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 Table of Contents  
ORIGINAL ARTICLE
Year : 2018  |  Volume : 19  |  Issue : 3  |  Page : 201-204

Correlation between choroidal thickness and central macular thickness measured by optical coherence tomography in nonproliferative diabetic retinopathy


1 Department of Ophthalmology, Cairo University, Giza, Egypt
2 Department of Ophthalmology, South Valley University, Qena, Egypt

Date of Submission17-Feb-2018
Date of Acceptance14-Jun-2018
Date of Web Publication24-Sep-2018

Correspondence Address:
Mohamed A Hamed
Qena Faculty of Medicine, South Valley University, Qena 83523
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/DJO.DJO_12_18

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  Abstract 


Purpose To investigate the correlation between central macular thickness (CMT) and subfoveal choroidal thickness (SFCT) measured by spectral-domain optical coherence tomography in nonproliferative diabetic retinopathy (NPDR).
Patients and methods This is a prospective observational randomized study (case series) that was performed on 48 eyes of 29 patients having NPDR. The 48 eyes were divided into two groups: group I comprised 28 eyes of diabetic patients having NPDR without macular edema [NPDR without diabetic macular edema (DME)] and group II included 20 eyes of diabetic patients having NPDR with macular edema (NPDR with DME). The patients underwent spectral-domain optical coherence tomography to measure the central subfoveal and parafoveal retinal and choroidal thicknesses.
Results The age for group I was 56.18±11.27 years and for group II was 60.35±7.67 years. In group I, the CMT was 297.57±40.66 µm and the central subfoveal choroidal thickness (C-SFCT) was 221.21±40.49 µm. In group II, the CMT was 425.1±136.4 µm and the C-SFCT was 209.65±27.92 µm. In group I, no statistically significant correlation between CMT and C-SFCT was found (r=0.211, P=0.282), suggesting that retinal thickness may not be directly related to the choroidal thickness in this study group. In group II, a weak negative correlation was observed (r=−0.518, P=0.019), indicating that the choroidal thickness may decrease as the central retinal thickness increases in this group.
Conclusion There was a statistically significant negative correlation between CMT and C-SFCT in patients with NPDR and DME. The SFCT decreased as the CMT increased. In addition, the subfoveal choroid was thinner in eyes with NPDR and DME than in eyes with NPDR without DME.

Keywords: choroidal thickness, diabetic macular edema, macular thickness, nonproliferative diabetic retinopathy, optical coherence tomography


How to cite this article:
Adel Hasan N, Aldghaimy AH, Hamed MA, Eltaher AM. Correlation between choroidal thickness and central macular thickness measured by optical coherence tomography in nonproliferative diabetic retinopathy. Delta J Ophthalmol 2018;19:201-4

How to cite this URL:
Adel Hasan N, Aldghaimy AH, Hamed MA, Eltaher AM. Correlation between choroidal thickness and central macular thickness measured by optical coherence tomography in nonproliferative diabetic retinopathy. Delta J Ophthalmol [serial online] 2018 [cited 2018 Nov 16];19:201-4. Available from: http://www.djo.eg.net/text.asp?2018/19/3/201/242143




  Introduction Top


Diabetic retinopathy (DR) and diabetic macular edema (DME) are common sight-threatening retinopathies caused by abnormalities in retinal vessels and capillaries of diabetic patients. So, early detection of DR can reduce the loss of visual acuity, blindness, and associated morbidity [1].

The choroid is a highly vascularized layer in the ocular coat interposed between the retina and sclera. It receives a large proportion of ocular blood flow and is responsible for the supply of nutrition to the outer retinal layers including the retinal pigment epithelium (RPE) and photoreceptors. So, a healthy choroid is essential for normal retinal function [2].

Diabetic patients have many pathological changes in their choroid. These changes are increased tortuosity and focal vascular dilatation, microaneurysms, and nonperfusion areas [3]. As there is no retinal vasculature in the foveal region, impairment of the choriocapillaris may cause severe functional damage to the retinal tissue in the fovea [4].

Until recently, the choroid could only be evaluated by indocyanine green angiography, laser flowmetry, and ultrasonography. However, these techniques are only able to show the choroidal vessel abnormalities and blood flow changes; they cannot show the three-dimensional anatomy of the choroidal layers or the RPE [5].

