- Research article
- Open access
- Published:
Comparison of the morphological characteristics of the choroidal sublayer between idiopathic macular holes and epiretinal membranes with automatic analysis
BMC Ophthalmology volume 23, Article number: 277 (2023)
Abstract
Purpose
To compare the choroidal sublayer morphologic features between idiopathic macular hole (IMH) and idiopathic epiretinal membrane (iERM) on spectral-domain optical coherent tomography (SD-OCT) using an automatic segmentation model.
Methods
Thirty-three patients with idiopathic IMHs and 44 with iERMs who underwent vitrectomies were involved. The enhanced depth imaging mode of SD-OCT was used to obtain the B-scan image after single line scanning of the macular fovea. The choroidal sublayer automatic analysis model divides the choroidal into the choroidal large vessel layer, the middle vessel layer and the small vessel layer (LVCL, MVCL and SVCL, respectively) and calculates the choroidal thickness (overall, LVCL, MVCL and SVCL) and vascular index (overall, LVCL, MVCL and SVCL). The morphological characteristics of the choroidal sublayer in the ERM eyes and the IMH eyes were compared.
Results
The mean choroidal thickness in the macular centre of the IMH eyes was significantly thinner than that of the ERM eyes (206.35 ± 81.72 vs. 273.33 ± 82.31 μm; P < 0.001). The analysis of the choroidal sublayer showed that the MVCL and SVCL macular centres and 0.5–1.5 mm of the nasal and temporal macula were significantly thinner in the IMH eyes than in the ERM eyes (P < 0.05), and there was a difference in the macular centre of the LVCL between the two groups (P < 0.05). In contrast, the choroidal vascular index of the macular centre in the IMH eyes was significantly higher than that in iERM eyes (0.2480 ± 0.0536 vs. 0.2120 ± 0.0616; P < 0.05). There was no significant difference in the CVI of other parts of the macula, the LVCL or MVCL between the two groups.
Conclusion
The choroidal thickness of the IMH eyes was significantly thinner than that of the iERM eyes, which was mainly observed in 3Â mm of the macular centre and the MVCL and SVCL layers of the choroid. The choroidal vascular index of the IMH eyes was higher than that of the iERM eyes. These findings suggest that the choroid may be involved in the pathogenesis of IMH and iERM.
Key messages
1. The pathogeneses of idiopathic macular hole (IMH) and idiopathic epiretinal membrane (iERM) are closely related to the relationship between the vitreous and the macula. Changes in the choroid are likely to be related to local pathological changes in the macula.
2. The choroidal thickness of the IMH eyes was significantly thinner than that of the iERM eyes, which was mainly observed in 3Â mm of the macular centre and the middle and small vessel layers of the choroid.
3. The choroidal vascular index of the IMH eyes was higher than that of the iERM eyes. These findings suggest that the choroid may be involved in the pathogenesis of IMH and iERM.
Introduction
An idiopathic macular hole (IMH) and idiopathic epiretinal membrane (iERM) are common manifestations in the macula in elderly individuals. IMHs are retinal defects in the fovea [1], and approximately two-thirds of affected patients are women [2]. It has been reported that the incidence rate of IMH in the general population is between 0.2% and 0.8% [3, 4]. An idiopathic epiretinal membrane is a fibrocellular proliferation at the vitreoretinal interface on the inner retinal surface, which leads to visual impairment or metamorphopsia. The prevalence of iERM did not differ significantly between men and women [5,6,7]. Population studies have shown that the overall iERM prevalence ranges from 7% to 11.8%, while the 5-year incidence is 5.3% [8,9,10]. An IMH and the iERM have similar appearances when they occur in the macular region; both are related to age, especially in elderly individuals. There was no pathological process of neovascularization in both diseases. The key point is that the pathogenesis of both is closely related to the relationship between the vitreous and the macula.
The possible pathogenesis of an IMH is related to the abnormal adhesion of the vitreous and macula. The posterior vitreous cortex applies direct anterior and posterior traction to the macular fovea [1, 11, 12]. An abnormal vitreous macular adhesion produces dynamic traction, and the longitudinal contraction of collagen fibres leads to progressive forward traction until a hole develops [13,14,15]. Posterior vitreous detachment (PVD) plays a critical role in the pathogenesis of the iERM [5, 16, 17]. The residual vitreous remnants on the retinal surface after PVD development, including hyalocytes, provide a medium for proliferation and transdifferentiation of glial cells. These hyalocytes stimulate Müller cells to send the process through an intact inner limiting membrane (ILM) to form a scaffold. Activated Müller glial cells lead to the formation of the preretinal membrane [18].
