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ORIGINAL ARTICLE
Year : 2017  |  Volume : 4  |  Issue : 1  |  Page : 1-5

Changes in subfoveal choroidal thickness in diabetic macular edema


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

Date of Web Publication20-Apr-2017

Correspondence Address:
Haitham Younis Al-Nashar
Department of Ophthalmology, Faculty of Medicine, Zagazig University, Zagazig
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/erj.erj_14_16

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  Abstract 

Purpose: The objective of this study is to detect the changes in subfoveal choroidal thickness (SFCT) in eyes with diabetic macular edema (DME) with the use of enhanced depth imaging optical coherence tomography (EDI-OCT). Patients and Methods: One hundred and eighty eyes were included in this prospective nonrandomized study. They were divided into three groups, each including sixty eyes; Group I with patients with DME, Group II included diabetic patients without maculopathy, and Group III were normal persons. All eyes were examined with fluorescein angiography to detect the retinopathy stage, and all eyes were examined by EDI spectral domain-OCT to measure the thickness of the choroid. Central macular thickness (CMT) and best-corrected visual acuity (BCVA) were measured in all groups to find the correlation between them and SFCT. Results: The SFCT was significantly decreased in DME group (215.12 5.6 μm) compared with the other two groups (in Group II, it was 253.1 9.3 μm and in Group III, it was 255.93 9.2 μm) (P < 0.001). A negative correlation (r = −0.6) was detected between CMT and SFCT in patients with DME while no correlation between them was found in other two groups (in Group II, r = 0.17 and Group III, r = 0.2). A significant correlation (r = 0.5) was observed between BCVA and SFCT in Group I, while in other two groups, no correlation between the two measures was detected (in Group II, r = −0.1 and Group III, r = −0.1). Conclusion: In eyes with DME, there is a choroidal thinning on EDI OCT. There is a negative correlation between SFCT and CMT in eyes with DME.

Keywords: Choroidal thickness, deep enhanced image, diabetic retinopathy


How to cite this article:
Al-Nashar HY. Changes in subfoveal choroidal thickness in diabetic macular edema. Egypt Retina J 2017;4:1-5

How to cite this URL:
Al-Nashar HY. Changes in subfoveal choroidal thickness in diabetic macular edema. Egypt Retina J [serial online] 2017 [cited 2017 Jun 23];4:1-5. Available from: http://www.egyptretinaj.com/text.asp?2017/4/1/1/204836


  Introduction Top


The disturbance in both outer and inner blood-retinal barriers functions is the main cause of diabetic macular edema (DME) with subsequent accumulation of sub- and intra-retinal fluid.[1]

The choroid has an important function in the physiological and metabolic functions of the normal eyes as most of the ocular perfusion, and blood flow is coming from the choroidal blood vessels, so the evaluation of the changes that may occur in the choroidal vasculature is important for understanding the different diseases affecting the retina.[2],[3]

Many studies showed that the choroid has an important role in the pathogenesis and pathological changes that occur in diabetic retinopathy.[4] Many histological changes are seen in the choroid in diabetic eyes. Localized dilatation of choroidal vessels with increased tortuosity may be seen in diabetic choroid, also the presence of poor vascular perfusion and microaneurysms are also detected in the choroid of diabetic eyes.[5],[6]

The metabolic functions of the fovea are dependent mainly on the choroidal vasculature and perfusion as the fovea is lacking of retinal blood vessels.[7],[8] Hence, the impairment of the choroidal vasculature may cause distortions in the functions of the fovea.[9]

Recently, the spectral domain-optical coherence tomography (SD-OCT) instrument may be used to allow better choroidal visualization and imaging.[10] Enhanced depth imaging (EDI) technique is used in SD-OCT for deeper imaging of the choroid with the ability to measure the full thickness of choroidal structure.[11],[12]

The aim of this study is to investigate the subfoveal choroidal thickness (SFCT) changes in patients with DME.


