Original Paper
Ophthalmologica
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
Received: March 26, 2013 Accepted after revision: September 20, 2013 Published online: March 13, 2014
Agreement between Central Corneal Thickness Measured Using Pentacam, Ultrasound Pachymetry, Specular Microscopy and Optic Biometer Lenstar LS 900 and the Influence of Intraocular Pressure L. Borrego-Sanz a, b F. Sáenz-Francés a, b M. Bermudez-Vallecilla a, b L. Morales-Fernández a, b J.M. Martínez-de-la-Casa a, b E. Santos-Bueso a, b L. Jañez c J. García-Feijoo a, b a
Department of Ophthalmology, Hospital Clínico San Carlos, Universidad Complutense de Madrid, b Instituto de Salud Carlos III, ‘Red Temática de Investigación Cooperativa’, and c Instituto de Tecnología del Conocimiento, Universidad Complutense de Madrid, Madrid, Spain
Key Words Central corneal thickness · Lenstar · Specular microscopy · Intraocular pressure
Abstract Purpose: To compare central corneal thickness (CCT) values obtained by Lenstar (LE), Pentacam (PC), specular microscopy (SM) and ultrasound pachymetry (UP) in healthy corneas and study their influence on intraocular pressure (IOP) readings determined by Goldmann applanation tonometry (GAT). Methods: CCT was measured in 76 healthy subjects by LE, PC, SM and UP. We established Lin’s concordance correlation coefficient (ρ-C) between different techniques. The influence of CCT on GAT was established through univariate linear regression models, IOP being the dependent variable. Results: The highest ρ-C was found between LE and SM at 0.94 (95% CI: 0.91–0.96) and between LE and UP at 0.95 (95% CI: 0.94–0.97). IOP readings showed less variability when CCT was determined using LE (7.7%, B = 0.16; 95% CI: 0.004–0.28). Conclusions: Although CCT values obtained with UP, PC, SM and LE show good correlation, these methods are not completely interchangeable. The amount of IOP variation differs when CCT is determined using LE or SM. © 2014 S. Karger AG, Basel
© 2014 S. Karger AG, Basel 0030–3755/14/2314–0226$39.50/0 E-Mail [email protected] www.karger.com/oph
Introduction
An accurate measurement of central corneal thickness (CCT) is a major factor for monitoring intraocular pressure (IOP) values in the context of glaucoma, interpreting corneal ectasias, assessing complications related to the use of contact lenses or planning refractive surgery procedures and monitoring their postoperative course [1]. There are several techniques to measure the CCT, but probably the most widespread method in clinical practice remains ultrasound pachymetry (UP), due to the high degree of interobserver reproducibility, the ease of its use, portability and low cost [1, 2]. However, several limitations have been described in its use, such as the fact that the measurements require corneal contact and therefore the need for topical anesthesia, and include risks such as damage to the corneal epithelium or transmission of infectious diseases. Furthermore, possible misalignment of the probe or lack of fixation by the patient may cause biases in the measurements [1]. Therefore, other methods to measure CCT such as the new Lenstar biometer (LE), the Pentacam (PC) or specular microscopy (SM) can provide substantial benefits as they are noncontact methods, easy to use, not operatordependent, with no great cooperation requirements from Lara Borrego-Sanz C/Santa Engracia 136 1 Dcha ES–28003 Madrid (Spain) E-Mail larabs70 @ hotmail.com
Material and Methods The subjects enrolled for this cross-sectional study were 76 healthy volunteers recruited among the staff and relatives of patients of our institution. Mean (±SD) age was 35.03 ± 11.5 years (42 women, 34 men). Only one eye per volunteer was examined; the decision to analyze the right or left eye was made according to an automated randomization procedure (www.randomization. com). Informed consent was obtained from each volunteer according to the tenets of the Declaration of Helsinki. Exclusion criteria were: a spherical equivalent greater than 5 diopters or 3 or more diopters of astigmatism, IOP higher than 21 mm Hg or glaucomatous appearance of the optic disk. We also excluded subjects who had undergone previous eye surgery or had a corneal disease including leukoma or pterygium. All the study participants underwent a PC (Oculus Inc., Lynnwood, USA) examination, LE LS 900 (Haag-Streit, Köniz, Switzerland) biometry, UP (Dicon P55, Paradigm Medical Industries Inc., Salt Lake City, Utah, USA) and SM (SP-2000P Topcon Corp., Tokyo, Japan) realized by the same experienced examiner. The order in which the different devices were used was automatically randomized (www.randomization.com) except for the UP, that was performed in all cases last for being a contact test. All measurements were obtained between 10 and 14 h, to avoid the influence of diurnal variations of CCT, with an interval of 5–10 min between the different measurements. IOP was determined using GAT (Haag-Streit) after instillation of one drop of Fluotest® (topical fluorescein 0.25% and oxybuprocain 0.4%). The measurements were obtained 1 h after UP measurement to avoid any interference of the applanation produced by the transducer of UP.