Optical coherence tomography (OCT) has a superior spatial resolution, shorter image acquisition time, does not require contact with the eye and is totally noninvasive. However, the use of OCT is limited by intraocular media opacities including corneal edema, cataract, and vitreous hemorrhage [6].

The aim of the current study was to investigate the correlation between the central macular thickness (CMT) and the subfoveal choroidal thickness (SFCT) measured by OCT in nonproliferative diabetic retinopathy (NPDR).


  Patients and methods Top


This is a prospective observational randomized study (case series) that was performed on 48 eyes of 29 patients having NPDR between December 2016 and June 2017 at the Outpatient Clinic of Ophthalmology Department, Qena University Hospital, South Valley University. A written informed consent was obtained from each patient, and the research was carried out in accordance with the Declaration of Helsinki. Local Ethics Committee approval for the study was obtained.

The 48 eyes were divided into two groups:
  1. Group I: 28 eyes of diabetic patients having NPDR without macular edema.
  2. Group II: 20 eyes of diabetic patients having NPDR with macular edema.


Inclusion criteria

The following were the inclusion criteria:
  1. Age between 34 and 67 years.
  2. Slit-lamp biomicroscopy, fundus fluorescein angiography (FFA) and OCT were used to diagnose DME based on the presence or absence of macular thickening (>300 µm) or hard exudates at or within 500 µm of the central macula, as defined by the early treatment DR study protocol.


Exclusion criteria

The following were the exclusion criteria:
  1. Presence of proliferative diabetic retinopathy in FFA.
  2. Macular scar diagnosed using slit-lamp biomicroscopy and OCT.
  3. Macular ischemia diagnosed by FFA.
  4. Other factors that may contribute to the presence of edema such as retinal vein occlusion, age-related maculopathy, postcataract surgery, and posterior uveitis.
  5. Eyes with media opacities leading to poor quality of OCT scans such as significant cataract or vitreous hemorrhage.
  6. Previous argon laser treatment or intravitreal injection within 6 months of scanning and previous pars plana vitrectomy.
  7. Hypertensive retinopathy.
  8. Presence of refractive errors of more than ±4.0 D, as the thickness of the choroid changes with ametropia.
  9. Vitreomacular interface disorders diagnosed by OCT.


The patients were subjected to full medical history including the duration and type of diabetes. Serum glycated hemoglobin A1C levels and random blood sugar were also measured. All eyes were subjected to slit-lamp examination of the anterior segment. Fundus examination was done by using slit-lamp biomicroscopy with a 90 D lens. Fluorescein angiography was performed by Zeiss fundus camera (Carl Zeiss Meditec, Jena, Germany) either on the same setting with OCT or within three months of it. OCT was done by a high-speed spectral-domain OCT machine (Spectralis; Heidelberg Engineering GmbH, Heidelberg, Germany) to measure the central subfoveal and parafoveal retinal and choroidal thickness. OCT was done for all eyes to measure the CMT and parafoveal thickness to diagnose DME, detect the type of macular edema and identify the presence of hard exudates. A 3-mm horizontal line centered on the fovea was used in the evaluation of choroidal thickness, starting perpendicularly from the outer part of the RPE (hyper-reflective line) to the line corresponding to the chorio-scleral junction. Central subfoveal choroidal thickness (C-SFCT) and choroidal thickness at the temporal and nasal distance from the central fovea of 1500 µm were measured ([Figure 1]); measurements were made manually using the caliber tool in the OCT Heidelberg software. In addition, the CMT measurement was obtained for each eye.
Figure 1 Steps of measurement of the choroidal thickness: a fovea-centered 3-mm horizontal line was drawn using the caliber tool and then a perpendicular line was drawn from the outer part of the hyper-reflective retinal pigment epithelium to the chorio-scleral junction.

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Statistical analysis

Descriptive statistics were used for illustrating the mean and SD of quantitative data. Ordinal and categorical data were represented by frequency and percentage. Comparison of means to check for statistical significance difference for different variables was conducted using the suitable tests. To calculate the correlation between different variables, Pearson’s correlation was used. All data were computed and conducted using the SPSS Statistics (IBM SPSS Statistics for Windows, Version 20.0; IBM Corp., Armonk, NY, USA).


