January 2013
Volume 54, Issue 1
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Retina  |   January 2013
Reproducibility of Subfoveal Choroidal Thickness Measurements with Enhanced Depth Imaging by Spectral-Domain Optical Coherence Tomography
Author Affiliations & Notes
  • Lei Shao
    From the Beijing Tongren Eye Center and the
  • Liang Xu
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Chang Xi Chen
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Li Hong Yang
    From the Beijing Tongren Eye Center and the
  • Kui Fang Du
    From the Beijing Tongren Eye Center and the
  • Shuang Wang
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Jin Qiong Zhou
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Ya Xing Wang
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Qi Sheng You
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
  • Jost B. Jonas
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China; and the
    Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University, Heidelberg, Germany.
  • Wen Bin Wei
    From the Beijing Tongren Eye Center and the
  • Corresponding author: Wen Bin Wei, Beijing Tongren Eye Center, Beijing Tongren Hospital, Capital Medical University, 1 Dong Jiao Min Xiang, Dong Cheng District, Beijing, China 100730; wenbing_wei@yahoo.com.cn
Investigative Ophthalmology & Visual Science January 2013, Vol.54, 230-233. doi:10.1167/iovs.12-10351
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      Lei Shao, Liang Xu, Chang Xi Chen, Li Hong Yang, Kui Fang Du, Shuang Wang, Jin Qiong Zhou, Ya Xing Wang, Qi Sheng You, Jost B. Jonas, Wen Bin Wei; Reproducibility of Subfoveal Choroidal Thickness Measurements with Enhanced Depth Imaging by Spectral-Domain Optical Coherence Tomography. Invest. Ophthalmol. Vis. Sci. 2013;54(1):230-233. doi: 10.1167/iovs.12-10351.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose.: To measure the interobserver reproducibility and intra-observer reproducibility of subfoveal choroidal thickness measurements performed by enhanced depth imaging of spectral-domain optical coherence tomography (EDI-OCT) in a population-based setting.

Methods.: The Beijing Eye Study 2011 was a population-based study performed in rural and urban regions of Greater Beijing. The study included 3468 individuals with a mean age of 64.6 ± 9.8 years (range, 5093 years). The participants underwent EDI-OCT and the subfoveal choroidal thickness (SFCT) was measured. To examine the interobserver variability, all images were assessed by two examiners independently of each other within 2 months. To examine the intra-observer reproducibility, a smaller study sample consisting of 21 eyes of 21 healthy subjects from the Tongren Eye Center was included in the study. These latter subjects were scanned 10 times with 1 minute breaks between each examination. The SFCT was measured by the same observer within 2 weeks. The intrasession within subject SD, the coefficient of variation, and the intraclass correlation coefficient (ICC) were calculated.

Results.: EDI-OCTs were performed for 3233 subjects. Mean SFCT measured by grader one and grader two were 254.6 ± 107.3 μm and 253.8 ± 107.4 μm, respectively, with a mean difference of 3.14 ± 13.1 μm (95% confidence interval, 0.0, 24.0). Bland-Altman plot showed 1.9% (61/3233) points outside the 95% limits of agreement. For the assessment of the intra-observer reproducibility, the ICC was 1.00 (P < 0.001, and the mean coefficient of variation was 0.85% ± 1.48%).

Conclusions.: Under routine examination conditions, SFCT measurements by EDI-OCT showed a high intra-observer reproducibility and interobserver reproducibility.