  Patients and Methods Top


One hundred and eighty eyes of 100 patients were included in this prospective nonrandomized study. These eyes were divided into three groups: Group I included sixty eyes of 36 diabetic patients with DME, the Group II included sixty eyes of 34 diabetic patients without macular edema, and Group III included sixty eyes of thirty normal persons (nondiabetics without any type of retinopathy).

All patients underwent a full ocular examination; cycloplegic refraction, best-corrected visual acuity (BCVA), intraocular pressure (IOP), slit-lamp examination, and dilated posterior segment examination. Fluorescein angiography (FA) and OCT scanning of the macula were performed for all eyes included in the study.

Inclusion criteria

Patients in age group (40–60 years) and patients with diabetes Type I and II are included in the study. Macular edema was assessed by clinical examination and SD-OCT imaging.

Exclusion criteria

Patients with systemic diseases other than diabetes, eyes with errors of refraction >−6 diopter (D), and eyes with IOP >20 mmHg were excluded from the study. Eyes with previous laser treatment or intravitreal injection of any drug, previous eye surgery, patients with proliferative diabetic retinopathy (PDR), patients with retinal disease other than DME (choroidal neovascularization, or any type of retinopathy) were also excluded from the study. FA was used to exclude the eyes with ischemic maculopathy.

Choroidal thickness measurement

All SD-OCT examinations were done using Heidelberg Spectralis-OCT (Heidelberg Engineering, Heidelberg, Germany) using 19-line (30°) raster scan centered on the fovea. All measurements were done by the same operator.

The choroidal thickness was measured using EDI-OCT technique, by making the position of SD-OCT instrument closer to the eye than ordinary; this maneuver will increase the sensitivity of the deep layer visualization and imaging.

The choroidal thickness was measured manually using the cursor in the OCT instrument software. The measure extends from the hyperreflective layer of retinal pigment epithelium to the hyporeflective line corresponding to the choroidal-scleral junction.

Choroidal thickness is measured at five locations (thefirst at the subfoveal (center of the fovea) location and other four locations at 2 mm intervals from the fovea (2 mm nasal, 2 mm temporal, 2 mm superior, and 2 mm inferior from the center of the fovea) [Figure 2], [Figure 3], [Figure 4].

All patients gave an informed consent according to the tenets of the Declaration of Helsinki. The collected data were analyzed statistically using SPSS software (IBM SPSS Statistics 14.0; Chicago, IL, USA). One-way ANOVA test and Pearson's correlation test were used to analyze the data. P < 0.05 was considered statistically significant.


  Results Top


Totally, 180 eyes of 100 persons were included in this study. They were divided into three groups (each included sixty eyes): Group I included 36 patients with mild or moderate non-PDR and with DME, their mean age of 55 2.3 years (range: 45–60 years), mean refractive error was - 2.3 0.57 D. (range: +1.5–−4.75 D.), the BCVA was 0.29 0.14 (range: 0.1–0.6), and their mean IOP was 17.2 1.3 mmHg (range: 12–18 mmHg). Macular edema was in the form of cystic type in 21 eyes, diffuse in eight eyes, and focal in seven ones.

Group II included 34 diabetic patients without DME with mean age of 52.3 1.7 years (range: 41–59 years), mean refractive error was − 2.6 0.81 D (range: +2.00 to − 5.5 D.), the BCVA was 0.84 0.15 (range: 0.7–1.0), and their mean IOP was 16.1 2.1 (range: 12–17 mmHg).

Group III included 30 normal persons with mean age 51.2 1.6 years (range: 42–58 years), mean refractive error was − 1.9 0.71 D. (range: +0.75–−3.5 D.), the BCVA was 0.87 0.09 (range: 0.7–1.0), and their mean IOP was 17.5 1.1 (range: 14–19 mmHg).

Central macular thickness (CMT) was measured in all groups; it was 463.6 11.8 μm (range: 446–485 μm) in Group I and 256.07 17.2 μm (range: 222–287 μm) and 252.2 17.8 μm (range: 222–285 μm) in Groups II and III, respectively.

