|Year : 2018 | Volume
| Issue : 4 | Page : 1105-1109
Changes in choroidal thickness in diabetic retinopathy
Khaled El-Ghonemy1, Ghada Z Al Abeden Rajab1, Asmaa M Ibrahim1, Ibrahim M Ibrahim Gohar2
1 Ophalmology Department, Faculty of Medicine, Minoufia University, Shebeen El-Kom, Egypt
2 Ophalmology Department, Damanhour Eye Hospital, Damanhour, Egypt
|Date of Submission||25-Mar-2017|
|Date of Acceptance||09-May-2017|
|Date of Web Publication||14-Feb-2019|
Ibrahim M Ibrahim Gohar
Gwad Hosny Street, Damanhour 22516, Al-Behira
Source of Support: None, Conflict of Interest: None
The aim of this study was to evaluate choroidal thickness (CT) in patients with diabetic retinopathy (DR) and normal individuals.
Data were collected from Medline databases (PubMed, Medscape, Science Direct, and EMF-Portal) and all materials available in the Internet from 2004 to 2015.
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.
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.
Comparisons were made using structured review with the results tabulated.
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.
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|| |
Diabetic retinopathy (DR) is a leading cause of vision loss worldwide. DR alone accounts for at least 12% of new cases of blindness each year in the USA. The development of macular edema and proliferative retinopathy are major causes of visual impairment,. 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,,.
Various choroidal abnormalities, including obstruction of the choriocapillaris, vascular degeneration, choroidal aneurysms, and choroidal neovascularization, have been reported in histopathologic studies of diabetic eyes,,.
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,.
Indocyanine green angiography reveals both hyperfluorescent and hypofluorescent spots in diabetic eyes, although the significance is unknown,. 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,. 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,,,.
Concurrently, Shiragami et al. 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). There was a more prominent decrease in flow in the case of PDR.
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,.
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,,. 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,.
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.|
Click here to view
| Materials and Methods|| |
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.
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.
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|
Click here to view
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.
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.
A structured systematic review was performed with the results tabulated.
| Results|| |
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.
Effect of diabetic retinopathy on choroidal thickness
The effect of DR on CT was examined in all studies [Table 1],,,,.
Three studies of all five studies found a significant decrease in the mean subfoveal CT with progression of DR,,. The changes in CT occurred in both vertical and horizontal scans.
Two studies detected a nonsignificant decrease in CT,.
Effect of diabetic macular edema on choroidal thickness
The effect of DME on CT was examined in four studies [Table 2],,,.
All studies found a significant decrease in the CT in DME. The changes in the CT occurred in both vertical and horizontal scans,,,.
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|| |
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.
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.
Recently, the emergence of SD-OCT has allowed the assessment of the choroidal cross-sectional structure and its thickness. EDI can provide a better view of the choroidoscleral interface by bringing the choroid closer to the zero-delay line.
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. 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., 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. 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|| |
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
Conflicts of interest
There are no conflicts of interest.
| References|| |
Moss SE, Klein R, Klein BE. The 14-year incidence of visual loss in a diabetic population. Ophthalmology 1998; 105
Elsaadani AK, Marey HM, Badawy NM, Omran SF. Effects of diabetes mellitus on the eye. Menoufia Med J 2015; 28
Klein R, Klein BE, Moss SE, Cruickshanks KJ. The Wisconsin Epidemiologic Study of diabetic retinopathy. XIV. Ten-year incidence and progression of diabetic retinopathy. Arch Ophthalmol 1994; 112
Hidayat AA, Fine BS. Diabetic choroidopathy. Light and electron microscopic observations of seven cases. Ophthalmology 1985; 92
Weinberger D, Kramer M, Priel E, Gaton DD, Axer-Siegel R, Yassur Y. Indocyanine green angiographic findings in nonproliferative diabetic retinopathy. Am J Ophthalmol 1998; 126
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
Cao J, McLeod S, Merges CA, Lutty GA. Choriocapillaris degeneration and related pathologic changes in human diabetic eyes. Arch Ophthalmol 1998; 116
Fukushima I, McLeod DS, Lutty GA. Intrachoroidal microvascular abnormality: a previously unrecognized form of choroidal neovascularization. Am J Ophthalmol 1997; 124
Spaide RF, Koizumi H, Pozzoni MC. Enhanced depth imaging spectral-domain optical coherence tomography. Am J Ophthalmol 2008; 146
Coscas G, Zhou Q, Coscas F, Zucchiatti I, Rispoli M, Uzzan J, et al.
Choroid thickness measurement with RTVue optical coherence tomography in emmetropic eyes, mildly myopic eyes, and highly myopic eyes. Eur J Ophthalmol 2012; 22
Bartsch DU, Weinreb RN, Zinser G, Freeman WR. Confocal scanning infrared laser ophthalmoscopy for indocyanine green angiography. Am J Ophthalmol 1995; 120
Shiraki K, Moriwaki M, Kohno T, Yanagihara N, Miki T. Age-related scattered hypofluorescent spots on late-phase indocyanine green angiograms. Int Ophthalmol 1999; 23
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
Schocket LS, Brucker AJ, Niknam RM, Grunwald JE, DuPont J, Brucker AJ. Foveolar choroidal hemodynamics in proliferative diabetic retinopathy. Int Ophthalmol 2004; 25
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
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
Imamura Y, Fujiwara T, Margolis R, Spaide RF. Enhanced depth imaging optical coherence tomography of the choroid in central serous chorioretinopathy. Retina 2009; 29
Spaide RF. Age-related choroidal atrophy. Am J Ophthalmol 2009; 147
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
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
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
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
McCourt EA, Cadena BC, Barnett CJ, Ciardella AP, Mandava N, Kahook MY. Measurement of subfoveal choroidal thickness using spectral domain optical coherence tomography. Ophthalmic Surg Lasers Imaging 2010; 41(Suppl)
MacGregor LC, Rosecan LR, Laties AM, Matschinsky FM. Altered retinal metabolism in diabetes. I. Microanalysis of lipid, glucose, sorbitol, and myo-inositol in the choroid and in the individual layers of the rabbit retina. J Biol Chem 1986; 261
Yeoh J, Rahman W, Chen F, Hooper C, Patel P, Tufail A, et al.
Choroidal imaging in inherited retinal disease using the technique of enhanced depth imaging optical coherence tomography. Graefes Arch Clin Exp Ophthalmol 2010; 248
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2]