|Year : 2020 | Volume
| Issue : 1 | Page : 49-56
Choroidal thickness measured by swept source optical coherence tomography in diabetic macular edema
Haitham Y Al-Nashar, Sahar Hemeda
Department of Ophthalmology, Zagazig University, Zagazig, Egypt
|Date of Submission||10-Jul-2019|
|Date of Decision||30-Nov-2019|
|Date of Acceptance||05-Dec-2019|
|Date of Web Publication||28-Feb-2020|
Haitham Y Al-Nashar
Department of Ophthalmology, Zagazig University, Zagazig 44519
Source of Support: None, Conflict of Interest: None
Purpose The aim of this study was to evaluate the choroidal thickness in eyes with diabetic macular edema (DME) with the use of swept source optical coherence tomography (SS-OCT).
Patients and methods A total of 240 eyes were included in this prospective nonrandomized study. They were divided into three groups, each including 80 eyes. Group I included patients with DME, group II included diabetic patients without retinopathy, and group III were normal persons. Fluorescein angiography was done for all diabetic patients. Macular and choroidal thicknesses were measured by SS-OCT in all eyes. Forty-five eyes from group I received two intravitreal injections of 0.5 mg/0.05 ml ranibizumab with 1-month interval. Correlation between choroidal and macular thickness was evaluated in eyes with DME.
Results The mean choroidal thickness in the central subfield area was 129.7±12.5 μm in group I (eyes with DME), 200.4±2.8 μm in group II (diabetic patients without DME), and 208.3±9.7 μm in group III (normal eyes). There was a statistically significant difference in choroidal thickness between eyes with DME (group I) and both groups II and III (P<0.001), whereas there was no statistically significant difference between diabetic patients without macular edema (group II) and normal participants (group III) (P=0.2). There was no statistically significant difference among the three groups regarding age, refractive errors, and intraocular pressure. The mean best-corrected visual acuity was 0.31±0.09, 0.78±1.1, and 0.84±1.2 in groups I, II, and III, respectively (P=0.001). Negative correlation between macular and choroidal thickness was observed in eyes with DME (r=−0.7, P<0.001). There was no significant difference between choroidal thickness before and after intravitreal injection of ranibizumab (P=0.4).
Conclusion Choroidal thickness measured with SS-OCT was decreased in eyes with DME in comparison with normal participants. A negative correlation was observed between choroidal and macular thickness in eyes having DME.
Keywords: choroidal thickness, diabetic macular edema, optical coherence tomography, Swept source
|How to cite this article:|
Al-Nashar HY, Hemeda S. Choroidal thickness measured by swept source optical coherence tomography in diabetic macular edema. Delta J Ophthalmol 2020;21:49-56
|How to cite this URL:|
Al-Nashar HY, Hemeda S. Choroidal thickness measured by swept source optical coherence tomography in diabetic macular edema. Delta J Ophthalmol [serial online] 2020 [cited 2020 Sep 22];21:49-56. Available from: http://www.djo.eg.net/text.asp?2020/21/1/49/279719
| Introduction|| |
Diabetic macular edema (DME) is a serious eye conditions caused mainly by hyperglycemia. It is considered a major cause of loss of vision and blindness in the world .
There is a complex pathological process with many contributing factors that are responsible for the pathogenesis of DME. Disturbance of the inner and outer retinal barriers may play a role in accumulation of subretinal and intraretinal fluid. Hypoperfusion with resulting ischemia, release of oxygen-free radicals, and inflammatory mediators are involved in the disturbance of the blood–retina barrier .
The choroid is a highly vascular structure that supports the metabolic needs of the retinal pigment epithelium (RPE) and outer retina . The choroid absorbs excess light and supplies nutrients that are important for retinal protection. However, the choroid is also the site of different pathological disorders such as inflammation, ischemia, and neovascularization ,.
Enhanced-depth imaging (EDI) spectral domain optical coherence tomography (SD-OCT) was used for measurement of the choroidal thickness. Today, the newly introduced technology of swept source optical coherence tomography (SS-OCT) is used for better evaluation of the choroid . EDI method enabled the chorio-scleral border to be detected. However, in some cases, a clear image of the choroid cannot be obtained owing to obscuring the choroidal outer boundary ,.