The macular fovea is a nonvascular area, and 100% of its blood supply comes from the choroid. Therefore, macular disease may affect choroidal blood flow and thus choroidal thickness. Similarly, changes in choroidal blood flow and thickness may also affect macular disease. The difference in choroidal function between IMH eyes and iERM eyes may be related to the different clinical manifestations of the two macular diseases. At present, choroidal thickness and blood flow is measured in vivo by OCT. The measured parameters include choroidal thickness and choroidal vascular index (CVI). Enhanced depth imaging (EDI-OCT) has allowed more accurate evaluation of choroidal thickness, provides detailed information about the choroid, and makes highly reliable and repeatable measurements of choroidal thickness [19, 20]. In addition, the CVI is another choroidal vascular marker based on EDI-OCT. It is calculated as the ratio of the vascular area to the matrix area by the image binarization method [21]. It is considered to be a more reliable parameter than choroidal thickness [22]. In contrast to choroidal thickness, it has been reported that the CVI is not affected by many biological variables, such as intraocular pressure, axial length, diurnal variation, and refractive error [23].
Many studies have observed the relationship between an IMH, the iERM and choroidal thickness. EDI-OCT has been used to compare the choroidal thickness [24,25,26] between IMH patients and control groups. The results showed that the choroid became thinner in the patients with IMHs, suggesting that the decrease in choroidal blood flow may be related to the presence of an IMH. The relationship between the choroid and the iERM is unclear. Previous studies have observed choroidal thinning in newly developed or significantly progressed iERM eyes and choroidal thickening in spontaneously resolved iERM eyes [27]. Several studies have found that choroidal thickness decreases after vitrectomy and that the iERM peels [28, 29]. Studies have found that the choroidal thickness of the iERM with contraction is significantly thickened [30]. Other studies found that there was no significant change in the CVI in iERM patients [31]. These studies show that the choroid is involved in the occurrence and development of an IMH and the iERM.
Due to the similarity between an IMH and the iERM and their relationship with the choroid, the comparison of the choroidal structure between an IMH and the iERM is helpful to understand the occurrence and development of an IMH and the iERM. To the best of our knowledge, there is no comparison of choroidal structures between an IMH and the iERM. In this study, we conducted a retrospective study using a new choroidal sublayer segmentation model based on deep learning to compare the choroidal sublayer thickness and CVI of an IMH and the iERM to observe the different morphological characteristics of the foveal choroidal sublayer in the two macular diseases and the possible relationship between the two diseases.
Subjects and methods
We retrospectively analysed the medical records of patients who underwent vitrectomy for an IMH and an iERM at the Ophthalmology Department of Peking University First Hospital between 1 January 2017, and 30 June 30 2021. The inclusion criteria were as follows: 1) IMH and iERM were diagnosed by OCT and treated with vitrectomy; 2) clear ocular media; and 3) a high-quality image was acquired to precisely measure choroidal thickness. The exclusion criteria were as follows: eyes with myopia of more than 6 dioptres; ocular trauma or tumour; eyes with other ocular pathologic features that could have interfered with functional results (such as glaucoma, previous uveitis, visually significant cataract or age-related macular degeneration); history of intravitreal drug injection, retinal surgery or refractive surgery; history of systemic corticosteroid use; or any systemic disease affecting the eyes. The Institutional Review Board waived the need for patient consent for this retrospective study (Peking University First Hospital No:2022–312).
All patients underwent a comprehensive ophthalmic assessment, including best corrected visual acuity, slit lamp biomicroscopy, intraocular pressure (IOP) measurement, fundus examination, refractive error examination (rm8900; TOPCON) and axial length measurement (Carl Zeiss Meditec AG, Jena, Germany). Snellen visual acuities were converted to the logarithm of the minimal angle of resolution (log-MAR) for statistical analysis.
Measurement of choroidal thickness and CVI
OCT images of IMH and iERM before surgery were used for analysis. The EDI mode of SD-OCT (Heidelberg Engineering, Heidelberg, Germany) was used to obtain the B-scan image after single-line scanning of macular fovea. A single B-scan consists of 768 A-scans (high-speed mode). To improve the signal-to-noise ratio, automatic real-time tracking is adopted. The B-scan images of single line scanning are composed of 100 two-dimensional images, which can improve the clarity of the image and remove the image artefacts. The OCT B-scan image set needs to have sufficient quality to analyse the choroid, and the quality of the images included in the study is greater than 28. The diagnosis and staging of IMH were determined according to the classification by Gass [1]. The ERM was classified into four stages by spectral-domain optical coherence tomography as previously described by Govetto et al. [32].
