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Year : 2017  |  Volume : 4  |  Issue : 2  |  Page : 31-36

Correlation between retinal and choroidal thickness in normal emmetropes

Department of Ophthalmology, Faculty of Medicine, University of Alexandria, Alexandria, Egypt

Date of Web Publication17-Nov-2017

Correspondence Address:
Amir Ramadan Gomaa
Department of Ophthalmology, Faculty of Medicine, University of Alexandria, Khartoum Square, Alexandria 21523
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/erj.erj_12_17

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Context: An objective and quantitative analysis of the normal choroid and retina relation is required for a better understanding of changes that occur in retinal and choroidal diseases. Aims: This study aimed to evaluate choroidal thickness (CT) and corresponding retinal thickness (RT) using enhanced depth imaging mode of spectral-domain optical coherence tomography (SD-OCT) in normal emmetropic eyes. Methods: One hundred and six eyes of healthy, nearly emmetropic eyes of volunteers were examined by Spectralis OCT. Manual measurements of CT were done under the fovea and on the vertical and horizontal line scans at the ETDRS 1 and 3 mm circles. RT was measured in the center foveal subfield and at the same locations of CT measurements. Statistical Analysis Used: Data were analyzed using IBM SPSS software package version 20.0 (SPSS, Inc., Chicago, IL, USA). Results: With a mean age of 50.3 ± 16.5 years, the mean subfoveal choroidal thickness (SCT) was 297.5 ± 86.2 μ while the mean central RT was 264.3 ± 15.9 μ. The mean CT was thinnest at the nasal location but without statistical significance and SCT was higher in males than females. Significant and correlated age-related thinning was observed in both retina and choroid at all locations, except the fovea, where these changes were significant but not correlated. Conclusions: CT has an age-related thinning pattern that correlates with age-related retinal thinning in extrafoveal macular locations. In addition, age can be used as a guide in predicting the normal SCT in emmetropes.

Keywords: Choroidal thickness, enhanced-depth imaging, optical coherence tomography

How to cite this article:
Gomaa AR. Correlation between retinal and choroidal thickness in normal emmetropes. Egypt Retina J 2017;4:31-6

How to cite this URL:
Gomaa AR. Correlation between retinal and choroidal thickness in normal emmetropes. Egypt Retina J [serial online] 2017 [cited 2021 Jun 21];4:31-6. Available from: https://www.egyptretinaj.com/text.asp?2017/4/2/31/218584

  Introduction Top

The choroid is a versatile tissue in the eye. Although its major role is to provide oxygen and nutrition to the photoreceptors, this is not its only function.[1] Other functions include thermoregulation, adjusting retinal position, regulating intraocular pressure, secreting growth factors, and sharing in the drainage of aqueous humor.[2],[3],[4],[5],[6],[7]

The vascular components of the choroid are arranged in 3 layers beginning from inside by the choriocapillaris followed by Haller's then Sattler's layers.[8]

As the choroid is mainly a vascular layer, it is usually affected in ischemic lesions as Elschnig spots and vascular diseases as polypoidal vasculopathy and central serous chorioretinopathy.[9] Aging processes as age-related macular degeneration also cause choroid changes and so does inflammatory diseases.[10],[11]

Choroidal thickness (CT) can vary in the same person during different times of the day as it is affected by intraocular pressure and perfusion pressure.[12] In addition, it could be affected by age, refractive error, and ethnicity.[13],[14]

Older methods of choroidal evaluation as fluorescein angiography, indocyanine green angiography or ultrasonography [15] cannot provide cross-sectional anatomical details of choroidal pathologies.[16] This created a need for an objective and quantitative method for choroidal analyses.

An accurate measurement of CT became possible with the recently developed spectral-domain optical coherence tomography (SD-OCT).[17] However, measurement reliability was limited by light scattering from the retinal pigment epithelium (RPE) and by decreased sensitivity with increased displacement from the zero-delay line, which is normally positioned at the posterior vitreous.[18]

The image of the choroid can be enhanced by the technique of enhanced depth imaging (EDI-OCT), which places the choroid closer to the zero-delay line, through moving the OCT device closer to the eye.[18]

This work aimed to study CT measurements by EDI-OCT in healthy emmetropic individuals and to correlate it with corresponding retinal thickness.

  Methods Top

This study was performed at Ophthalmology department of Alexandria main University hospital on healthy Egyptian volunteers. This study was approved by the ethics committee and conformed to the tenets of the Declaration of Helsinki. Written and informed consent was obtained from all participants, and full ophthalmological examination was gone to exclude any ocular pathology.

