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 Table of Contents  
REVIEW ARTICLE
Year : 2018  |  Volume : 31  |  Issue : 4  |  Page : 1105-1109

Changes in choroidal thickness in diabetic retinopathy


1 Ophalmology Department, Faculty of Medicine, Minoufia University, Shebeen El-Kom, Egypt
2 Ophalmology Department, Damanhour Eye Hospital, Damanhour, Egypt

Date of Submission25-Mar-2017
Date of Acceptance09-May-2017
Date of Web Publication14-Feb-2019

Correspondence Address:
Ibrahim M Ibrahim Gohar
Gwad Hosny Street, Damanhour 22516, Al-Behira
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_224_17

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  Abstract 


Objective
The aim of this study was to evaluate choroidal thickness (CT) in patients with diabetic retinopathy (DR) and normal individuals.
Data sources
Data were collected from Medline databases (PubMed, Medscape, Science Direct, and EMF-Portal) and all materials available in the Internet from 2004 to 2015.
Study selection
The initial search presented 27 articles, of which five met the inclusion criteria. The articles studied the changes in the mean subfoveal choroidal thickness (SFCT) in different stages of DR.
Data extraction
If the studies did not fulfill the inclusion criteria, they were excluded. Study quality assessment included whether ethical approval was gained, eligibility criteria specified, appropriate controls, adequate information, and defined assessment measures.
Data synthesis
Comparisons were made using structured review with the results tabulated.
Findings
In total, five potentially relevant publications were included; three studies detected a significant decrease in SFCT with progression of DR. Some authors found a correlation between the presence of diabetic macular edema (DME) and changes in choroidal thickness. Three studies detected a significant decrease in SFCT in DME.
Conclusion
CT is altered in diabetes and may be related to the severity of retinopathy. The presence of DME is associated with a significant decrease in the CT.

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


How to cite this article:
El-Ghonemy K, Al Abeden Rajab GZ, Ibrahim AM, Ibrahim Gohar IM. Changes in choroidal thickness in diabetic retinopathy. Menoufia Med J 2018;31:1105-9

How to cite this URL:
El-Ghonemy K, Al Abeden Rajab GZ, Ibrahim AM, Ibrahim Gohar IM. Changes in choroidal thickness in diabetic retinopathy. Menoufia Med J [serial online] 2018 [cited 2019 Mar 22];31:1105-9. Available from: http://www.mmj.eg.net/text.asp?2018/31/4/1105/252030




  Introduction Top


Diabetic retinopathy (DR) is a leading cause of vision loss worldwide[1]. DR alone accounts for at least 12% of new cases of blindness each year in the USA[2]. The development of macular edema and proliferative retinopathy are major causes of visual impairment[1],[3]. A healthy choroid is essential for retinal function. Clinical and experimental findings suggested that choroidal vasculopathy in diabetes may play a role in the pathogenesis of DR[4],[5],[6].

Various choroidal abnormalities, including obstruction of the choriocapillaris, vascular degeneration, choroidal aneurysms, and choroidal neovascularization, have been reported in histopathologic studies of diabetic eyes[4],[7],[8].

There are few clinical studies on choroidal angiopathy in diabetes. This is because of the difficulty in imaging the choroid in vivo. Until recently, the choroid could only be evaluated by means of indocyanine green angiography, laser flowmetry, and ultrasonography. However, these techniques are only able to show choroidal vessel abnormalities and blood flow changes. They cannot show the three-dimensional anatomy of choroid layers or the retinal pigment epithelium[9],[10].

Indocyanine green angiography reveals both hyperfluorescent and hypofluorescent spots in diabetic eyes, although the significance is unknown[5],[11]. It has been proposed that the hypofluorescent spots result from ischemic changes of the choroidal vessels and represent either a dye-filling delay or a defect in the choriocapillaris[8],[12]. It is further postulated that the hyperfluorescent spots may be secondary to the presence of choroidal neovascularization, intrachoroidal microvasculature abnormalities, or nodules at the level of the choriocapillaris or underlying stroma[5],[6],[7],[11].

Concurrently, Shiragami et al.[6] described risk factors associated with diabetic choroidopathy, including the presence of severe DR, poor glycemic control, and the nature of the treatment regimen.

