and 2 Diyarbakir Children Hospital, Ophthalmology Clinic, Diyarbakir, Turkey
ABSTRACT Objective: To compare central corneal thickness (CCT) measurements with a rotating Scheimpflug camera (RSC), noncontact specular microscopy (SM), optical low-coherence reflectometry (OLCR), and ultrasonic pachymetry (UP) in keratoconus (KC) patients. Method: In this prospective study, four CCT measurements taken with an RSC, SM, OLCR, and UP were compared in 81 eyes of 44 consecutive KC patients. The KC patients were divided into four subgroups according to Amsler-Krumeich’s KC classification. Results: The RSC and UP measurements of the CCT were not statistically significant in all the groups. Comparison of the SM vs. the OLCR measurements yielded statistically significant differences in all the KC patients and in all KC stages. In all the KC patients, RSC and OLCR showed a high correlation coefficient factor (r = 0.87, p = 0.000). Conclusion: CCT measurements with RSC are comparable to those achieved with UP. Compared with the other devices, according to SM measurements, the central cornea is thicker in all keratoconic eyes and in all KC grades, and it is thinner according to OLCR. RSC, UP, SM, and OLCR should not be used interchangeably in keratoconic eyes. Keywords: Central corneal thickness, keratoconus, pachymetry, scheimpflug camera, reflectometry
INTRODUCTION
Various techniques are available to measure the central corneal thickness (CCT), including ultrasonic pachymetry (UP), optical pachymetry,1 ultrasound biomicroscopy,2 slit scanning corneal topography,3–4 optical coherence tomography (OCT),5 confocal microscopy,6 optical low-coherence reflectometry (OLCR),7 contact or noncontact specular microscopy (SM),8 and dual-beam partial coherence interferometry.9 UP measures corneal thickness using the reflection of sound waves, whereas SM and OLCR utilize light reflection. OLCR measurements provide CCT, details on the axial length, and keratometric readings. SM provides information on the endothelium and CCT.
Keratoconus (KC) is a bilateral noninflammatory disorder characterized by progressive corneal thinning and steepening that results in induced myopia and astigmatism. The diagnosis of KC in patients with classical biomicroscopic findings or retinoscopic signs is not difficult. However, it is challenging in early KC or subclinical KC patients with good visual acuity and delicate signs on examination. In progressive KC, early detection of corneal thinning might be important for patients who could be considered for collagen crosslinking treatment or intracorneal ring segment implantation.
Received 12 April 2013; accepted 26 July 2013; published online 19 September 2013 ¨ niversitesi Tip Fakultesi, Goz Hastaliklari A.D.,21280 Kampus, Diyarbakir, Turkey. E-mail: Correspondence: Yasin Cinar, Dicle U [email protected]
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The rotating Scheimpflug camera (RSC) system yields information on the anterior and posterior corneal topography, corneal volume, corneal pachymetry, and anterior chamber depth. The most widely used method of measuring corneal thickness is UP, which is considered to be the gold standard because of its ease of use, portability, and cost-effectiveness.10–11 As UP is a contact method, topical anesthesia is required. Touching the cornea during the procedure may cause patients discomfort and lead to epithelial erosion and the transmission of infections.12 Indentation of the cornea13 or tear film displacement by the probe14 may produce inaccurate (thinner) measurements. Inappropriate probe placement and tissue hydration may cause observer bias. Thus, UP measurements require some experience.9,15 Many comparisons of different pachymetric techniques have been performed in healthy corneas,5,13,16 and there are few studies of keratoconic eyes.17–19 In this prospective study, we aimed to compare CCT measurements using RSC and SM, OLCR, and UP in keratoconic eyes.