High-speed SS-OCT has many advantages for choroidal assessment, as it uses a different light with longer wavelength (1050 nm). This allows more penetration with less scattering effect of the underlying RPE, which allows better choroidal visualization and imaging ,.
SS-OCT (DRI-OCT, Topcon) is a completely new technology that enhances the visualization of the choroid. For the first time, it is possible to obtain automatic choroidal volume and thickness measurements by using the software included in this device .
The aim of this study was to investigate and determine if there is a change in the choroidal thickness in eyes with DME.
| Patients and methods|| |
This prospective observational study included 240 eyes of 150 patients. The included eyes were divided into three groups (each one contained 80 eyes): group I included patients diagnosed with DME, group II included diabetic patients without macular edema, and group III included normal persons (nondiabetics without any type of retinopathy). The study was done according to the tenets of the Declaration of Helsinki. All patients signed a written informed consent to participate in the study and for publication of data before enrollment in the study. The study was granted the prerequisite acceptance from the Medical Bioethics Committee at Egypt Eye Center, Zagazig, Egypt.
All patients had a full ocular examination including cycloplegic refraction, best-corrected visual acuity (BCVA), intraocular pressure (IOP) measurement, slit-lamp examination, and fundus examination. Fluorescein angiography was done only for diabetic patients, whereas SS-OCT scanning of the macula was performed for all eyes included in the study.
Diabetic patients (types I and II) having nonproliferative diabetic retinopathy with age range from 40 to 60 years were included in the study.
Patients with systemic diseases other than diabetes, eyes with errors of refraction more than −6 D, and eyes with IOP more than 20 mmHg were excluded from the study. Eyes with proliferative diabetic retinopathy, eyes with previous laser treatment or intravitreal injection of any drug, previous eye surgery, and patients with retinal disease other than DME (e.g. choroidal neovascularization or any type of retinopathy) were also excluded from the study.
Retinal and choroidal thickness measurements
All SS-OCT examinations were done using deep range imaging (DRI) OCT (Triton; Topcon Corporation, Tokyo, Japan). OCT images were acquired covering a 6×6 mm retinal area centered at the fovea using a raster scanning strategy.
Three-dimensional thickness mapping of the retina and choroid was performed. The retina was defined as the layer between the internal limiting membrane and the RPE, whereas the choroid was defined as the layer between the RPE and the chorio-scleral interface.
From these three-dimensional thickness maps of the retina and choroid, the mean regional thickness was calculated for the nine sectors of the early-treatment diabetic retinopathy study (ETDRS) layout which was averaged by SS-OCT automatically ([Figure 1]). The inner and outer rings had diameters of 1–3 and 3–6 mm, respectively, and they were segmented into superior, inferior, temporal, and nasal quadrants. The individual sectors were referred to as the central subfield, nasal inner macula, superior inner macula, temporal inner macula, inferior inner macula, nasal outer macula, superior outer macula, temporal outer macula, and inferior outer macula. Choroidal thickness was measured at the fovea and at each of the other eight sectors for each group ([Figure 2]).
|Figure 1 Early-treatment diabetic retinopathy study (ETDRS) layout area and nine sectors of the ETDRS layout: C, central subfield; I1, inferior inner macula; I2, inferior outer macula; N1, nasal inner macula; N2, nasal outer macula; S1, superior inner macula; S2, superior outer macula; T1, temporal inner macula; T2, temporal outer macula.|
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|Figure 2 Choroidal thickness in eyes of different study groups. (a) Eyes with diabetic macular edema, (b) eyes of diabetic patients without retinopathy, and (c) eyes of normal participants. Left: B-scan OCT with autosegmentation of the choroid. Right: choroidal thickness map according to early-treatment diabetic retinopathy study (ETDRS) grid. OCT, optical coherence tomography.|
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Forty-five eyes from group I received two intravitreal injections of 0.5 mg/0.05 ml ranibizumab (Lucentis; Novartis Pharma Stein AG, Basle, Switzerland) with 1-month interval. A 27-G needle was used in the intravitreal injection, which was administered 4 mm from the limbus. Paracentesis with aqueous humor removal was performed after the injection to avoid the increase of IOP. The choroidal thickness was measured 1 month after the last injection.