In addition, studies assessing the choroidal blood flow beneath the fovea with the use of laser Doppler flowmetry indicate a reduction in choroidal blood flow and volume in patients with nonproliferative diabetic retinopathy (NPDR) and proliferative diabetic retinopathy (PDR)[13]. There was a more prominent decrease in flow in the case of PDR[14].

A better clinical understanding of choroidal damage might be important for an accurate assessment of diabetic eye disease, but adequate visualization of the choroid using optical coherence tomography (OCT) has not been possible until recently, owing to its posterior location and the presence of pigmented cells that attenuate the incident light[15],[16].

Recent reports showed successful examination and measurement of choroidal thickness (CT) in normal and pathologic states using the Heidelberg Spectralis (Heidelberg Engineering, Heidelberg, Germany) and Cirrus HD-OCT (Carl Zeiss Meditec Inc., Dublin, California, USA) spectral-domain (SD) OCT instruments[17],[18],[19]. OCT is a noninvasive imaging modality, which is used in acquiring high-resolution sections of the retina. Recently, enhanced-depth imaging (EDI) SD-OCT has described that EDI software automatically captures a cross-sectional image with the choroid close to the zero-delay line to maximize sensitivity on the outer limit of the choroid[9],[10].

The present study was designed to determine whether CT is abnormal in patients with various stages of DR and diabetic macular edema (DME) [Figure 1].
Figure 1: Example for choroidal thickness measurement using enhanced-depth imaging spectral-domain optical coherence tomography.

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  Materials and Methods Top


Search strategy

This is meta analysis that doesn't need a patient consent as there is no patients in the study we reviewed papers on changes in CT in DR from Medline databases (PubMed, Medscape, and Science Direct) and also materials available in the Internet. We used diabetic retinopathy/diabetic macular edema/choroid/SFCT/EDI-OCT as searching terms. The search was performed in the electronic databases from 2008 to 2016.

Study selection

All studies were independently assessed for inclusion. They were included if they fulfilled the following criteria:

Inclusion criteria of the published studies:

  • Published in English language
  • Published in peer-reviewed journals
  • Discussed the relation between DR and CT
  • If a study had several publications on certain aspects we used the latest publication giving the most relevant data.


Data extraction

If the studies did not fulfill the above criteria, they were excluded:

  • Studies on changes in CT after any eye surgery or previous treatment for DR whether injection, laser, or surgery
  • CT in central or branch retinal vein occlusion
  • Age-related macular degeneration or choroidal neovascularization
  • Surveys about correlations between CT and age
  • Refractive errors and axial length not involving DR
  • Report without peer-review
  • Letters, comment, editorials, news, and studies not focused on the effect of DR on the choroid.


The analyzed publications were evaluated according to evidence-based medicine (EBM) criteria using the classification of the US Preventive Services Task Force and UK National Health Service protocol for EBM in addition to the Evidence Pyramid [Figure 2].
Figure 2: The pyramid of evidence-based medicine. RCT, randomized controlled trial. SR, systemic review. MA, meta analysis

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US Preventive Services Task Force

  • Level I: Evidence obtained from at least one properly designed randomized controlled trial
  • Level II-1: Evidence obtained from well-designed controlled trials without randomization
  • Level II-2: Evidence obtained from well-designed cohort or case–control analytic studies, preferably from more than one center or research group
  • Level II-3: Evidence obtained from multiple time series with or without the intervention. Dramatic results in uncontrolled trials might also be regarded as this type of evidence
  • Level III: Opinions of respected authorities, based on clinical experience, descriptive studies, or reports of expert committees.


Quality assessment

The quality of all studies was assessed. Important factors included study design, attainment of ethical approval, evidence of a power calculation, specified eligibility criteria, appropriate controls, adequate information, and specified assessment measures. It was expected that confounding factors would be reported and controlled and appropriate data analysis made in addition to an explanation of missing data.

Data synthesis

A structured systematic review was performed with the results tabulated.