Other than BCVA and CMT, there was no significant difference between the three groups in other data. These data are summarized in [Table 1].
Table 1: Age, best-corrected visual acuity, refractive error, intraocular pressure, and central macular thickness in the three groups of the study

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The SFCT was significantly reduced in Group I compared with the other two groups; in Group I, the SFCT was 215.12 5.6 μm (range: 202–222 μm); in Group II, it was 253.1 9.3 μm (range: 237–279 μm); and in Group III, it was 255.9 9.2 μm (range: 240–281 μm) (P< 0.001). The mean choroidal thickness was significantly reduced in Group I at 2 mm intervals from the fovea (2 mm nasal, temporal, superior, and inferior from the center of the fovea) compared with the other two groups (P< 0.001). These data are summarized in [Table 2] and [Figure 1].
Table 2: The choroidal thickness in five locations measured by enhanced depth imaging-optical coherence tomography technique

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Figure 1: The mean choroidal thickness in Groups I, II, and III. Mean choroidal thickness at subfoveal and each of the four locations measured at 2 mm intervals nasal, temporal superior, and inferior.

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Figure 2: Fluorescein angiography and enhanced depth imaging optical coherence tomography of patient with diabetic macular edema. Upper: the color image and fluorescein angiography showing cystoid macular edema. Lower: the enhanced depth imaging optical coherence tomography image showing the subfoveal choroidal thickness at subfoveal (red) and 2 mm nasal and temporal (green).

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Figure 3: Fluorescein angiography and enhanced depth imaging optical coherence tomography of diabetic patient without macular edema. Upper: The color image and fluorescein angiography showing no maculopathy. Lower: The enhanced depth imaging optical coherence tomography image showing the subfoveal choroidal thickness at subfoveal and 2 mm nasal and temporal (green).

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Figure 4: Fluorescein angiography and enhanced depth imaging optical coherence tomography of normal subject. Upper: The color image and fluorescein angiography showing normal retina. Lower: The enhanced depth imaging optical coherence tomography image showing the subfoveal choroidal thickness at subfoveal (red) and 2 mm nasal and temporal (green).

Click here to view


The correlation between CMT and SFCT was measured in each group. In Group I, a negative correlation was observed (r = −0.6, P < 0.001) indicating that the CMT increases as the SFCT decreases. In other two groups (Groups II and III), no statistically significant correlation between two measurements was found (in Group II, r = 0.17 and in Group III, r = 0.2 with P = 0.2 and 0.07, respectively) suggesting that macular thickness is not directly related to SFCT in these groups.

In addition, the correlation between BCVA and SFCT was examined in each group. In Group I, a statistically significant correlation was observed (r = 0.5, P < 0.001) indicating that the BCVA decreases as the SFCT decreases. In other two groups (Groups II and III), no significant statistically significant correlation between the two measurements was found (in Group II, r = −0.1 and in Group III, r = −0.1 with P = 0.6 and 0.4, respectively) suggesting that BCVA is not directly related to SFCT in these groups [Table 3].
Table 3: Pearson's correlation between subfoveal choroidal thickness and central macular thickness and best-corrected visual acuity in each group

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  Discussion Top


The outer retina metabolism is dependent mainly on the choroid, so it has an important role in the pathogenesis and changes that occur in of diabetic eye. On histological examination, the choroid shows areas of capillary nonperfusion which is associated with diabetic retinopathy.[13],[14]

A retinal hypoxia may occur secondary to decreased the blood flow to choroid and so the vascular endothelial growth factor is released due to this retinal hypoxia resulting in disturbance of the blood-retinal barrier with subsequent occurrence of macular edema.[15] Therefore, the evaluation of the changes that occur in the choroid may be helpful to understand the pathological development of macular edema in diabetic eyes.[16]

Choroidal imaging and thickness measurements have been reported with different commercially available OCT instruments.[17]

Lin et al.[18] concluded that the most suitable method to measure the choroidal thickness was Spectralis OCT in either EDI or inverted mode, and they also concluded that it was difficult to compare between different instruments in measurement of the thickness of the choroid.