Central Corneal Thickness and Intraocular Pressure
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the patient, multiple applications in corneal examination and with the added ability to estimate biometric measurements or performing a count of endothelial cells [1, 3]. On the other hand, it is widely known that CCT measurements significantly affect IOP values. The influence of corneal thickness on IOP readings measured by conventional tonometry, Goldmann applanation tonometry (GAT), has been extensively studied, showing that CCT is one of the main sources of error of this tonometry system. For this reason, a wide variety of new instruments has been developed with the aim to overcome the limitations of the GAT results [4, 5]. However, less is known about the influence that the different devices chosen to measure CCT may have on IOP variation. The purpose of this study was to assess the agreement between the CCT measurements obtained by the currently most widespread method, the UP, and the measurements obtained with the PC, noncontact SM and biometer LE LS900 in healthy subjects, and to analyze the influence of each CCT determination on IOP readings obtained using GAT.
700
600
500
400 PC
LE
SM
UP
Fig. 1. Box-plot diagrams showing the distribution of measurements between the CCT values measured by the four systems.
Table 1. Mean (±SD) CCT obtained by SM, PC, LE, UP and the
mean IOP value measured with GAT Variable
Mean
SD
PC LE SM UP IOP GAT
565.3553 543.0526 537.2368 549.6053 13.99747
36.33573 34.27181 36.33176 32.63049 1.826921
Agreement between the pachymeters (every pair) was established using Lin’s concordance correlation coefficient (ρ-C). The Bland-Altman method was used to identify systematic and/or proportional biases between the pairs of CCT measurements. The influence of CCT on GAT was established through four univariate linear regression models, IOP being the dependent variable in all of them, and each of the four pachymetric measurements the predictive variable in each model. The differences of the amount of GAT variation produced by each CCT measurement (regression sum of squares) were compared using t test for repeated measures for each pair of CCT determination. The level of significance was set at p < 0.05.
Results
The distribution of measurements between the different CCT values measured by the four systems are shown in figure 1 by box-plot diagrams. The mean CCT (±SD) for SM, PC, LE and UP is shown in table 1, also the mean IOP value measured with GAT. Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
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10
Difference of LE and UP
0
–10
–20
–30
–40 500
550
600
Mean of LE and UP Observed average agreement
95% limits of agreement
y = 0 is the line of perfect average agreement
Fig. 2. Bland-Altman of agreement be-
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tween Lenstar and UP measurements.
Difference of LE and SM
40
20
0
–20
450
500
550
600
Mean of LE and SM
Fig. 3. Bland-Altman of agreement be-
tween Lenstar and specular microscopy measurements.
Observed average agreement
The ρ-C between PC and LE was 0.78 (95% confidence interval, 95% CI: 0.71–0.85), between PC and SM 0.69 (95% CI: 0.6–0.78), between PC and UP 0.83 (95% CI: 0.76–0.89), between LE and SM 0.94 (95% CI: 0.91–0.96), between LE and UP 0.95 (95% CI: 0.94–0.97) and between SM and UP 0.86 (95% CI: 0.8–0.91). Figures 2–7 show the Bland-Altman graphics between the pair of methods used to determine the CCT and table 2 shows the mean differ228
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
9 95% limits of agreement
y = 0 is the line of perfect average agreement
ences between the measurements of each pair of methods within 95% limits of agreement. The regression models revealed that when CCT was determined using the PC, the amount of GAT variation was 8.9% (adjusted R2, B = 0.016; 95% CI: 0.005–0.27, fig. 8), when CCT was determined using the LE the amount of GAT variation was 7.7% (B = 0.16; 95% CI: 0.004–0.28, fig. 9), when CCT was determined using the Borrego-Sanz et al.
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Difference of PC and LE
60
40
20
0
–20 500
550
600
650
Mean of PC and LE Observed average agreement
95% limits of agreement
y = 0 is the line of perfect average agreement
Fig. 4. Bland-Altman of agreement be-
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tween PC and Lenstar measurements. 80
Difference of PC and UP
60
40
20
0
–20 500
550
600
650
Mean of PC and UP Observed average agreement
Fig. 5. Bland-Altman of agreement be-
95% limits of agreement
y = 0 is the line of perfect average agreement
tween PC and UP measurements.