Introduction
The choroids, an integral structure between the sclera and the retina, receives most of the ocular blood flow, and is involved in the pathogenesis of major diseases of the posterior segment of the eye, such as AMD, polypoidal choroidal vasculopathy, central serous chorioretinopathy, and myopic retinopathy. 13 Until recently, the choroid was imaged by sonography, which due to its limited spatial resolution, could deliver only rough information without details. Since the development of optical coherence tomography based enhanced depth imaging (EDI-OCT) by Spaide and colleagues, 46 studies have shown associations between an abnormal choroidal thickness and diseases, such as central serous chorioretinopathy, polypoidal choroidal vasculopathy, and myopic retinopathy. 79 These studies have suggested that measurement of choroidal thickness by EDI-OCT has become a promising new method in clinical ophthalmology. Since EDI-OCT is a new technique, one has to know its reproducibility to be able to interpret measurements. We, therefore, conducted this study to assess the interobserver reproducibility and the intra-observer reproducibility of the technique. 
Methods
The Beijing Eye Study 2011 is a population-based, cross-sectional study in Northern China. 1012 The Medical Ethics Committee of the Beijing Tongren Hospital had approved the study protocol, all participants had given informed consent, and this study was performed according to the tenants of the Declaration of Helsinki. It was carried out in five communities in the urban district of Haidian in the North of Central Beijing and in three communities in the village area of Yufa of the Daxing District south of Beijing. The only eligibility criterion for inclusion into the study was an age of 50+ years. In 2011, the eight communities had a total population of 4403 individuals aged 50 years or older. In total, 3468 individuals (1963 [56.6%] were women) participated in the eye examination, corresponding to an overall response rate of 78.8%. The study was divided into a rural part (1633 [47.1%] subjects; 943 [57.7%] were women) and an urban part (1835 [52.9%] subjects; 1020 [55.6%] were women). The mean age was 64.6 ± 9.8 years (median, 64 years; range, 50–93 years). 
All examinations were carried out in the communities, either in schoolhouses or in community houses. All study participants underwent an interview with standardized questions on their family status, level of education, income, quality of life, psychic depression, physical activity, known major systemic diseases, such as arterial hypertension and diabetes mellitus, and quality of vision. Fasting blood samples were taken for measurement of blood lipids, glucose, and glycosylated hemoglobin HbA1c. Blood pressure was measured. Body height and weight, and the circumference of the waist and hip were recorded. The ophthalmic examination included measurement of presenting visual acuity, uncorrected visual acuity, and best corrected visual acuity, tonometry, slit lamp examination of the anterior segment, optical low-coherence reflectometry (Lensstar 900 Optical Biometer; Haag-Streit, Koeniz, Switzerland) for biometry and digital photography of the cornea, lens, macula, and optic disc. 
Subfoveal choroidal thickness (SFCT) was measured using a spectral domain optical coherence tomography (SD-OCT; Spectralis, Wavelength: 870nm; Heidelberg Engineering Co., Heidelberg, Germany) with enhanced depth imaging (EDI) modality (Fig. 1) after pupil dilation. 12 Seven sections, each comprising 100 averaged scans, were obtained in an angle of 5° to 30° rectangle centered onto the fovea. The horizontal section running through the center of the fovea was selected for further analysis. SFCT was defined as the vertical distance from the hyperreflective line of the Bruch's membrane to the hyperreflective line of the inner surface of the sclera. The measurements were performed using the Heidelberg Eye Explorer software (version 5.3.3.0; Heidelberg Engineering Co.). Only the right eye of each study participant was assessed. The images were taken by one technician (CXC) and the images were assessed in a masked manner by two ophthalmologists (LS, KFD). The quality of the scans was assessed prior to the analysis and poor quality scans were rejected and repeated. The technique was described in detail recently. 12  
Figure 1. 
 
Optical coherence tomogram (enhanced depth imaging) of the retina and the choroid. Red line: Line of measurements of the SFCT.
Figure 1. 
 
Optical coherence tomogram (enhanced depth imaging) of the retina and the choroid. Red line: Line of measurements of the SFCT.
The intra-observer reproducibility was examined in a considerably smaller study group consisting of 21 healthy volunteers with no known eye disease (10 men; mean age, 63.1 ± 10.6 years; range, 50–83 years), who did not participate in the Beijing Eye Study, who were recruited from the Tongren Eye Center and who were scanned 10 times with 1 minute breaks between each measurement. The right eye of each subject was selected for the EDI-OCT analysis. The SFCT was measured in a masked manner by the same observer (LS) within 2 weeks. 
Statistical analysis was performed using a commercially available statistical software package (SPSS for Windows, version 20.0; IBM-SPSS, Chicago, IL). For the interobserver study, the average of SFCT measurements obtained from both visits was compared by paired t-tests. Bland-Altman plot was used to visualize the interobserver agreement between the two observers. The intra-observer reproducibility was measured with 10 EDI-OCT images obtained from the 21 volunteers. We calculated the intra-session within subject SD (Sw), the coefficient of variation (COV, 100% × Sw/overall mean), and the intraclass correlation coefficient (ICC). Almost perfect reliability was defined as an ICC greater than 0.80. 95% confidence intervals (CI) were presented. All P values were two-sided and were considered statistically significant when the values were less than 0.05. 
Results
Out of the 3468 participants, SFCT measurements were available for 3233 (93.2%) subjects (1818 [56.2%] were women). The mean age was 64.3 ± 9.6 years (median, 63 years; range, 50–93 years), the mean refractive error (spherical equivalent) was −0.18 ± 1.98 diopters (D; median, 0.25 D; range, −20.0 to +7.00 D) (Table 1). For 235 (6.8%) eyes, OCT images could not be examined either because images were not taken or because available images could not be assessed due to severe lens opacities or vitreous clouding. The group of subjects without SFCT measurements as compared with the group of subjects with SFCT measurements was significantly (P < 0.001) older (69.6 ± 10.9 years vs. 64.3 ± 9.6 years), more myopic (1.44 ± 4.75 D vs. −0.16 ± 2.02 D; P = 0.007), and did not vary significantly in sex (P = 0.12). 
Table 1. 
 