The cross-sectional structure of the choroid can be displayed on EDI-OCT B-scan images. To study the morphological characteristics of the choroidal sublayer, according to the previously reported automatic analysis model of the choroidal sublayer [33], the choroid was divided into large, medium, and small vessel choroidal layers (LVCL, MVCL and SVCL, respectively), and the choroidal thickness (overall, LVCL, MVCL and SVCL) and vascular index (overall, LVCL and MVCL) were calculated. The measurement range is shown in Fig. 1.
There are 5 areas in total. The width of each area in the horizontal direction is 1 mm. The average choroidal thickness and CVI of each area were calculated. The middle position is the macular fovea. BM, Bruch’s membrane; CSI, choroidoscleral interface; SVCL-MVCL interface, interface of small-vessel choroidal layer and medium-vessel choroidal layer; MVCL-LVCL interface, interface of medium-vessel choroidal layer and large-vessel choroidal layer.
Statistical analysis
The data were processed and analysed statistically using SPSS statistical software for Windows, version 23.0 (IBM Corp., Armonk, NY, USA). All values are presented as the mean ± standard deviation (SD). Categorical variables were assessed using the chi-square test, and the independent sample t test was used to evaluate differences in continuous variables for normally distributed variables. A value of P < 0.05 was considered statistically significant.
Results
Demographic data of the subjects
Thirty-three eyes of 33 patients (22 females, 11 males) with full-thickness IMHs (3 eyes in stage 2, 11 eyes in stage 3 and 19 eyes in stage 4) and 44 eyes of 44 patients (25 females, 19 males) with iERM (1 eye in stage 2, 19 eyes in stage 3 and 24 eyes in stage 4) were examined. The mean age of IMH patients was 67.12 ± 6.38 years and that of iERM patients was 69.43 ± 7.84 years. The IOP of IMH patients was 17.70 ± 1.86 mmHg, while that of iERM patients was 17.07 ± 2.35 mmHg. The AL of the IMH patients was 23.61 ± 0.91 mm, while that of the iERM patients was 23.28 ± 0.90 mm. The demographic and clinical characteristics of the patients are summarized and compared in Table 1. The BCVA measurements were significantly different between the 2 groups (P < 0.001), and there was no statistically significant difference in age, percentage of women, IOP, or AL between the 2 groups.
Macular choroidal thickness measurements
In the measured area, the central choroidal thickness (1 mm in the centre) in the IMH patients was almost the thinnest; in contrast, that of the iERM patients was the thickest, and the thickness generally decreased away from the fovea. The mean central choroidal thickness was 206.35 ± 81.72 µm in the IMH group and 273.33 ± 82.31 µm in the iERM group, with a statistically significant difference (P < 0.001). Table 2 shows the central choroidal thickness and the thickness of the nasal and temporal choroids 0.5–1.5 mm and 1.5–2.5 mm from the fovea of the two groups. The comparison of choroidal thickness between the two groups showed that the choroidal thickness of the central side, 0.5–1.5 mm, in the nasal and temporal sides in the IMH patients was significantly thinner than that in the iERM group (all P < 0.05). The choroidal thickness of 1.5–2.5 mm in the nasal and temporal sides in the IMH group was thinner than that in the iERM group, but there was no significant difference (P > 0.05). In further analysis of the thickness of the sublayers of the choroid, the thickness of the LVCL of the central choroidal thickness in the IMH group was thinner than that in the iERM group (P < 0.05), and there was no difference in the thickness of the other parts (P > 0.05). For the thickness of the MVCL, there was no difference from 1.5–2.5 mm on the temporal side, and the thickness of the other four parts in the IMH group was thinner than that in the iERM group (P < 0.05). The comparison of the SVCL thickness was consistent with that of the overall thickness. The representative figures of IMH and ERM are shown in Fig. 2.