SM the amount of GAT variation was 10.3% (B = 0.017; 95% CI: 0.006–0.028, fig. 10) and when CCT was determined using UP the amount of GAT variation was 8.9% (B = 0.19; 95% CI: 0.006–0.03, fig. 11). There was a statistically significant difference between the amount of variation produced by SM and LE (p = 0.02, fig. 12).
Central Corneal Thickness and Intraocular Pressure
Discussion
To perform an accurate measurement of CCT is increasingly important in clinical ophthalmology [6, 7]. Currently there are several methods to calculate the CCT, although probably the most widespread method is still UP. UP is an easy to use tool, and in addition it provides a high degree of intraobserver reproducibility [8, 9]. Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
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Difference of PC and SM
80
60
40
20
0 500
550
600
Mean of PC and SM Observed average agreement
Fig. 6. Bland-Altman of agreement be-
95% limits of agreement
Color version available online
y = 0 is the line of perfect average agreement
tween PC and specular microscopy measurements. 20
Difference of SM and UP
0
–20
–40
–60
–80 500
550
600
Mean of SM and UP
Fig. 7. Bland-Altman of agreement be-
tween specular microscopy and UP measurements.
Observed average agreement
However, UP is a manual technique, and thus, the interexaminer reproducibility of this instrument, although suitable, is slightly lower [8, 10]. It also has the disadvantage that the measurements depend on the contact between the cornea and the probe, which may change according to the pressure applied by the operator and can lead to ocular surface distortion [2]. Several studies have shown that the probe can change the thickness of the tear 230
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
95% limits of agreement
y = 0 is the line of perfect average agreement
film by 7–40 μm and this compression could reduce epithelial thickness, resulting in biases in CCT measurements [2, 11]. Another limitation is the fact that instillation of topical anesthesia is necessary to perform the measurements. Changes in CCT of ±10 μm after topical anesthesia instillation have also been reported [12, 13]. Therefore, new techniques to determine CCT have been developed with the added advantage of evaluating Borrego-Sanz et al.
Color version available online
18
16
14
12
10 500
Fig. 8. Regression model of CCT deter-
550
600 PC Fitted values
mined using the specular microscopy and GAT variation.
650
700
IOP
parameters useful for clinical practice. For example, PC is used to calculate corneal topography with multiple applications in corneal and refractive surgery, intraocular lens implantation and glaucoma [14, 15]; the LE biometer provides information on keratometry, anterior chamber depth, lens thickness or intraocular lens measurements, and SM, whose substantial properties are endothelial cell counting, is essential in assessing the evolution of certain refractive surgical procedures, such as phakic lens implants, cataract surgery or corneal transplants [1, 3, 6, 16]. In this study we compared the agreement between the CCT measurements obtained using the PC, LE LS 900, UP and SM and analyzed their influence on IOP readings determined by GAT. Today’s gold standard for measur-
ing IOP remains the GAT, although its measurements are conditioned by various morphometric features of the cornea including CCT [17, 18]. Several new IOP measuring instruments have been developed with the express purpose to make measurements less conditioned by corneal factors. However, while much attention has been paid to the method used to determine IOP and its reliability, the influence that the different systems used to measure CCT may have on IOP variations has not been subject to such rigorous validation [19, 20]. In this study, we found that the LE-UP showed the closest agreement, followed by the LE-SM and PC-UP. This was also reported by previously publications. Tai et al. [21], in a study of 184 eyes, also found close agreement between LE and UP. This statement agrees with another study by Beutelspacher et al. [22], who compared CCT measures obtained with OCT, LE, PC and UP showing good agreement. The relatively new LE biometer is a promising noninvasive device with a high reproducibility [23]. A high degree of concordance has been described between the LE and LioMaster regarding to the biometric measurements, although unlike LioMaster, LE has the advantage of measuring additional variables such as the CCT [24]. In previous reports, O’Donnell et al. [3] and Zhao et al. [23] showed good concordance between CCT measurements obtained by PC and LE, although they could not be considered interchangeable in clinical practice. In
Central Corneal Thickness and Intraocular Pressure
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
Table 2. Mean difference between the measurements obtained by each pair of methods
Method 1 – method 2 PC-LE PC-SM PC-UP LE-SM LE-UP SM-UP
Mean difference, 95% limits of agreement μm low high 22.3 28.12 15.75 5.82 –6.55 –12.37
–3.09 –4.47 –12.51 –16.32 –21.95 –40.49
47.7 60.71 44.01 27.95 8.85 15.75
231
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18
16
14
12
10 450
500
Fig. 9. Regression model of CCT deter-
550 LE Fitted values
650
IOP
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mined using the Lenstar biometer and GAT variation.