Demographic and Ophthalmologic Data (mean ± SD) of Study Participants
Table 1. 
 
Demographic and Ophthalmologic Data (mean ± SD) of Study Participants
Variable Value Range
Age, y 54.3 ± 9.6 50 to 93
Sex, male/female 1415/1818
Height, cm 162.0 ± 8.1 130.0 to 188.0
Weight, kg 67.0 ± 11.7 33.0 to 120.0
Refractive error, D −0.18 ± 1.98 −20.00 to +7.00
Axial length, mm 23.24 ± 1.11 18.96 to 30.88
IOP, mm Hg 14.5 ± 2.7 6.0 to 32.0
The correlation coefficient of the association between the measurements performed independently by the two examiners was r = 0.99 (Fig. 2), indicating a high interobserver agreement. The mean SFCT was 254.6 ± 107.3 and 253.8 ± 107.4 μm for the first examination and the second examination of the OCT images, respectively, with a mean difference of 3.14 ± 13.1 μm (P = 0.001; 95% CI: 0.0, 24.0). The Bland-Altman plot showed that 1.9% (61/3233) of the points was located outside of the 95% limits of agreement (Fig. 3). Stratifying the study population by age or by refractive error, similar results were obtained (Tables 2, 3). As reported previously, 12 the SFCT decreased with older age and increasing myopia (Tables 2, 3). The data for the reproducibility did not differ markedly between the various age groups and the various refractive error groups (Tables 2, 3). 
Figure 2. 
 
Scatter plot showing the correlation between the subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other.
Figure 2. 
 
Scatter plot showing the correlation between the subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other.
Figure 3. 
 
Bland-Altman plot of subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other. X-axial defined as mean of the SFCT measurement with observer one and observer two. Y-axial defined as the average SFCT by observer one minus the SFCT by observer two. The mean differences and the 95% confidence limits of the bias are shown as three dotted lines.
Figure 3. 
 