The collected data were analyzed statistically using SPSS software (IBM SPSS Statistics 22.0; SPSS Inc., Chicago, Illinois, USA). One-way analysis of variance test and Pearson’s correlation test were used to analyze the data. P value less than 0.05 was considered statistically significant.
| Results|| |
A total of 240 eyes of 150 persons were included in this study. They were divided into three groups (each included 80 eyes): group I included 55 patients with DME, group II included 50 diabetic patients without DME, and group III included 45 normal persons. There was no statistically significant difference among the three groups regarding age, refractive error, and IOP. The mean BCVA was 0.31±0.09, 0.78±1.1, and 0.84±1.2 in groups I, II, and III, respectively. There was a statistically significant difference in BCVA between group I (eyes with macular edema) and groups II and III (P=0.001, [Table 1]).
|Table 1 Demographic and clinical data of the participants in different study groups|
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The mean macular thickness in all nine sectors of ETDRS grid was statistically significantly different between eyes with DME (group I) and eyes in the other two groups (groups II and III) ([Table 2]).
|Table 2 Mean±SD macular thickness (μm) in early-treatment diabetic retinopathy study sectors in different study groups|
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Quantitative overview of the ETDRS maps in all eyes included in the study showed that the choroidal thickness was significantly decreased in eyes with DME (129.7±12.5 μm) in comparison with normal eyes (208.3±9.7 μm) and eyes of diabetic patients but without macular edema (200.4±2.8 μm) ([Table 3] and [Figure 3]).
|Table 3 Mean±SD choroidal thickness (μm) in early-treatment diabetic retinopathy study sectors in different study groups|
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|Figure 3 Choroidal thickness in eyes of different study groups: group I, eyes with diabetic macular edema; group II, diabetic patients without retinopathy, and group III, normal participants.|
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The correlation between the mean retinal thickness and corresponding choroidal thickness in each sector of the ETDRS map was measured in eyes with DME (group I). A negative correlation was observed, indicating that the retinal thickness increases as the choroidal thickness decreases in eyes with DME ([Table 4] and [Figure 4]).
|Table 4 Pearson correlation between mean choroidal and macular thickness at each sector in eyes with diabetic macular edema|
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|Figure 4 Correlation between choroidal and macular thickness in eyes with diabetic macular edema. Left: B-scan OCT with autosegmentation of the choroid. Middle: choroidal thickness map according to early-treatment diabetic retinopathy study (ETDRS) grid. Right: macular thickness according to ETDRS grid. OCT, optical coherence tomography.|
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Before intravitreal ranibizumab injection, the mean choroidal thickness in the nine subfield areas was measured and compared with the choroidal thickness in the same locations 1 month after the last injection. There was no statistically significant difference between choroidal thickness before and after intravitreal injection ([Table 5] and [Figure 5]).
|Table 5 Mean±SD choroidal thickness (μm) in early-treatment diabetic retinopathy study sectors in eyes with diabetic macular edema before and after intravitreal injection|
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|Figure 5 Effect of intravitreal ranibizumab injection on choroidal thickness in eyes with diabetic macular edema. (a) Choroidal thickness before intravitreal injection. (b) Choroidal thickness 1 month after the last intravitreal injection.|
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| Discussion|| |
The choroid is an important tissue that is responsible for blood supply to the outer retina. A deficiency in choroidal vascular supply leads to retinal dysfunction and visual loss . Disorders of the choroid may have an important role in the development of many retinal disorders including diabetic retinopathy . In diabetic retinopathy, similar metabolic changes and similar growth factors were found in both retina and choroid .
Accurate measurement of the choroidal thickness is important for better understanding of the pathophysiological changes in different retinal diseases. Previously, the choroidal full thickness could not be investigated in most eyes because of scattering and insufficient light penetration beyond the RPE . Many studies examined the choroidal structure using SD-OCT instruments such as Heidelberg Spectralis and Cirrus HD-OCT. These SD-OCT instruments use a light source with wavelength of ∼800 nm, giving a tissue axial resolution of 5 μm .