600
18
16
14
12
10 400
Fig. 10. Regression model of CCT deter-
mined using specular microscopy and GAT variation.
contrast, our study showed a relatively low correlation between these two devices when compared with the high agreement obtained between LE-UP or PC-UP. Additionally, some studies have shown that LE offered lower CCT values than those provided by the PC. This could happen because the CCT is calculated using only one measurement in the case of the PC and LE relies on five measurements on average, leading to biases in measurements [25]. 232
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
450
500 SM
550
Fitted values
600
IOP
In spite of the amount of studies showing good correlation between UP and PC measurements, Tai et al. [21] have claimed recently that the mean CCT by PC was 10 μm higher than that obtained using UP [10], which correlates well with our findings, showing significantly higher values in PC measurements. This could be explained because the PC pachymeter may include the precorneal tear film in the measurement of corneal thickness, whereas the UP probe displaces the Borrego-Sanz et al.
Color version available online
18
16
14
12
10 450
500
550 UP Fitted values
Fig. 11. Regression model of CCT deter-
600
650
IOP
Color version available online
mined using UP and GAT variation.
tear film and compresses the corneal surface, resulting therefore in lower values [21, 26]. On the other hand, it has been widely stated that SM shows lower values of CCT than those obtained by UP and PC in healthy subjects [1, 12, 21]. Nevertheless, good linear correlations between the measurements of the three instruments have been shown in the literature [1]. Furthermore, Almubrad et al. [12] and other authors agree that CCT is significantly underestimated by SM (28.17 ± 19.20 μm) comparing with UP in healthy sub-
jects, so that they could not be considered to be interchangeable [12, 27]. Similar results were also reported by Özlenen-Ucakhan et al. [1] in normal eyes or eyes affected with mild keratoconus. These differences may be due to the different operating principles that guide each device. While SM relies on light reflection, UP depends on sound transmission. Although these authors claim that the reproducibility and repeatability of SM were higher than those achieved with UP, probably this happens because UP is a contact device, operator-dependent and therefore subject to potential biases in the measurements [1, 12, 21, 27]. Surprisingly, in our study we found high correlation in CCT measures between SM-LE and SM-UP, which correlates well with Chaudhry [28], who found no significant differences in the mean CCT values performed with SM and UP. Furthermore, SM proved to be a reliable and reproducible method in pediatric patients with poor cooperation [29]. Besides agreement between the different pachymeter systems, this study was also designed to determine how the use of one or the other pachymetry method might influence IOP measurements made using GAT. Our data revealed that as in previous studies, GAT readings were conditioned by CCT. The amount of variation in GATdetermined IOP due to CCT was greater when this variable was measured by SM than by UP and PC. The lowest variation was found when CCT was measured by LE, in
Central Corneal Thickness and Intraocular Pressure
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
30
20
10
0 PC
LE
SM
UP
Fig. 12. IOP variation with CCT (regression sum of squares). A
statistically significant difference exists between specular microscopy and Lenstar.
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fact, when analyzing the differences between the amount of IOP variation produced by the different CCT determinations, only a statistically significant difference between SM and LE arose. This could also be explained, because the SM image is reflected at the optical interface between the corneal endothelium and aqueous humor, corneal morphometry appreciably influences the rest of measurements due to light transmission distortion [1, 11, 12]. The pachymetry of choice should be the one that offers accuracy, precision and no need for long measurement time. Our study revealed that LE agreement with SM and UP is excellent and this, added to the ease of its use and its noninvasiveness, results in a very promising tool [23, 30]. Moreover, for LE and SM proper alignment has shown to be easier and less time-consuming than for UP and PC [21]. Nevertheless, our results are limited to a sample of healthy subjects, so future studies are needed to determine whether our findings may be extrapolated to other populations with ophthalmic diseases, such as glaucoma patients, who often show CCT and IOP variation, and
therefore to assess what is the most beneficial option in each case. In conclusion, we can assume that although the CCT values obtained with UP, PC, SM and LE show good correlation, especially measurements between LE-UP and LE-SM, it should be noted that these methods are not completely interchangeable. The amount of IOP variation differs when CCT is determined using LE or SM; no other IOP variation differences arose when comparing the remaining pairs of CCT measurement methods. Acknowledgments Supported in part by Instituto de Salud Carlos III, ‘Red Temática de Investigación Cooperativa, Proyecto RD07/0062: Patología ocular del envejecimiento, calidad visual y calidad de vida’.
Disclosure Statement All authors disclose no conflict of interest in the products, drugs, instruments and pieces of equipment mentioned in this article.