Bland-Altman plot of subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other. X-axial defined as mean of the SFCT measurement with observer one and observer two. Y-axial defined as the average SFCT by observer one minus the SFCT by observer two. The mean differences and the 95% confidence limits of the bias are shown as three dotted lines.
Table 2. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Age of Study Participants
Table 2. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Age of Study Participants
Age Group, y SFCT (Mean ± SD), μm; Exam 1 SFCT (Mean ± SD), μm; Exam 2 Correlation Coefficient, r P Value Mean Difference Exam 1 to 2
50 to 59 1244 301.6 ± 96.9 300.5 ± 97.4 0.980 <0.001 1.08
60 to 69 937 258.5 ± 97.8 257.7 ± 98.0 0.996 <0.001 0.78
70 to 79 836 204.1 ± 99.1 203.5 ± 99.2 0.998 <0.001 0.59
≥80 216 161.7 ± 86.2 161.6 ± 85.3 0.997 <0.001 0.11
Table 3. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Refractive Error
Table 3. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Refractive Error
Refractive Error, D SFCT (Mean ± SD); Exam 1 SFCT (Mean ± SD); Exam 2 Correlation, r P Value Mean Difference Exam 1 to 2
Refractive data not available 49 197.6 ± 92.4 196.8 ± 92.5 0.998 <0.001 0.76
<−1.00 789 211.3 ± 112.3 211.0 ± 113.7 0.985 <0.001 0.25
−1.00 to 1.00 1422 272.0 ± 98.5 271.0 ± 98.3 0.994 <0.001 1.05
>1.00 973 267.0 ± 105.6 266.1 ± 105.2 0.995 <0.001 0.90
To assess the intra-observer reproducibility, the images of 21 healthy volunteers (11 [52%] were women) with no known eye disease were re-examined. The mean age was 63.1 ± 10.6 years (median, 61 years; range, 50–83 years). Uncorrected visual acuity was equal to or higher than 1.0. The analysis of the intra-observer variability revealed an ICC of 1.00 (P < 0.001). The mean coefficient of variation was 0.85% ± 1.48%. 
Discussion
Enhanced depth imaging by optical coherence tomography allows visualization of the posterior choroids, and has opened up a new avenue for the examination of the choroids, and for the diagnosis of retinal and choroidal diseases. 49 Previous studies have revealed abnormally high SFCT measurements in patients with central serous chorioretinopathy in the affected eyes as well as in the contralateral, clinically unaffected eyes. 6,1315 In a similar manner, patients with polypoidal choroidal vasculopathy have been described to have an increased thickness of the subfoveal choroid. 13,16,17 Other investigations examining the choroidal thickness in normal subjects and in patients with glaucoma and other retinal disorders, showed that choroidal thickness significantly decreases with older age, longer axial length, female sex, less anterior chamber depth, thinner lens, steeper corneas, and lower best corrected visual acuity. 1822 The major part of the basis for the interpretation and the clinical validity of these choroidal thickness measurements is the reproducibility of the technique. The results of our study show that under routine examination conditions, the variability between two examiners in measuring SFCT was low (Figs. 2, 3). The same results were obtained if the study population was stratified by age or by refractive error (Tables 2, 3). As a corollary, the intra-observer reproducibility of repeatedly performed measurements was high with a coefficient of variation of 0.85%. 
Our results obtained in a relatively large population-based study agree with the findings by Spaide and colleagues, 4 who studied the interobserver reproducibility of EDI-OCT with 17 healthy subjects, and who reported on high correlations between the measurements performed by independent observers (correlation coefficient r = 0.93 [right eye]; r = 0.97 [left eye]). In our study, the correlation coefficient was (r = 0.99) (Fig. 2). Our study, thus, extends the results of the study by Spaide and colleagues 4 onto a wider age range and a considerably larger study population, with the reproducibility tested under routine examination conditions. In another study, Rahman and coworkers 23 reported a good interobserver and intra-observer reproducibility of the choroidal thickness measurements by EDI-OCT. Their study revealed that a change of more than 32 μm in SFCT was likely to exceed the inter-observer variability. The Bland-Altman plot in our study (Fig. 3) showed that only 1.9% (61/3233) measurement points were located outside of the 95% limits of agreement. The mean difference between two observers was 3.14 ± 13.1 μm what is markedly lower than the value of 32 μm in the investigation by Rahman and colleagues. 23 Both studies agree that reproducible SFCT measurements can be obtained by EDI-OCT. The results of our study also agree with the study by Ikuno and colleagues, 24 who examined 24 eyes of 12 healthy volunteers and found an interexaminer ICC reproducibility value of 0.97. The intervisit ICC value, assessed by examining 10 of the volunteers 4 months later, was 0.89. Our study also agrees with the investigation by Branchini and coworkers 25 who reported on an interobserver correlation of SFCT measurements of 0.96. The highest value for the difference in the measurements between the two examiners was 488 μm. The reason why the range of the parameter was so high may be the composition of the study population. Since the Beijing Eye Study 2011 included normal subjects and patients with diseases such as myopic retinopathy, which are associated with a marked change in choroidal thickness and other structural abnormalities, so that it might have been difficult to delineate the choroidal boundaries. 
Potential limitations of our study should be mentioned. First, as a population-based study, our investigation included mostly healthy subjects, while patients with retinal or choroidal diseases formed a minor part of the study population. Under clinical conditions, however, mostly patients are examined. Second, from the aspect of a population-based study, a concern is nonparticipation. The Beijing Eye Study 2011 had, however, a reasonable response rate of 78.8%, and above all, it may be unlikely, that a selection artifact in the study population may have influenced the results of the reproducibility of choroidal thickness measurements. Third, previous studies by Chakraborty and colleagues 26 and others have shown a circadian (diurnal) rhythm of approximately a 20- to 30-μm change in choroidal thickness measurements by EDI-OCT. 2729 The re-examinations in our study were performed at the same time of the day, so that the potentially physiological variations in choroidal thickness have to be added to the variations due to the measurement technique, if re-examinations are performed at different times of the day. 
In conclusion, our study showed a relatively high intra-observer reproducibility and interobserver reproducibility of SFCT measurements by EDI-OCT. Future studies may address whether disease related changes in SFCT are larger than the inaccuracy by the measurement technique. 
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Footnotes
 Supported by grants from the State Natural Sciences Fund (81041018) and the Natural Sciences Fund of Beijing government (7092021, 7112031).
Footnotes
 Disclosure: L. Shao, None; L. Xu, None; C.X. Chen, None; L.H. Yang, None; K.F. Du, None; S. Wang, None; J.Q. Zhou, None; Y.X. Wang, None; Q.S. You, None; J.B. Jonas, None; W.B. Wei, None
Figure 1. 
 