EDI-OCT technology was introduced to improve choroidal visualization, which gives a significant advancement in the understanding of the pathophysiological choroidal changes that may occur in retino-choroidal diseases .
EDI-OCT was used to assess the choroidal thickness in eyes with diabetic retinopathy. The main drawbacks of EDI-OCT in choroidal examination are poor light penetration and manual segmentation.
SS-OCT is a new type of OCT that uses light with longer wavelength (1050 nm). This longer wavelength allows more penetration to a deeper tissue than that can be done with the conventional SD-OCT. This enables the imaging of the choroid. Thus, SS-OCT instruments should be more suitable for examining choroidal pathology than the present SD-OCT instruments. In addition, SS-OCT gives an automated choroidal thickness map ,.
In the present study, we used a SS-OCT instrument to acquire a choroidal thickness map using a fully automated choroidal segmentation algorithm.
SS-OCT has the ability to quantify retinal and choroidal thickness in eyes with DME with a good repeatability, reliability, and reproducibility .
The results of the present study showed that the choroidal thickness was significantly decreased in eyes with DME compared with eyes of normal participants. The choroidal thickness was similar in eyes of normal participants and diabetic patients without retinopathy. Moreover the study showed no effect of intravitreal ranibizumab injection on choroidal thickness.
Similar results were observed by Regatieri et al. , who examined choroidal thickness in diabetic patients using SD-OCT. They found a significant decrease in choroidal thickness in patients with DME compared with normal participants. Lee et al.  evaluated choroidal thickness in diabetes patients using SD-OCT. They found that subfoveal choroid thickness was significantly decreased in patients with diabetic retinopathy compared with normal participants, which is similar to the results of the present study. However, they found that the presence of macular edema did not result in additional choroidal thinning.
The results of the present study showed that diabetic patients without macular edema had similar choroidal thickness as normal participants and presence of macular edema was associated with decreased choroidal thickness.
Choroidal thickness can be influenced by many factors such as age, sex, ocular axial length, and IOP . All individuals included in the present study were from the same age group, with no significant difference between the different study groups regarding age, sex, and IOP.
The current study found that there was a significant negative correlation between choroidal and macula thickness in eyes with DME. The choroidal thickness was decreased when the thickness of the corresponding area of macula increased owing to the presence of macula edema.
Adhi et al.  found an alteration in choroidal morphology in eyes with diabetic retinopathy with significant decrease in subfoveal choroidal thickness.
Unsal et al.  in their study assessed both choroidal thickness and central macular thickness in patients with diabetic retinopathy (both nonproliferative and proliferative). They found that choroidal thickness was significantly decreased in eyes with DME and proliferative diabetic retinopathy. However, the present study investigated only eyes with nonproliferative retinopathy with DME.
Abadia et al.  used SS-OCT to compare choroidal thickness between diabetic patients with DME and healthy ones. They found that the choroid was significantly thinner in patients with DME with moderate nonproliferative diabetic retinopathy than in healthy individuals. These results are comparable with the results of the current study.
Wang et al.  compared choroidal vascular density and volume in diabetic eyes and controls using en face technology of SS-OCT. They found a significant reduction of both choroidal vascular density and volume, and the reduction was more in the advanced stages of diabetic retinopathy.
In conclusion, the choroidal thickness measured with SS-OCT was decreased in eyes with DME in comparison with normal participants. Negative correlation was observed between choroidal and macular thickness in eyes with DME. There was no difference in choroidal thickness between normal eyes and eyes of diabetic patients without diabetic retinopathy. In addition, there was no effect of intravitreal injection of ranibizumab on the choroidal thickness.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med 2012; 366:1227–1239.
Bhagat N, Grigorian RA, Tutela A, Zarbin MA. Diabetic macular edema: pathogenesis and treatment. Surv Ophthalmol 2009; 54:1–32.
Nickla DL, Wallman J. The multifunctional choroid. Prog Retin Eye Res 2010; 29:144–168.
Manjunath V, Goren J, Fujimoto JG, Duker JS. Analysis of choroidal thickness in age-related macular degeneration using spectral-domain optical coherence tomography. Am J Ophthalmol 2011; 152:663–668.
Wood A, Binns A, Margrain T, Drexler W, Považay B, Esmaeelpour M et al.