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Copyright: S. Karger AG, Basel 2014. Reproduced with the permission of S. Karger AG, Basel. Further reproduction or distribution (electronic or otherwise) is prohibited without permission from the copyright holder.
Ophthalmologica
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
Received: March 26, 2013 Accepted after revision: September 20, 2013 Published online: March 13, 2014
Agreement between Central Corneal Thickness Measured Using Pentacam, Ultrasound Pachymetry, Specular Microscopy and Optic Biometer Lenstar LS 900 and the Influence of Intraocular Pressure L. Borrego-Sanz a, b F. Sáenz-Francés a, b M. Bermudez-Vallecilla a, b L. Morales-Fernández a, b J.M. Martínez-de-la-Casa a, b E. Santos-Bueso a, b L. Jañez c J. García-Feijoo a, b a
Department of Ophthalmology, Hospital Clínico San Carlos, Universidad Complutense de Madrid, b Instituto de Salud Carlos III, ‘Red Temática de Investigación Cooperativa’, and c Instituto de Tecnología del Conocimiento, Universidad Complutense de Madrid, Madrid, Spain
Key Words Central corneal thickness · Lenstar · Specular microscopy · Intraocular pressure
Abstract Purpose: To compare central corneal thickness (CCT) values obtained by Lenstar (LE), Pentacam (PC), specular microscopy (SM) and ultrasound pachymetry (UP) in healthy corneas and study their influence on intraocular pressure (IOP) readings determined by Goldmann applanation tonometry (GAT). Methods: CCT was measured in 76 healthy subjects by LE, PC, SM and UP. We established Lin’s concordance correlation coefficient (ρ-C) between different techniques. The influence of CCT on GAT was established through univariate linear regression models, IOP being the dependent variable. Results: The highest ρ-C was found between LE and SM at 0.94 (95% CI: 0.91–0.96) and between LE and UP at 0.95 (95% CI: 0.94–0.97). IOP readings showed less variability when CCT was determined using LE (7.7%, B = 0.16; 95% CI: 0.004–0.28). Conclusions: Although CCT values obtained with UP, PC, SM and LE show good correlation, these methods are not completely interchangeable. The amount of IOP variation differs when CCT is determined using LE or SM. © 2014 S. Karger AG, Basel
© 2014 S. Karger AG, Basel 0030–3755/14/2314–0226$39.50/0 E-Mail [email protected] www.karger.com/oph
Introduction
An accurate measurement of central corneal thickness (CCT) is a major factor for monitoring intraocular pressure (IOP) values in the context of glaucoma, interpreting corneal ectasias, assessing complications related to the use of contact lenses or planning refractive surgery procedures and monitoring their postoperative course [1]. There are several techniques to measure the CCT, but probably the most widespread method in clinical practice remains ultrasound pachymetry (UP), due to the high degree of interobserver reproducibility, the ease of its use, portability and low cost [1, 2]. However, several limitations have been described in its use, such as the fact that the measurements require corneal contact and therefore the need for topical anesthesia, and include risks such as damage to the corneal epithelium or transmission of infectious diseases. Furthermore, possible misalignment of the probe or lack of fixation by the patient may cause biases in the measurements [1]. Therefore, other methods to measure CCT such as the new Lenstar biometer (LE), the Pentacam (PC) or specular microscopy (SM) can provide substantial benefits as they are noncontact methods, easy to use, not operatordependent, with no great cooperation requirements from Lara Borrego-Sanz C/Santa Engracia 136 1 Dcha ES–28003 Madrid (Spain) E-Mail larabs70 @ hotmail.com
Material and Methods The subjects enrolled for this cross-sectional study were 76 healthy volunteers recruited among the staff and relatives of patients of our institution. Mean (±SD) age was 35.03 ± 11.5 years (42 women, 34 men). Only one eye per volunteer was examined; the decision to analyze the right or left eye was made according to an automated randomization procedure (www.randomization. com). Informed consent was obtained from each volunteer according to the tenets of the Declaration of Helsinki. Exclusion criteria were: a spherical equivalent greater than 5 diopters or 3 or more diopters of astigmatism, IOP higher than 21 mm Hg or glaucomatous appearance of the optic disk. We also excluded subjects who had undergone previous eye surgery or had a corneal disease including leukoma or pterygium. All the study participants underwent a PC (Oculus Inc., Lynnwood, USA) examination, LE LS 900 (Haag-Streit, Köniz, Switzerland) biometry, UP (Dicon P55, Paradigm Medical Industries Inc., Salt Lake City, Utah, USA) and SM (SP-2000P Topcon Corp., Tokyo, Japan) realized by the same experienced examiner. The order in which the different devices were used was automatically randomized (www.randomization.com) except for the UP, that was performed in all cases last for being a contact test. All measurements were obtained between 10 and 14 h, to avoid the influence of diurnal variations of CCT, with an interval of 5–10 min between the different measurements. IOP was determined using GAT (Haag-Streit) after instillation of one drop of Fluotest® (topical fluorescein 0.25% and oxybuprocain 0.4%). The measurements were obtained 1 h after UP measurement to avoid any interference of the applanation produced by the transducer of UP.