Examination included measurement of best corrected visual acuity using LogMAR chart at a distance of 4 m, intraocular pressure measurement using Goldmann applanation tonometer, anterior segment examination by slit lamp and fundus examination by slit lamp biomicroscopy. Autorefraction was done for all participants using Topcon RM-800 autorefractometer.

Participants with any of the following criteria were excluded; diabetes mellitus, glaucoma, uveitis, macular lesions, retinal vascular diseases, media opacity, spherical equivalent more than +1 or −1 diopter and previous ocular surgery apart from cataract surgery of more than 6 months.

A horizontal and vertical 30° line scans centered on the fovea were obtained using a SD-OCT (Spectralis, Heidelberg Engineering, Heidelberg, Germany) with EDI modality after pupil dilation. To maximize the signal-to-noise ratio and ensure high-quality images, we used the automatic real-time averaging and eye tracking features and each scan comprised 100 averaged scans. Only scans with a signal-to-noise ratio >18 dB were used for analysis.

CT was manually measured in separate lines extending from the outer border of the hyperreflective line, corresponding to the RPE, to the line corresponding to the choroid-scleral interface (CSI). The CSI was determined qualitatively as the inner surface of the sclera.[19] Measurements were done subfoveally and at the 1 and 3 mm locations on the ETDRS circle in the 4 main directions; nasal, temporal, superior, and inferior.

Care was taken to draw the lines perpendicular to the tangential to the retinal contour at each measuring location. Furthermore, all OCT scans were performed at standardized time so as to minimize the effect of diurnal variation on choroidal thickness, which was described in earlier studies.[17],[20] Retinal thickness (RT) was manually measured at the same location of CT measurements on the 2-line scans. RT of central 1-mm region was obtained from Spectralis OCT macular map.

Statistical analysis of the data

Data were fed to the computer and analyzed using IBM SPSS software package version 20.0 (SPSS, Inc., Chicago, IL, USA). The Kolmogorov–Smirnov test was used to verify the normality of distribution of variables, Student's t-test was used to compare two groups for normally distributed quantitative variables while analysis of variance was used for comparing the multiple studied groups. Pearson coefficient was used to correlate between quantitative variables. Multiple regression analysis was performed to explore independent associated factors. The significance of the obtained results was judged at the 5% level.

  Results Top

Using epi Info ® sample size calculator and accepting 5% margin of error in our estimate, we calculated a sample size of 100 eyes of patients attending our institute to be sufficient to achieve a study power 80% with a confidence level of 95% to estimate mean population choroidal thickness.

Based on this calculation, 106 eyes were selected for our study; 49 (46.2%) belonged to males while 57 (53.8%) belonged to females. Age ranged from 18 to 79 years (range = 61 years), mean age was 50.32 ± 16.57 years.

Mean age of males was 47.9 ± 16 years and mean age of females was 52.4 ± 16.8 years. Thirty eyes belonged to patients between 20 and 40 years, 40 eyes belonged to patients between 40 and 60 years and 36 eyes belonged to patients between 60 and 80 years.

Mean logMAR BCVA was 0.02 ± 0.03 with median of 0.00 and min–max (0.0–0.10). Mean subfoveal CT (SCT) was 297.5 ± 86.2 μ while mean central RT (CRT) was 264.3 ± 15.9 μ.

The distribution of clinical findings according to sex is presented in [Table 1]. There was a significant difference between sex in mean SCT (t = 2.010 P = 0.047) but not in mean CRT (t = 1.053 P = 0.295).
Table 1: Distribution of clinical findings according to sex

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The values of choroidal and RT according to location are presented in [Table 2] and [Figure 1] and [Figure 2]. Both CT and RT measurements in each of the 4 directions were averaged from the readings at the1 mm and 3 mm circles and presented as a single value. There was no significant difference in the CT measurements in the 5 locations although the nasal location was the thinnest (F = 0.924, P = 0.450). As for the RT, it was significantly thinner in the fovea than the other 4 locations (F = 267.268, P < 0.0001).
Table 2: Mean values of choroidal and retinal thickness according to location

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Figure 1: Distribution of means of choroidal thickness according to location

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Figure 2: Distribution of means of retinal thickness according to location

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There was a significant difference between age groups in mean SCT (F = 31.8 P = 0.000) but not in mean CRT (F = 1.275 P = 0.284) as shown in [Table 3].
Table 3: Mean values of subfoveal choroidal thickness and central retinal thickness according to age group