  Results Top


This prospective study included 48 eyes of 29 patients, with 14 females and 15 males. All patients had diabetes mellitus type II with a mean age of 57.92±10.05 years (range, 34–72 years) for analysis as per our eligibility criteria. The baseline clinical characteristics between the two groups are summarized in [Table 1].
Table 1 Baseline clinical characteristics

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In group I, the CMT was 297.57±40.66 µm. The C-SFCT was 221.21±40.49 µm, whereas the nasal subfoveal choroidal thickness (N-SFCT) was 199.90±41.23 µm and the temporal subfoveal choroidal thickness (T-SFCT) was 231.65±40.47 µm.

In group II, the CMT was 425.1±136.4 µm. The C-SFCT was 209.65±27.92 µm, whereas the N-SFCT was 194.43±62.70 µm and the T-SFCT was 204.11±25.27 µm.

In group I, there was no statistically significant correlation between the CMT and the C-SFCT (r=0.211, P=0.282), suggesting that the retinal thickness may not be directly related to the choroidal thickness in this study group ([Table 2]).
Table 2 Correlation between central macular thickness and central subfoveal choroidal thickness

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In group II, a weak negative correlation was observed (r=−0.518, P=0.019), indicating that the choroidal thickness may decrease as the CMT increases in this group ([Table 2]).

Choroidal thickness measurements in different locations are summarized in [Table 3]. The mean T-SFCT was lower in group II than in group I. In addition, The N-SFCT was also lower in group II than in group I. There was a statistically significant difference between the two groups at the N-SFCT (P<0.001).
Table 3 Choroidal thickness measurements in different locations

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  Discussion Top


In the present study, the CMT in group I was 297.57±40.66 µm, whereas in group II, it was 425.1±136.4 µm. This was similar to the study by Querques et al. [7] who reported that the CMT in group I was 294.5±23.5 µm, whereas in group II was 385.6±75.1 µm, which was slightly lower than our results. Most of the other studies did not mention the value of the CMT in detail [8],[9],[10].

In group I, in this study, the C-SFCT was 221.21±40.49 µm, whereas in group II, it was 209.65±27.92 µm. The results of group I matched that of the study by Regatieri et al. [9] (222±21.6 µm) and the study by Querques et al. [7] (207±55.9 µm). It is also close to the study by Ünsal et al. [10] in which the C-SFCT was 235.4±84.5 µm. In contrast, some authors reported thicker C-SFCT, such as Sudhalkar et al. [11] (248.0±56.3 µm), Vujosevic et al. [8] (275.2±81.6 µm), and Zhang et al. [12] (311±80 μm).

However, the results of group II matched with the studies by Ünsal et al. [10] (206.8±45.4 µm) and Querques et al. [9] (190.8±48.4 µm). Regatieri et al. [7] reported thinner C-SFCT, which was 169.5±14.7 µm. In contrast to the present study, Kim et al. [13] showed that the C-SFCT increased with increasing severity of DR (from no DR to proliferative diabetic retinopathy) and with the presence of DME.

In the current study, there was no significant correlation between choroidal thickness and retinal thickness in the macular area in group I. However, there was a significant decrease in choroidal thickness as the retinal thickness increased in the macular area in group II.

In the present study, the mean of both T-SFCT and N-SFCT was lower in group II than in group I. There was a statistically significant difference between the two groups at N-SFCT only. This matched with previous studies that reported that the choroidal volume in the nasal quadrant was significantly lower than all other quadrants [14]. Ünsal et al. [10] considered the decrease in choroidal thickness in DME to be false owing to inhibition of the signal transduction and reflection from the choroid secondary to increased ocular opacity as a result of macular edema.

Esmaeelpour et al. [15] demonstrated that there was a decreased macular choroidal thickness in diabetic patients with or without diabetic maculopathy, with no difference in foveal choroidal thickness among different maculopathy groups.