MATERIALS AND METHOD Eighty-one eyes of 44 consecutive patients (24 female and 20 male) previously diagnosed as KC were included in the study. Patients with KC with a clear central cornea were included in the study. The exclusion criteria were as follows: use of contact lens, corneal scarring, previous ocular surgery (e.g., cataract, pterygium, corneal collagen crosslinking, intracorneal ring segment implantation), systemic connective tissue disease, atopy, and dry eye syndrome. Informed consent was obtained from all the patients in accordance with the Declaration of Helsinki before any intervention was performed, and the local ethics committee approved this study. If the patient was under 18 years, a consent form was also obtained from his/her parents. A complete ophthalmic examination was performed, including uncorrected and best corrected visual acuity, refraction for best corrected visual acuity, KC classification, and slit lamp biomicroscopy. A KC diagnosis was made if there was a scissor reflex on retinoscopy and central or paracentral steepening of the cornea on corneal topography with one of the following biomicroscopic findings: central or paracentral steepening, hemosiderin deposition, Vogt’s stria, apical scarring, or breaks in the Descement’s membrane. The eyes were classified into four groups according to the Amsler–Krumeich KC classification,20 which is based on biomicroscopic findings, keratometric readings, pachymetry at the thinnest area of the cornea, and refraction. The corneal thickness measurements were performed in the order of RSC (Pentacam HR, Oculus,
Germany), SM (Konan Noncon Robo specular microscope, Konan Medical Inc., Hyogo, Japan), OLCR (LenStar LS 900, Haag-Streit AG, Koeniz, Switzerland), and UP (US 4000, Nidek, Japan) by the same investigator on the same day. If the patients moved their eyes or blinked, the measurement was repeated to standardize the examinations. For each subject, the pachymetric measurements were performed on the same day, with a 10 min interval between the measurements with the four devices. During the measurement with the RSC, the patients were seated and asked to place their chin on a chinrest, with their forehead touching the headband. The patients were then instructed to look at the black spot in the middle of the blue fixation lamp. On the monitor, the investigator evaluated the position of the image of the eye and then focused the image. The image was then centralized in the aiming circle on the monitor. To eliminate operator-dependent variables, the automatic release mode was used. Three successive measurements of both eyes of the patients were taken over the course of a few minutes. Inappropriate measurements were indicated by a red color on the monitor and were deleted, as recommended by the manufacturer. The average of three pachymetric measurements of the center of the pupil was used for the study. For the SM, the patients were asked to look into the fixation target. The center of the cornea was adjusted by focusing on the center of the pupil on the screen until a clear image appeared on the monitor. When the alignment and focus were appropriate, the endothelial image and the CCT were measured automatically with the device. Three successive measurements were taken. The mean of these three measurements was used for statistical analysis. For the OLCR, the patients were seated and placed their chins on a chinrest with their foreheads on the headrest of the device and were asked to look at the fixation light. According to the manufacturer’s recommendations, both hands were used to adjust the position of the device (for better alignment, one hand was placed on the joystick and the other one on the cross slide), and the device was not moved between the measurements. Implausible measurements marked in a red color on the monitor were deleted, as recommended by the manufacturer. The software calculated the mean of five consecutive measurements. Three successive measurements were obtained for both eyes and the mean of these measurements was used for the analysis. The UP measurements were performed last because they require a contact method. After instillation of one drop of 0.5% proparacaine hydrochloride to the cornea for anesthesia, the patients were asked to look at a distant fixation point, and the UP probe was placed perpendicularly, touching the center of the cornea. Three consecutive measurements were Seminars in Ophthalmology
Central Corneal Thickness Measurements in Keratoconus performed for both eyes, and the mean of these measurements was used for the analysis.
were stage 4 KC). OLCR could not measure the CCT only in one eye, which was stage 2 KC.
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STATISTICAL ANALYSIS
Comparison of the Mean CCT Measurements
The Statistical Package for the Social Sciences statistical software, version 11.5 (SPSS Inc., Chicago, IL, USA) was used for the statistical analysis. To analyze the distribution of the data, a Kolmogorov-Smirnov test was performed. The data were distributed normally, and a paired t test was used to analyze the differences between the measurements of the devices. Pearson’s coefficient of correlation was used to express the strength of the relationship between the measurements of the devices. A p value less than 0.05 was considered significant.
The KC grades and the mean CCT measurements of all the patients obtained by the four devices are shown in Table 1. Table 1 also shows the p values of the binary comparisons of the four different methods used to measure the CCT. The CCT measurements obtained by the RSC and UP were not significantly different in any of the groups (Table 1). The SM vs. the OLCR measurements were significantly different in the whole cohort and also in every KC stage. There were significant differences between the CCT measurements of RSC vs. SM, RSC vs. OLCR, SM vs. OLCR, SM vs. UP, and OLCR vs. UP in the whole cohort. The RSC measures were, on average, 0.02 26.7 mm thinner than UP in all the KC patients. The CCT measurements with SM were significantly greater than those of the other devices in every stage of KC.