Retinal and choroidal thickness in early age-related macular degeneration. Am J Ophthalmol 2011; 152:1030–1038.
Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008; 146:496–500.
Yamashita T, Yamashita T, Shirasawa M, Arimura N, Terasaki H, Sakamoto T. Repeatability and reproducibility of subfoveal choroidal thickness in normal eyes of Japanese using different SD-OCT devices. Invest Ophthalmol Vis Sci 2012; 53:1102–1107.
Margolis R, Spaide RF. A pilot study of enhanced depth imaging optical coherence tomography of the choroid in normal eyes. Am J Ophthalmol 2009; 147:811–815.
Esmaeelpour M, Povay 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; 52:5311–5316.
Ferrara D, Mohler KJ, Waheed N, Adhi M, Liu JJ, Grulkowski I et al.
En face enhanced-depth swept-source optical coherence tomography features of chronic central serous chorioretinopathy. Ophthalmology 2014; 121:719–726.
Pasaoglu I, Satana B, Altan C, Artunay O, Basarir B, Onmez FE, Inal A. Lamina cribrosa surface position in idiopathic intracranial hypertension with swept-source optical coherence tomography. Indian J Ophthalmol. 2019; 67:1085–1088.
Nagaoka T, Kitaya N, Sugawara R, Yokota H, Mori F, Hikichi T et al.
Alteration of choroidal circulation in the foveal region in patients with type 2 diabetes. Br J Ophthalmol 2004; 88:1060–1063.
Wong IY, Wong RL, Zhao P, Lai WW. Choroidal thickness in relation to hypercholesterolemia on enhanced depth imaging optical coherence tomography. Retina 2013; 33:423–428.
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.
Wei X, Balne PK, Meissner KE, Barathi VA, Schmetterer L, Agrawal R. Assessment of flow dynamics in retinal and choroidal microcirculation. Surv Ophthalmol 2018; 63:646–664.
Imamura Y, Fujiwara T, Margolis R, Spaide RF. Enhanced depth imaging optical coherence tomography of the choroid in central serous chorioretinopathy. Retina 2009; 29:1469–1473.
Manjunath V, Taha M, Fujimoto JG, Duker JS. Choroidal thickness in normal eyes measured using Cirrus HD optical coherence tomography. Am J Ophthalmol 2010; 150:325–329.
Kumar V, Kumawat D, Kumar P. Swept source optical coherence tomography analysis of choroidal thickness in macular telangiectasia type 2: a case-control study. Graefes Arch Clin Exp Ophthalmol 2019; 257:567–573.
Ogawa Y, Maruko I, Koizumi H, Iida T. Quantification of choroidal vasculature by high-quality en face swept-source optical coherence tomography images in eyes with central serous chorioretinopathy. Retina 2018; 38:1–8.
Lee HK, Lim JW, Shin MC. Comparison of choroidal thickness in patients with diabetes by spectral-domain optical coherence tomography. Korean J Ophthalmol 2013; 27:433–439.
Li XQ, Larsen M, Munch IC. Subfoveal choroidal thickness in relation to sex and axial length in 93 Danish university students. Invest Ophthalmol Vis Sci 2011; 52:8438–8441.
Adhi M, Brewer E, Waheed NK, Duker JS. Analysis of morphological features and vascular layers of choroid in diabetic retinopathy using spectral-domain optical coherence tomography. JAMA Ophthalmol 2013; 131:1267–1274.
Unsal E, Eltutar K, Zirtiloğlu S, Dinçer N, Ozdoğan Erkul S, Güngel H. Choroidal thickness in patients with diabetic retinopathy. Clin Ophthalmol 2014; 8:637–642.
Abadia B, Suñen I, Calvo P, Bartol F, Verdes G, Ferreras A. Choroidal thickness measured using sweptsource optical coherence tomography is reduced in patients with type 2 diabetes. PLoS One 2018; 13:e0191977.
Wang JC, Laíns I, Providência J, Armstrong GW, Santos AR, Gil P et al.
Diabetic choroidopathy: choroidal vascular density and volume in diabetic retinopathy with swept-source optical coherence tomography. Am J Ophthalmol. 2017; 184:75–83.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]