  Results Top


Study selection and characteristics

In total, 27 potentially relevant publications were identified; 22 articles were excluded as they did not meet our inclusion criteria [Figure 3]. A total of five studies were included in the review as they were deemed eligible by fulfilling the inclusion criteria. All studies examined the effects of DR on CT. Four studies examined the effect of DME on CT. The studies were analyzed with respect to the study design using the classification of the US Preventive Services Task Force and UK National Health Service protocol for EBM.
Figure 3: Flow chart of study selection.

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Effect of diabetic retinopathy on choroidal thickness

The effect of DR on CT was examined in all studies [Table 1][13],[20],[21],[22],[23].
Table 1: Effect of diabetic retinopathy on choroidal thickness

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Three studies of all five studies found a significant decrease in the mean subfoveal CT with progression of DR[13],[21],[22]. The changes in CT occurred in both vertical and horizontal scans.

Two studies detected a nonsignificant decrease in CT[20],[23].

Effect of diabetic macular edema on choroidal thickness

The effect of DME on CT was examined in four studies [Table 2][13],[20],[21],[22].
Table 2: Effect of diabetic macular edema on choroidal thickness

Click here to view


All studies found a significant decrease in the CT in DME. The changes in the CT occurred in both vertical and horizontal scans[13],[20],[21],[22].

Correlation between changes in choroidal thickness with other variants

Many factors can affect changes in the CT in DR. Some of these factors are age, sex, hypertension, axial length, refractive error, and intraocular pressure. All authors took these factors in their consideration. Therefore, they do not consider these factors to have an extra effect on measurements.


  Discussion Top


Research into the effect of DR on different ocular structures is an area in which there is a significant number of scientific studies about its effect on the retina and the choroid. Most of these studies are about the effect of DR on pre-existing diseases. Other studies are about changes in SFCT with progression of DR. Therefore, this study tried to provide an update on the general status and briefly describes, classifies, and evaluates recent studies.

On reviewing the recent studies about the possible effects of DR on CT, we found that progression of stage of DR from mild, moderate to severe NPDR to PDRwas associated with a significant decrease in SFCT. Some studies have suggested that the presence of DME was associated with further decrease in SFCT.

A structurally and functionally normal choroidal vasculature is essential for the function of the retina. Abnormal choroidal blood volume and/or compromised flow can result in photoreceptor dysfunction and death[7].

The possible role of choroidal vessels in the pathophysiology of DR has been investigated in previous studies. It was found that similar metabolic changes affect the retinal and choroidal vascular beds and similar growth factors are produced and released in the diabetic choroid and retina. It was suggested that the choroidal vascular system is affected by diabetes and might in fact be involved in the pathogenesis of DR[24].

Recently, the emergence of SD-OCT has allowed the assessment of the choroidal cross-sectional structure and its thickness[15]. EDI can provide a better view of the choroidoscleral interface by bringing the choroid closer to the zero-delay line[25].

In this study, the authors aimed to compare the CT in patients with NPDR, PDR, and DME with healthy controls. The authors found that CT decreases as the disease progresses from mild, moderate, severe NPDR to PDR.

Regatieri et al.[20] compared NPDR, PDR, and DME patients with healthy controls using a Cirrus HD-OCT (Carl Zeiss Meditec Inc.) and reported no significant difference between the NPDR and control groups, but that the CT decreased in the DME groups.

In the study by Kim et al.[21], CT was found to be significantly increased as the disease progressed in severity from moderate–severe NPDR to untreated PDR. In our study, the CT of patients with DME was significantly thinner than that of non-DME patients.

Nagaoka et al.[13] showed that NPDR patients with DME have a reduction in choroidal circulation compared with NPDR patients without DME. They presumed this decreased circulation could be secondary to retinal hypoxia because of the inadequate blood flow and that this could cause the macular edema.

In the present study, CT was the thickest in the subfoveal area and became thinner toward the nasal and temporal areas.

SD-OCT is a successful noninvasive device to evaluate the choroid. Especially in DR, it can be a useful device to evaluate blood flow changes in the choroid. To understand the role of the choroid in DR and its pathophysiology, more prospective studies should be conducted.


  Conclusion Top


CT is altered in diabetes and related to the severity of retinopathy. Presence of DME is associated with a significant decrease in the CT. SD-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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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.  Back to cited text no. 13
    
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    Figures

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

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