In this study, the EDI-OCT technique of Heidelberg Spectralis-OCT was used to measure and compare the choroidal thickness in eyes with DME, in eyes of diabetic patients without macular edema, and in eyes of normal individuals.

The axial length of the eye and its refractive error may have an impact on the choroidal thickness as there is an inverse relation between degree of myopia and the thickness of the choroid.[19],[20] Age and IOP are other factors that must be considered when comparing choroidal thickness between different eyes.[21]

Hence, in this study, all patients and individuals in the control group were selected in the same age group (40–60 years), and they all had a refractive error ˂−6 D, with normal IOP.

As the thickness of the choroid is different according to its location in the posterior segment of the eye.[22],[23] In this study, the choroidal thickness is measured at five locations (subfoveal and other four locations at 2 mm interval nasal, temporal, upper, and lower from the fovea).

This study showed that the choroidal thickness is significantly decreased in eyes with DME. There was no significant difference in the choroidal thickness measurement between eyes of diabetic patients without macular edema and those of normal individuals.

Querques et al.[24] examined the changes in choroidal thickness at the macular area in diabetic eyes. They compared the choroidal thickness in diabetic eyes with different stages of retinopathy, and they found that there was no difference in the choroidal thickness in the different diabetic stages.

Vujosevic et al.,[25] in their study, showed that the choroidal thickness was indirectly proportional to the degree of diabetic retinopathy. The choroidal thickness in diabetic patients without retinopathy did not differ from normal eyes. In addition, there was no correlation observed between macular edema and choroidal thickness.

This study showed a negative correlation between CMT and SFCT (−0.74) and also, a statistically significant correlation was observed (r = 0.75) between BCVA and SFCT in cases with macular edema suggesting that in eyes with DME, there was an inverse proportion between the CMT and SFCT and that the BCVA decreases as the SFCT decreases.


  Conclusion Top


Eyes with DME showed decreasing in SFCT as measured by EDI-OCT. There is correlation between SFCT and of both BCVA and CMT in eyes with DME.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Mori F, Hikichi T, Takahashi J, Nagaoka T, Yoshida A. Dysfunction of active transport of blood-retinal barrier in patients with clinically significant macular edema in type 2 diabetes. Diabetes Care 2002;25:1248-9.  Back to cited text no. 1
    
2.
Chen FK, Yeoh J, Rahman W, Patel PJ, Tufail A, Da Cruz L. Topographic variation and interocular symmetry of macular choroidal thickness using enhanced depth imaging optical coherence tomography. Invest Ophthalmol Vis Sci 2012;53:975-85.  Back to cited text no. 2
    
3.
Usui S, Ikuno Y, Miki A, Matsushita K, Yasuno Y, Nishida K. Evaluation of the choroidal thickness using high-penetration optical coherence tomography with long wavelength in highly myopic normal-tension glaucoma. Am J Ophthalmol 2012;153:10-6.e1.  Back to cited text no. 3
    
4.
Xu J, Xu L, Du KF, Shao L, Chen CX, Zhou JQ, et al. Subfoveal choroidal thickness in diabetes and diabetic retinopathy. Ophthalmology 2013;120:2023-8.  Back to cited text no. 4
    
5.
Lutty GA. Effects of diabetes on the eye. Invest Ophthalmol Vis Sci 2013;54:ORSF81-7.  Back to cited text no. 5
    
6.
Esmaeelpour M, Považay B, Hermann B, Hofer B, Kajic V, Hale SL, et al. Mapping choroidal and retinal thickness variation in type 2 diabetes using three-dimensional 1060-nm optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:5311-6.  Back to cited text no. 6
    
7.
Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med 2012;366:1227-39.  Back to cited text no. 7
    
8.
Bhagat N, Grigorian RA, Tutela A, Zarbin MA. Diabetic macular edema: Pathogenesis and treatment. Surv Ophthalmol 2009;54:1-32.  Back to cited text no. 8
    
9.
Regatieri CV, Branchini L, Carmody J, Fujimoto JG, Duker JS. Choroidal thickness in patients with diabetic retinopathy analyzed by spectral-domain optical coherence tomography. Retina 2012;32:563-8.  Back to cited text no. 9
    