Central Corneal Thickness and Intraocular Pressure
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the patient, multiple applications in corneal examination and with the added ability to estimate biometric measurements or performing a count of endothelial cells [1, 3]. On the other hand, it is widely known that CCT measurements significantly affect IOP values. The influence of corneal thickness on IOP readings measured by conventional tonometry, Goldmann applanation tonometry (GAT), has been extensively studied, showing that CCT is one of the main sources of error of this tonometry system. For this reason, a wide variety of new instruments has been developed with the aim to overcome the limitations of the GAT results [4, 5]. However, less is known about the influence that the different devices chosen to measure CCT may have on IOP variation. The purpose of this study was to assess the agreement between the CCT measurements obtained by the currently most widespread method, the UP, and the measurements obtained with the PC, noncontact SM and biometer LE LS900 in healthy subjects, and to analyze the influence of each CCT determination on IOP readings obtained using GAT.
700
600
500
400 PC
LE
SM
UP
Fig. 1. Box-plot diagrams showing the distribution of measurements between the CCT values measured by the four systems.
Table 1. Mean (±SD) CCT obtained by SM, PC, LE, UP and the
mean IOP value measured with GAT Variable
Mean
SD
PC LE SM UP IOP GAT
565.3553 543.0526 537.2368 549.6053 13.99747
36.33573 34.27181 36.33176 32.63049 1.826921
Agreement between the pachymeters (every pair) was established using Lin’s concordance correlation coefficient (ρ-C). The Bland-Altman method was used to identify systematic and/or proportional biases between the pairs of CCT measurements. The influence of CCT on GAT was established through four univariate linear regression models, IOP being the dependent variable in all of them, and each of the four pachymetric measurements the predictive variable in each model. The differences of the amount of GAT variation produced by each CCT measurement (regression sum of squares) were compared using t test for repeated measures for each pair of CCT determination. The level of significance was set at p < 0.05.
Results
The distribution of measurements between the different CCT values measured by the four systems are shown in figure 1 by box-plot diagrams. The mean CCT (±SD) for SM, PC, LE and UP is shown in table 1, also the mean IOP value measured with GAT. Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
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Difference of LE and UP
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Mean of LE and UP Observed average agreement
95% limits of agreement
y = 0 is the line of perfect average agreement
Fig. 2. Bland-Altman of agreement be-
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tween Lenstar and UP measurements.
Difference of LE and SM
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0
–20
450
500
550
600
Mean of LE and SM
Fig. 3. Bland-Altman of agreement be-
tween Lenstar and specular microscopy measurements.
Observed average agreement
The ρ-C between PC and LE was 0.78 (95% confidence interval, 95% CI: 0.71–0.85), between PC and SM 0.69 (95% CI: 0.6–0.78), between PC and UP 0.83 (95% CI: 0.76–0.89), between LE and SM 0.94 (95% CI: 0.91–0.96), between LE and UP 0.95 (95% CI: 0.94–0.97) and between SM and UP 0.86 (95% CI: 0.8–0.91). Figures 2–7 show the Bland-Altman graphics between the pair of methods used to determine the CCT and table 2 shows the mean differ228
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
9 95% limits of agreement
y = 0 is the line of perfect average agreement
ences between the measurements of each pair of methods within 95% limits of agreement. The regression models revealed that when CCT was determined using the PC, the amount of GAT variation was 8.9% (adjusted R2, B = 0.016; 95% CI: 0.005–0.27, fig. 8), when CCT was determined using the LE the amount of GAT variation was 7.7% (B = 0.16; 95% CI: 0.004–0.28, fig. 9), when CCT was determined using the Borrego-Sanz et al.
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Difference of PC and LE
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40
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–20 500
550
600
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Mean of PC and LE Observed average agreement
95% limits of agreement
y = 0 is the line of perfect average agreement
Fig. 4. Bland-Altman of agreement be-
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tween PC and Lenstar measurements. 80
Difference of PC and UP
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40
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0
–20 500
550
600
650
Mean of PC and UP Observed average agreement
Fig. 5. Bland-Altman of agreement be-
95% limits of agreement
y = 0 is the line of perfect average agreement
tween PC and UP measurements.