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There was a highly significant main effect of age groups on mean CT (F = 144.6, P < 0.0001) while adjusting for anatomical location. Pair-wise comparisons did not detect significant mean difference between subfoveal anatomical location and all other locations. There was also a highly significant main effect of age groups on mean RT (F = 85.4, P < 0.0001) while adjusting for anatomical location. Pair-wise comparison revealed a highly significant mean difference between central retinal anatomical location and all other locations. P < 0.0001 [Table 4] and [Figure 3], [Figure 4]. In our cases, both CT and RT at the 4 noncentral locations and the SCT showed significant changes with age.
Table 4: Mean values of choroidal thickness and retinal thickness at various locations according to age group

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Figure 3: Distribution of means of choroidal thickness at various locations according to age groups

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Figure 4: Distribution of means of retinal thickness at various locations according to age groups

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There was a highly significant moderate negative linear relationship between SCT and age (r = −0.627, P < 0.0001). There was also a significant but weak negative linear relationship between CRT and age (r = −0.213, P = 0.028) [Figure 5] and [Figure 6].
Figure 5: Correlation between subfoveal choroidal thickness and age

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Figure 6: Correlation between central retinal thickness and age

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No significant linear relationship was detected between SCT and CRT (r = 0.144, P = 0.141). On the other hand, there was a highly significant moderate positive linear relationship between CT and RT at all extrafoveal locations; temporal CT and temporal RT (r = 0.37, P < 0.001). Nasal CT and nasal RT (r = 0.31 P = 0.001), superior CT and superior RT (r = 0.294 P = 0.002) inferior CT and inferior RT (r = 0.27 P = 0.005).

Overall model using age as predictor for SCT was highly statistically significant (F = 33.33, P = < 0.0001) age (t = −7.766, P < 0.0001) explains 39.3% of variability of SCT.

Regression model: SCT = 461.6–3.26 (age). The estimated rate of change of conditional mean of SCT with respect to age was −3.26 μ (−57.3, −5.9) 95% confidence interval.

Overall model using age as predictor for CRT was not found to be statistically significant (F = 2.526, P = 0.085) age explains only 4.5% of the variability of CRT.

Regression model: CRT = 274.6–0.193 (age).

  Discussion Top

CT measurements can be obtained with either SD-OCT or swept source-OCT and values obtained by both are significantly correlated.[21] Spectralis OCT, which was used in our study, was reported to be superior to the cirrus HD-OCT due to its eye-tracking ability and the 100 B-scans averaging versus the 20 B-scans of the Cirrus HD-OCT.[22],[23]

CT varies with axial length and refractive error and many studies had reported a progressive decrease in CT with increasing severity of myopia.[24],[25],[26] Therefore, we limited our selection to individuals with spherical equivalent from −1 to +1 diopters to minimize the effects of change in refraction on CT.

Defining CSI could be challenging. Only 60% of subjects in a study by Gupta et al. had a well-delineated CSI that allowed good measurements.[19] Although most choroidal imaging is currently performed manually, there is a high intervisit, interobserver and intermachine agreement among the available SD-OCT devices.[22],[23]

The normal SCT showed a wide range of variation among studies. The mean age in our group was 50.32 ± 16.57 years, and the mean SCT was 297.5 ± 86.2 μ while mean CRT was 264.3 ± 15.9 μ.

Our SCT results were slightly higher than values reported on the same age group as in Margolis and Spaide study (287 ± 76 with an average age of 50.4 years) and Ding et al. study (261.93 ± 88.42 μ with a mean age of 50 years).[13],[27] In contrast, studies with mean age around 40 years showed a much greater thickness as seen in Ikuno et al. study (354 ± 111 μ).[28]

Egyptian population was evaluated in 2 studies. In the first by Moussa et al.[29] mean SCT was 319.72 ± 76.45 μm for the line measurements. Their higher values were explained by using swept source SSOCT and due to their younger mean age (36.8 years). In the second study by Abdellatif,[30] eyes were stratified into 3 age groups. The SCT was highest in individuals between 20 and 40 years (337.23 ± 37.51 μm) and lowest in individuals between 60 and 80 years (270.24 ± 22.37 μm).