RESULTS Six patients had unilateral KC. One eye of a patient with facial nerve paralysis accompanying mild exposure keratopathy was excluded. The mean age of the patients was 19.0 5.33 years (range 10–32 years). The mean keratometric value (K) was 50.5 5.25 Diopter (D) according to the RSC. The mean manifest refraction spherical equivalent (MRSE) was 5.13 3.02 D. According to the Amsler-Krumeich classification, there were 25 stage 1, 35 stage 2, 13 stage 3, and eight stage 4 eyes. The mean MRSE was 3.2 1.7 D in stage 1, 4.6 1.8 D in stage 2, 7.3 2.0 D in stage 3, and 9.8 4.4 D in stage 4 KC. The CCT measurements could be performed in all the patients using RSC and UP, whereas SM could not measure the CCT in seven eyes of six patients (two eyes were stage 2, three eyes were stage 3, two eyes
Correlations between the Pachymetry Methods Table 2 represents the correlation coefficients (r values) and p values of Pearson’s correlation test, showing the agreements between the CCT measurements with RSC, SM, OLCR, and UP in the study. A scatter plot of the CCT measurements is shown in Figure 1. When all the patients were considered, the highest correlation coefficient was found between RSC and
TABLE 1. The mean CCT measurements of four instruments in the whole cohort and in the subgroups according to Amsler-Krumeich classification; at the bottom p values of CCT measurements among four devices in all patients and subgroups. RSC
UP
SM
OLCR
All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
458 45.6 478 43.6 468 30.6 441 29.0 379 39.5
458 46.5 480 40.2 465 27.8 440 38.5 389 69.2
474 38.9 487 49.6 468 22.7 456 33.3 474 58.4
448 44.6 473 36.1 457 23.2 429 24.8 357 38.7
*p Values All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
RSC vs UP 0.993 0.674 0.307 0.902 0.658
RSC vs SM 0.004 0.062 0.535 0.025 0.078
RSC vs OLCR 50.001 0.274 50.001 0.018 0.277
SM vs OLCR 50.001 0.013 0.001 0.018 0.010
SM vs UP 0.009 0.106 0.394 0.183 0.087
OLCR vs UP 0.002 0.126 0.005 0.167 0.273
UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera; CCT: Central Corneal Thickness; KC: Keratoconus. p50.05 considered as significant; *paired t test. !
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TABLE 2. Degree correlation between the CCT measurements of the devices. RSC vs UP þ
All patients Grade 1 KC Grade 2 KC Grade 3 KC Grade 4 KC
RSC vs SM
RSC vs OLCR
SM vs OLCR
SM vs UP
OLCR vs UP
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
þ
r
*p
0.83 0.9 0.83 0.68 0.46
50.001 50.001 50.001 0.011 0.251
0.59 0.87 0.6 0.8 0.62
50.001 50.001 50.001 0.005 0.263
0.87 0.88 0.88 0.85 0.1
50.001 50.001 50.001 50.001 0.798
0.59 0.86 0.63 0.57 0.42
50.001 50.001 50.001 0.083 0.483
0.44 0.89 0.49 0.68 0.89
50.001 50.001 0.004 0.03 0.044
0.79 0.87 0.8 0.75 0.1
50.001 50.001 50.001 0.003 0.814
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UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera; KC: Keratoconus; CCT: Central Corneal Thickness. þPearsons correlation coefficient; *paired t test. p50.05 considered as significant.
OLCR (r = 0.87, p5.001). In the grade 1 KC group, there were high correlations between each binary comparison of the four different methods, particularly with RSC and UP (r = 0.9, p50.001). RSC vs. OLCR had the highest correlation coefficient in grade 2 KC (r = 0.88, p50.001) and grade 3 KC (r = 0.85, p50.001) patients. In the grade 4 KC group, UP vs. SM had a significant negative correlation coefficient (r = 0.89, p = 0.044) (Table 2).
DISCUSSION The measurement of the CCT is crucial in the diagnosis, follow-up, and treatment of KC. In the corneal collagen crosslinking procedure, the recommended corneal thickness is at least 400 mm to avoid damage to the corneal endothelium and deeper structures of the eye, such as the lens and the retina.21 In corneal intrastromal ring segment implantation, the thickness at the implanted site should not be less than 400 mm to prevent full thickness corneal incision or shallow placement of the ring segment.22 In recent years, new devices have been introduced to measure the CCT in a noncontact way. This study compared CCT measurements obtained by four different methods in keratoconic eyes: RSC, SM, OLCR, and UP. To the best of our knowledge, this is the first study to compare the use of these four devices to measure the CCT in KC patients. Uc¸akhan et al. reported a comparison of CCT with RSC, SM, and UP measurements in normal and keratoconic corneas.17 According to their results, RSC had better reproducibility than UP and SM in moderate keratoconic eyes. They found a very high correlation between the RSC and UP measurements in mild and severe KC, whereas SM was unable to measure the CCT in any of the eyes with severe KC and 42.9% of the eyes with moderate KC in their study population. They reported a correlation coefficient of 0.92 between the RSC and UP measurements in the keratoconic eyes. In the current study, the KC patients were staged according to the Amsler–Krumeich KC classification, and SM could not measure the CCT