Vujosevic et al. [8] stated that the choriocapillaris degeneration, previously demonstrated in histopathology studies, may be responsible for the photoreceptor dysfunction and death by insufficient removal of waste products generated by the RPE cells and consequent accumulation of such waste in the Bruch’s membrane. These can ultimately lead to choroidal auto-infarction and atrophy indirectly visualized as reduced choroidal thickness.


  Conclusion Top


There was a statistically significant negative correlation between C-SFCT and CMT in patients with NPDR and macular edema, whereas there was no significant correlation in patients with NPDR without macular edema. Spectral-domain OCT is a noninvasive technology to assess the choroid and may be a useful tool in the evaluation of chorioretinal vascular changes in DR.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Georgieva DK, Sivkova N. Assessment of serous macular detachment in eyes with diabetic macular edema by use of spectral-domain optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2009; 247:1461–1469.  Back to cited text no. 1
    
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Shiragami C, Shiraga F, Matsuo T, Tsuchida Y, Ohtsuki H. Risk factors for diabetic choroidopathy in patients with diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 2002; 240:436–442.  Back to cited text no. 3
    
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Nagaoka T, Kitaya N, Sugawara R. Alteration of choroidal circulation in the foveal region in patients with type 2 diabetes. Br J Ophthalmol 2004; 88:1060–1063.  Back to cited text no. 4
    
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Weinberger D, Kramer M, Priel E, Gaton D, Axer-Siegel R, Yassur Y. Indocyanine green angiographic findings in nonproliferative diabetic retinopathy. Am J Ophthalmol 1998; 126:238–247.  Back to cited text no. 5
    
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Cole ED, Novais EA, Louzada RN, Waheed NK. Contemporary retinal imaging techniques in diabetic retinopathy. Clin Experiment Ophthalmol 2016; 44:289–299.  Back to cited text no. 6
    
7.
Querques G, Lattanzio R, Querques L, Turco C, Forte R, Pierro L et al. Enhanced depth imaging optical coherence tomography in type 2 diabetes. Invest Ophthalmol Vis Sci 2012; 53:6017–6024.  Back to cited text no. 7
    
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Vujosevic S, Martini F, Cavarzeran F, Pilotto E, Midena E. Macular and peripapillary choroidal thickness in diabetic patients. Retina 2012; 32:1781–1790.  Back to cited text no. 8
    
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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; 32:563–568.  Back to cited text no. 9
    
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Ünsal E, Eltutar K, Zirtiloğlu S, Dinçer N, Özdoğan Erkul S, Güngel H. Choroidal thickness in patients with diabetic retinopathy. Clin Ophthalmol 2014; 8:637–642.  Back to cited text no. 10
    
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Sudhalkar A, Chhablani JK, Venkata A, Raman R, Rao PS, Jonnadula GB. Choroidal thickness in diabetic patients of Indian ethnicity. Indian J Ophthalmol 2015; 63:912–916.  Back to cited text no. 11
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Zhang Z, Meng X, Wu Z, Zou W, Zhang J, Zhu D et al. Changes in choroidal thickness after panretinal photocoagulation for diabetic retinopathy: a 12-week longitudinal study. Invest Ophthalmol Vis Sci 2015; 56:2631–2638.  Back to cited text no. 12
    
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Kim JT, Lee DH, Joe SG, Kim JG, Yoon YH. Changes in choroidal thickness in relation to the severity of retinopathy and macular edema in type 2 diabetic patients. Invest Ophthalmol Vis Sci 2013; 54:3378–3384.  Back to cited text no. 13
    
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Barteselli G, Chhablani J, El-Emam S, Wang H, Chuang J, Kozak I et al. Choroidal volume variations with age, axial length, and sex in healthy subjects: a three-dimensional analysis. Ophthalmology 2012; 119:2572–2578.  Back to cited text no. 14
    
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Esmaeelpour M, Brunner S, Ansari-Shahrezaei S, Nemetz S, Povazay B, Kajic V, Drexler W, Binder S. Choroidal thinning in diabetes type 1 detected by 3-dimensional 1060 nm optical coherence tomography. Invest Ophthalmol Vis Sci 2012; 53:6803–6809.  Back to cited text no. 15
    


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  [Table 1], [Table 2], [Table 3]



 

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