Optical coherence tomogram (enhanced depth imaging) of the retina and the choroid. Red line: Line of measurements of the SFCT.
Figure 1. 
 
Optical coherence tomogram (enhanced depth imaging) of the retina and the choroid. Red line: Line of measurements of the SFCT.
Figure 2. 
 
Scatter plot showing the correlation between the subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other.
Figure 2. 
 
Scatter plot showing the correlation between the subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other.
Figure 3. 
 
Bland-Altman plot of subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other. X-axial defined as mean of the SFCT measurement with observer one and observer two. Y-axial defined as the average SFCT by observer one minus the SFCT by observer two. The mean differences and the 95% confidence limits of the bias are shown as three dotted lines.
Figure 3. 
 
Bland-Altman plot of subfoveal choroidal thickness measurements performed on optical coherence tomograms by two examiners independently of each other. X-axial defined as mean of the SFCT measurement with observer one and observer two. Y-axial defined as the average SFCT by observer one minus the SFCT by observer two. The mean differences and the 95% confidence limits of the bias are shown as three dotted lines.
Table 1. 
 
Demographic and Ophthalmologic Data (mean ± SD) of Study Participants
Table 1. 
 
Demographic and Ophthalmologic Data (mean ± SD) of Study Participants
Variable Value Range
Age, y 54.3 ± 9.6 50 to 93
Sex, male/female 1415/1818
Height, cm 162.0 ± 8.1 130.0 to 188.0
Weight, kg 67.0 ± 11.7 33.0 to 120.0
Refractive error, D −0.18 ± 1.98 −20.00 to +7.00
Axial length, mm 23.24 ± 1.11 18.96 to 30.88
IOP, mm Hg 14.5 ± 2.7 6.0 to 32.0
Table 2. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Age of Study Participants
Table 2. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Age of Study Participants
Age Group, y SFCT (Mean ± SD), μm; Exam 1 SFCT (Mean ± SD), μm; Exam 2 Correlation Coefficient, r P Value Mean Difference Exam 1 to 2
50 to 59 1244 301.6 ± 96.9 300.5 ± 97.4 0.980 <0.001 1.08
60 to 69 937 258.5 ± 97.8 257.7 ± 98.0 0.996 <0.001 0.78
70 to 79 836 204.1 ± 99.1 203.5 ± 99.2 0.998 <0.001 0.59
≥80 216 161.7 ± 86.2 161.6 ± 85.3 0.997 <0.001 0.11
Table 3. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Refractive Error
Table 3. 
 
Reproducibility of SFCT by Two Masked Examiners, Stratified by Refractive Error
Refractive Error, D SFCT (Mean ± SD); Exam 1 SFCT (Mean ± SD); Exam 2 Correlation, r P Value Mean Difference Exam 1 to 2
Refractive data not available 49 197.6 ± 92.4 196.8 ± 92.5 0.998 <0.001 0.76
<−1.00 789 211.3 ± 112.3 211.0 ± 113.7 0.985 <0.001 0.25
−1.00 to 1.00 1422 272.0 ± 98.5 271.0 ± 98.3 0.994 <0.001 1.05
>1.00 973 267.0 ± 105.6 266.1 ± 105.2 0.995 <0.001 0.90
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