No significant statistical difference in thickness was found in our cases between different locations, although the mean CT was thinner at the nasal location. In Tan et al., Moussa et al. and Hirata et al. studies, the nasal choroid was also the thinnest.[20],[29],[31] Ouyang et al.[32] proposed that choroidal watershed and fetal choroidal fissure were the reasons for relative choroidal thinning nasally and inferiorly. In the majority of other studies,[13],[28],[32] the choroid was thickest under the fovea. Lack of consistency in choosing the measuring locations might be an explanation for these discrepancies between studies. In our analysis, we used the mean of the 1 and 3 mm locations in each direction. This might have contributed to decreasing the location-dependent variability in thickness.

In our study, only the fovea was significantly thinner that the rest of the retina (264.26 ± 15.92). The next thinnest location was the temporal retina. Our results were similar to Natung et al. study,[33] in which the macular was thinnest at the fovea, thickest at the nasal subfield, followed by the superior, inferior, and temporal subfields. They were also consistent with Appukuttan and Adhi studies.[34],[35] The increased thickness in the nasal retina can be explained by the increased thickness of the nerve fiber layer nasally.

Analysis by sex in our group showed a significantly higher SCT in males (315.45 ± 91.64 μ) than females (282.18 ± 78.85 μ) but no difference in CRT between males (266.02 ± 16.78 μ) and females (262.75 ± 15.14 μ).

Gender might play a role in choroidal thickness, although literature reports had shown contradicting results. While Tan et al.[20] and Moussa et al.[29] found no significant differences in CT between sex, men in Li et al.[36] study on young adults (mean age 24.9 years) had a thicker choroid compared with women after adjusting for axial length. The difference in hormonal exposure was a likely biological explanation.

As the choroid is a highly vascular tissue, it may show structural and functional alterations with aging.[37] In our study, both CT and RT in the 4 noncentral locations showed significant thinning in older age groups. As for the central location, there was significant thinning in older age groups in SCT but not in CRT. Chhablani et al.[38] also reported a negative correlation of age with CT at all locations while Moussa et al.[29] detected a significant negative correlation between CT and age in all subfields except the nasal subfields which were already thin in all ages.

Although correlations in our cases, between age and each of SCT and CRT was negative and significant, the relationship was moderate for SCT (r = -0.627, r2 = 0.39) and weak for CRT (r = -0.213, r2 = 0.04). Because CT is affected by many factors other than age, it may be difficult to attribute changes only to age. This was revealed in a number studies [28],[30],[31] including ours, where the correlation of SCT with age was negative but moderate.

In our study, age was a significant predictor for SCT as it explained 39.3% of its variability with a rate of change of-3.26 μ per year. Many studied had reported and calculated an age-related choroidal thinning in healthy eyes.[39] The reported rate of thinning varied from 1.18 μm/year by Chhablani et al.[38] and 1.56/year by Margolis and Spaide [13] up to 4 μm/year by Wei et al.[40] Other studies showed variability in the pattern of choroidal thinning with age. Both Ding et al.[27] and Abdellatif [30] claimed that thinning occurs only above 60 years. In contrast, Kim et al.[41] reported choroidal thinning only in subjects younger than 60 years. Kim postulated that CT decreases significantly with advancing age until the age of 60 years. Past this age, age-related choroidal atrophy masks statistical significance. These findings imply that choroidal thinning rate with age is a dynamic and not a fixed process.

In contrast, age in our group was not a significant predictor for CRT as it explained only 4.5% of its variability and caused CRT thinning by only −0.19 μ/year. Our results were in agreement with multiple studies that reported no association between macular thickness and age.[35],[42]

Alamouti and Funk showed that 80% of thinning in RT over time was caused by shrinkage of the retinal nerve fiber layer (RNFL) and that age-related changes of actual retinal tissue were very small (0.09 μ per year).[43] Furthermore, Sung et al. found that macular thickness decreased with age in the outer sectors, but not in the foveal center and that the loss corresponded with the loss in the RNFL. They concluded that central fovea, which is devoid of the RNFL remains stable throughout life as the majority of the thinning was due to age-related ganglion cell axonal loss with thinning of the RNFL.[44]

The limitations of our study include manual segmentation bias, the relatively small number of eyes studied and evaluating thickness at only 2 subfoveal lines.

  Conclusions Top

In healthy emmetropic eyes, age results in corresponding thinning of both retina and choroid in extrafoveal macular locations, while in the foveal area, the retina in relatively resistant to age-related thinning compared to subfoveal choroid. Furthermore, age can be used as a guide in predicting the normal SCT in emmetropes.

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Conflicts of interest

There are no conflicts of interest.

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]

  [Table 1], [Table 2], [Table 3], [Table 4]

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