only in seven eyes of six bilateral KC patients. Of these, two eyes were stage 2, three eyes were stage 3, and two eyes were stage 4 KC. In the present study, when we compared the UP and RSC measurements in all the keratoconic patients, the measurements were not statistically significant (p = 0.993), and there was a significant correlation (r = 0.83, p50.001). The measurements with UP were slightly thicker than those obtained with the RSC, a finding in agreement with some previous studies13,17,23 in which UP measured thicker than RSC. The thinnest pachymetry point measured by the RSC and the slit scan corneal topography showed no significant difference in mean deviation.19 However, Dutta et al. demonstrated that UP yielded significantly higher CCT values than slit scan corneal topography.18 This finding was attributed to the posterior reflection point of the sound waves of the UP not being identified. However, this point is supposed to be between Descement’s membrane and the anterior chamber.17 Furthermore, compression of the epithelium and displacement of a 7 to 40 mm thick tear film by the UP probe may underestimate CCT measurements.24–25 Some studies have reported that the agreement between OLCR and US pachymetry in CCT measurements is very good.12,26 Spadea et al. reported that a comparison of OLCR and US pachymetry in the measurement of the CCT before and after photorefractive keratectomy had a smaller effect on the agreement between the two devices. They also noted that these two devices could be used interchangeably in normal eyes and in the planning of refractive surgery.26 In the present study, the UP measurements were thicker than those obtained with OLCR, in agreement with a previous study.27 When all the KC patients were considered, the mean difference between the CCT measurements of these two devices was 10.5 mm. The mean difference between the UP and OLCR measurements was greater in grade 4 KC compared to grade 1 KC. The correlation coefficient between UP and OLCR was 0.79 (p50.001) in grade 1 KC and 0.1 (p = 0.814) in grade 4 KC. These two devices should not be used interchangeably in KC patients. Seminars in Ophthalmology
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Central Corneal Thickness Measurements in Keratoconus
FIGURE 1. (a) Scatterplot of CCT measurements taken by UP and RSC; (b) scatterplot of CCT measurements taken by RSC and SM; (c) scatterplot of CCT measurements taken by RSC and OLCR; (d) scatterplot of CCT measurements taken by SM and OLCR; (e) scatterplot of CCT measurements taken by UP and SM; (f) scatterplot of CCT measurements taken by UP and OLCR. UP: Ultrasonic Pachymetry; SM: Specular Microscopy; OLCR: Optical Low Coherence Reflectometer; RSC: Rotating Scheimpflug Camera.
Ucakhan and associates17 reported that the mean differences between UP-SM, RSC-SM, and RSC-UP were 18.8 mm, 12.7 mm, and 11.2 mm, respectively, in keratoconic eyes. In the current study, the mean !
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differences between UP-SM, RSC-SM, and RSC-UP were 14.4 mm, 13 mm, and 0.02 mm, respectively. In contrast to the results of Ucakhan and associates, SM failed to measure the CCT in only two grade 4 KC
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eyes in the current study. This may be because the anterior corneal refractive power affects noncontact specular images.28 Tai et al.29 reported CCT measurements in healthy subjects using RSC, SM, OLCR, and UP. They found that the mean CCT differences between the methods in pairwise comparisons were statistically significant except for OLCR vs. UP and OLCR vs. RSC. They found the greatest mean difference (30.57 mm) among the comparisons between the RSC and SM. The smallest mean difference was 3.54 mm. This was found between OLCR and UP in the same study. In the current study, the greatest mean difference was between SM and OLCR (21.8 mm), and the smallest mean difference was between UP and RCS (0.02 mm) in the whole cohort. Barkana and associates13 reported that the RSC system and OLCR pachymeter are convenient and provide excellent intraoperator repeatability and reproducibility in CCT measurements in healthy subjects. They found CCT values achieved by the RSC were similar to those achieved with both the OLCR pachymeter and the US pachymeter. The correlation coefficient was 0.96 between the RSC and OLCR, according to their results. In the current study, the CCT measurements with the RSC and OLCR were close to each other, and the correlation coefficient was 0.87 between these two devices. However, it was not statistically significant in all the KC patients. The current study has some limitations, such as the lack of a healthy control group, the reliability and reproducibility analyses of the devices, and the small sample size of the study population. Nevertheless, this is the first study comparing CCT measurements of SM and OLCR in keratoconic eyes. The study found that SM and OLCR measurements of the CCT are significantly different in keratoconic eyes. In conclusion, CCT measurements with the RSC seem to be comparable to those achieved with UP. Compared with the other three devices, the CCT is thicker according to SM measures and thinner according to OLCR measures in all keratoconic eyes and in all KC grades. RSC, UP, SM, and OLCR should not be used interchangeably in keratoconic eyes.
DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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