SM the amount of GAT variation was 10.3% (B = 0.017; 95% CI: 0.006–0.028, fig. 10) and when CCT was determined using UP the amount of GAT variation was 8.9% (B = 0.19; 95% CI: 0.006–0.03, fig. 11). There was a statistically significant difference between the amount of variation produced by SM and LE (p = 0.02, fig. 12).
Central Corneal Thickness and Intraocular Pressure
Discussion
To perform an accurate measurement of CCT is increasingly important in clinical ophthalmology [6, 7]. Currently there are several methods to calculate the CCT, although probably the most widespread method is still UP. UP is an easy to use tool, and in addition it provides a high degree of intraobserver reproducibility [8, 9]. Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
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Difference of PC and SM
80
60
40
20
0 500
550
600
Mean of PC and SM Observed average agreement
Fig. 6. Bland-Altman of agreement be-
95% limits of agreement
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y = 0 is the line of perfect average agreement
tween PC and specular microscopy measurements. 20
Difference of SM and UP
0
–20
–40
–60
–80 500
550
600
Mean of SM and UP
Fig. 7. Bland-Altman of agreement be-
tween specular microscopy and UP measurements.
Observed average agreement
However, UP is a manual technique, and thus, the interexaminer reproducibility of this instrument, although suitable, is slightly lower [8, 10]. It also has the disadvantage that the measurements depend on the contact between the cornea and the probe, which may change according to the pressure applied by the operator and can lead to ocular surface distortion [2]. Several studies have shown that the probe can change the thickness of the tear 230
Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
95% limits of agreement
y = 0 is the line of perfect average agreement
film by 7–40 μm and this compression could reduce epithelial thickness, resulting in biases in CCT measurements [2, 11]. Another limitation is the fact that instillation of topical anesthesia is necessary to perform the measurements. Changes in CCT of ±10 μm after topical anesthesia instillation have also been reported [12, 13]. Therefore, new techniques to determine CCT have been developed with the added advantage of evaluating Borrego-Sanz et al.
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16
14
12
10 500
Fig. 8. Regression model of CCT deter-
550
600 PC Fitted values
mined using the specular microscopy and GAT variation.
650
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IOP
parameters useful for clinical practice. For example, PC is used to calculate corneal topography with multiple applications in corneal and refractive surgery, intraocular lens implantation and glaucoma [14, 15]; the LE biometer provides information on keratometry, anterior chamber depth, lens thickness or intraocular lens measurements, and SM, whose substantial properties are endothelial cell counting, is essential in assessing the evolution of certain refractive surgical procedures, such as phakic lens implants, cataract surgery or corneal transplants [1, 3, 6, 16]. In this study we compared the agreement between the CCT measurements obtained using the PC, LE LS 900, UP and SM and analyzed their influence on IOP readings determined by GAT. Today’s gold standard for measur-
ing IOP remains the GAT, although its measurements are conditioned by various morphometric features of the cornea including CCT [17, 18]. Several new IOP measuring instruments have been developed with the express purpose to make measurements less conditioned by corneal factors. However, while much attention has been paid to the method used to determine IOP and its reliability, the influence that the different systems used to measure CCT may have on IOP variations has not been subject to such rigorous validation [19, 20]. In this study, we found that the LE-UP showed the closest agreement, followed by the LE-SM and PC-UP. This was also reported by previously publications. Tai et al. [21], in a study of 184 eyes, also found close agreement between LE and UP. This statement agrees with another study by Beutelspacher et al. [22], who compared CCT measures obtained with OCT, LE, PC and UP showing good agreement. The relatively new LE biometer is a promising noninvasive device with a high reproducibility [23]. A high degree of concordance has been described between the LE and LioMaster regarding to the biometric measurements, although unlike LioMaster, LE has the advantage of measuring additional variables such as the CCT [24]. In previous reports, O’Donnell et al. [3] and Zhao et al. [23] showed good concordance between CCT measurements obtained by PC and LE, although they could not be considered interchangeable in clinical practice. In
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Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
Table 2. Mean difference between the measurements obtained by each pair of methods
Method 1 – method 2 PC-LE PC-SM PC-UP LE-SM LE-UP SM-UP
Mean difference, 95% limits of agreement μm low high 22.3 28.12 15.75 5.82 –6.55 –12.37
–3.09 –4.47 –12.51 –16.32 –21.95 –40.49
47.7 60.71 44.01 27.95 8.85 15.75
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16
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12
10 450
500
Fig. 9. Regression model of CCT deter-
550 LE Fitted values
650
IOP
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mined using the Lenstar biometer and GAT variation.