10.
Povazay B, Hermann B, Hofer B, Kajic V, Simpson E, Bridgford T, et al. Wide-field optical coherence tomography of the choroid in vivo. Invest Ophthalmol Vis Sci 2009;50:1856-63.  Back to cited text no. 10
    
11.
Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008;146:496-500.  Back to cited text no. 11
    
12.
Margolis R, Spaide RF. A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol 2009;147:811-5.  Back to cited text no. 12
    
13.
Sogawa K, Nagaoka T, Takahashi A, Tanano I, Tani T, Ishibazawa A, et al. Relationship between choroidal thickness and choroidal circulation in healthy young subjects. Am J Ophthalmol 2012;153:1129-32.e1.  Back to cited text no. 13
    
14.
McLeod DS, Lutty GA. High-resolution histologic analysis of the human choroidal vasculature. Invest Ophthalmol Vis Sci 1994;35:3799-811.  Back to cited text no. 14
    
15.
Funatsu H, Yamashita H, Ikeda T, Nakanishi Y, Kitano S, Hori S. Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with diabetic macular edema and other retinal disorders. Am J Ophthalmol 2002;133:537-43.  Back to cited text no. 15
    
16.
Aiello LP, Northrup JM, Keyt BA, Takagi H, Iwamoto MA. Hypoxic regulation of vascular endothelial growth factor in retinal cells. Arch Ophthalmol 1995;113:1538-44.  Back to cited text no. 16
    
17.
Manjunath V, Taha M, Fujimoto JG, Duker JS. Choroidal thickness in normal eyes measured using cirrus HD optical coherence tomography. Am J Ophthalmol 2010;150:325-9.e1.  Back to cited text no. 17
    
18.
Lin P, Mettu PS, Pomerleau DL, Chiu SJ, Maldonado R, Stinnett S, et al. Image inversion spectral-domain optical coherence tomography optimizes choroidal thickness and detail through improved contrast. Invest Ophthalmol Vis Sci 2012;53:1874-82.  Back to cited text no. 18
    
19.
Fujiwara T, Imamura Y, Margolis R, Slakter JS, Spaide RF. Enhanced depth imaging optical coherence tomography of the choroid in highly myopic eyes. Am J Ophthalmol 2009;148:445-50.  Back to cited text no. 19
    
20.
Nishida Y, Fujiwara T, Imamura Y, Lima LH, Kurosaka D, Spaide RF. Choroidal thickness and visual acuity in highly myopic eyes. Retina 2012;32:1229-36.  Back to cited text no. 20
    
21.
Rahman W, Chen FK, Yeoh J, Patel P, Tufail A, Da Cruz L. Repeatability of manual subfoveal choroidal thickness measurements in healthy subjects using the technique of enhanced depth imaging optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:2267-71.  Back to cited text no. 21
    
22.
Ouyang Y, Heussen FM, Mokwa N, Walsh AC, Durbin MK, Keane PA, et al. Spatial distribution of posterior pole choroidal thickness by spectral domain optical coherence tomography. Invest Ophthalmol Vis Sci 2011;52:7019-26.  Back to cited text no. 22
    
23.
Branchini L, Regatieri CV, Flores-Moreno I, Baumann B, Fujimoto JG, Duker JS. Reproducibility of choroidal thickness measurements across three spectral domain optical coherence tomography systems. Ophthalmology 2012;119:119-23.  Back to cited text no. 23
    
24.
Querques G, Lattanzio R, Querques L, Del Turco C, Forte R, Pierro L, et al. Enhanced depth imaging optical coherence tomography in type 2 diabetes. Invest Ophthalmol Vis Sci 2012;53:6017-24.  Back to cited text no. 24
    
25.
Vujosevic S, Martini F, Cavarzeran F, Pilotto E, Midena E. Macular and peripapillary choroidal thickness in diabetic patients. Retina 2012;32:1781-90.  Back to cited text no. 25
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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