600
18
16
14
12
10 400
Fig. 10. Regression model of CCT deter-
mined using specular microscopy and GAT variation.
contrast, our study showed a relatively low correlation between these two devices when compared with the high agreement obtained between LE-UP or PC-UP. Additionally, some studies have shown that LE offered lower CCT values than those provided by the PC. This could happen because the CCT is calculated using only one measurement in the case of the PC and LE relies on five measurements on average, leading to biases in measurements [25]. 232
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450
500 SM
550
Fitted values
600
IOP
In spite of the amount of studies showing good correlation between UP and PC measurements, Tai et al. [21] have claimed recently that the mean CCT by PC was 10 μm higher than that obtained using UP [10], which correlates well with our findings, showing significantly higher values in PC measurements. This could be explained because the PC pachymeter may include the precorneal tear film in the measurement of corneal thickness, whereas the UP probe displaces the Borrego-Sanz et al.
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18
16
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12
10 450
500
550 UP Fitted values
Fig. 11. Regression model of CCT deter-
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IOP
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mined using UP and GAT variation.
tear film and compresses the corneal surface, resulting therefore in lower values [21, 26]. On the other hand, it has been widely stated that SM shows lower values of CCT than those obtained by UP and PC in healthy subjects [1, 12, 21]. Nevertheless, good linear correlations between the measurements of the three instruments have been shown in the literature [1]. Furthermore, Almubrad et al. [12] and other authors agree that CCT is significantly underestimated by SM (28.17 ± 19.20 μm) comparing with UP in healthy sub-
jects, so that they could not be considered to be interchangeable [12, 27]. Similar results were also reported by Özlenen-Ucakhan et al. [1] in normal eyes or eyes affected with mild keratoconus. These differences may be due to the different operating principles that guide each device. While SM relies on light reflection, UP depends on sound transmission. Although these authors claim that the reproducibility and repeatability of SM were higher than those achieved with UP, probably this happens because UP is a contact device, operator-dependent and therefore subject to potential biases in the measurements [1, 12, 21, 27]. Surprisingly, in our study we found high correlation in CCT measures between SM-LE and SM-UP, which correlates well with Chaudhry [28], who found no significant differences in the mean CCT values performed with SM and UP. Furthermore, SM proved to be a reliable and reproducible method in pediatric patients with poor cooperation [29]. Besides agreement between the different pachymeter systems, this study was also designed to determine how the use of one or the other pachymetry method might influence IOP measurements made using GAT. Our data revealed that as in previous studies, GAT readings were conditioned by CCT. The amount of variation in GATdetermined IOP due to CCT was greater when this variable was measured by SM than by UP and PC. The lowest variation was found when CCT was measured by LE, in
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Ophthalmologica 2014;231:226–235 DOI: 10.1159/000356724
30
20
10
0 PC
LE
SM
UP
Fig. 12. IOP variation with CCT (regression sum of squares). A
statistically significant difference exists between specular microscopy and Lenstar.
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fact, when analyzing the differences between the amount of IOP variation produced by the different CCT determinations, only a statistically significant difference between SM and LE arose. This could also be explained, because the SM image is reflected at the optical interface between the corneal endothelium and aqueous humor, corneal morphometry appreciably influences the rest of measurements due to light transmission distortion [1, 11, 12]. The pachymetry of choice should be the one that offers accuracy, precision and no need for long measurement time. Our study revealed that LE agreement with SM and UP is excellent and this, added to the ease of its use and its noninvasiveness, results in a very promising tool [23, 30]. Moreover, for LE and SM proper alignment has shown to be easier and less time-consuming than for UP and PC [21]. Nevertheless, our results are limited to a sample of healthy subjects, so future studies are needed to determine whether our findings may be extrapolated to other populations with ophthalmic diseases, such as glaucoma patients, who often show CCT and IOP variation, and
therefore to assess what is the most beneficial option in each case. In conclusion, we can assume that although the CCT values obtained with UP, PC, SM and LE show good correlation, especially measurements between LE-UP and LE-SM, it should be noted that these methods are not completely interchangeable. The amount of IOP variation differs when CCT is determined using LE or SM; no other IOP variation differences arose when comparing the remaining pairs of CCT measurement methods. Acknowledgments Supported in part by Instituto de Salud Carlos III, ‘Red Temática de Investigación Cooperativa, Proyecto RD07/0062: Patología ocular del envejecimiento, calidad visual y calidad de vida’.
Disclosure Statement All authors disclose no conflict of interest in the products, drugs, instruments and pieces of equipment mentioned in this article.
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Copyright: S. Karger AG, Basel 2014. Reproduced with the permission of S. Karger AG, Basel. Further reproduction or distribution (electronic or otherwise) is prohibited without permission from the copyright holder.