The choroidal thickness in the macular centre of the IMH eyes was thinner than that of the iERM eye. From top to bottom, each column of data (white) represents the overall choroidal thickness, thickness of the LVCL, thickness of the MVCL, and thickness of the SVCL. BM, Bruch’s membrane; CSI, choroidoscleral interface; LVCL, large-vessel choroidal layer; MVCL, medium-vessel choroidal layer; SVCL, small-vessel choroidal layer.
Macular CVI measurements
The mean CVI of the central choroid was 0.2480 ± 0.0536 in the IMH group, which was significantly higher than that in the iERM group (0.2120 ± 0.0616) (P < 0.05). The comparison of the CVI in other parts of the macula and the CVI in the LVCL and MVCL between the two groups showed no significant difference (all P > 0.05) (Table 3). The CVI of SVCL could not be detected.
Discussion
The pathogeneses of IMH and iERM are closely related to the relationship between the vitreous and the macula. The difference between them is whether there is an abnormal adhesion in the vitreous macular region when posterior vitreous detachment occurs. The local pathological changes in the macula may be closely related to the exclusive occurrence of an abnormal adhesion in the macula. Changes in the choroid are likely to be related to local pathological changes in the macula. Previous studies have shown that chorioretinopathy involving the macula associated with choroidal thickening includes central serous chorioretinopathy, polypoid chorioretinopathy and Vogt Koyanagi Harada [34,35,36], while age-related macular degeneration, diabetic retinopathy, pathological myopia, and retinal dystrophy lead to a decrease in choroidal thickness [37,38,39,40,41].
The choroidal thickness measurement is affected by many factors, such as imaging time, refractive error, age, axial length, and sex. In this study, there was no difference in age or sex composition between the IMH and iERM groups. Axial length in the iERM group was shorter than that in the IMH group, but there was no significant difference. Therefore, the factors affecting choroidal thickness in the two groups were comparable. Most previous studies on idiopathic macular hole and choroidal thickness showed that the choroidal thickness was thinner than that of normal people. Although some studies did not correct the influencing factors of the choroid, such as axis length [24, 25], the same conclusion was reached in some studies that corrected axis length [4, 26]. The relationship between the iERM and choroidal thickness has not been determined. Some studies have found that the thickness of the iERM with traction is greater than that of the normal control group [30], but many studies have not found a relationship between the iERM and choroidal thickness [28, 29, 31]. Our results show that choroidal thickness in patients with IMH is lower than that in patients with ERM, with comparable ages and axial lengths, which is consistent with previous results.
Studies have shown that, although the choroidal thickness in the macular area of an IMH is thinner, the central thickness of the macula is still the thickest in the macular area [4, 24], and choroidal thickness was measured manually, rather than automatically calculated via the software instrument. Our study found that the choroidal thickness of 1Â mm around the macular fovea is almost the thinnest in the macular area. Since our study measured the average thickness of 1Â mm under the macular fovea of patients undergoing vitrectomy with an automatic analysis model, such inconsistency may be related to the method of measurement used and the composition of IMH patients.
The choroidal measurement method used in this study is an automatic recognition system based on deep learning choroidal sublayer thickness and CVI, which can measure choroidal thickness in different parts of the macula and choroidal thickness in different vascular layers [33] The results show that the choroidal thickness within 1.5 mm around the fovea in the IMH group is thinner than that in the iERM group, but there is no difference in the choroidal thickness 1.5–2.5 mm away from the fovea between the two groups, The choroidal thickness in the sublayers was analysed and showed that the thinning of the LVCL occurred within 1 mm of the fovea in the centre of the macula in the IMH group, and the thinning of MVCL and SMCL were basically consistent with the thinning of the whole choroid. These results showed that, compared with iERM, choroidal thinning of IMH mainly occurred in the MVCL and SVCL in the centre of the macula.
We also compared the CVI in the macular region between the two groups. The results showed that the CVI in the IMH group was higher than that in the iERM group within 1Â mm of the macular fovea. The analysis of other parts and LVCL and MVCL showed that there was no difference in the CVI between the two groups. These results suggest that the increase in the CVI in IMH patients may mainly occur in the SVCL in the centre of the macula, which is roughly consistent with the thinning of choroidal thickness. We analysed the possible reasons why the CVI in the IMH group was higher than that in the iERM group. One is that the thinning of foveal choroidal thickness may mainly occur in the matrix, and the other is the compensatory change in the choroidal microvessels after the thinning of foveal choroidal thickness.
The results of this study show that after excluding influencing factors such as age, sex and axial length, the choroidal thickness of IMH is significantly lower than that of iERM, indicating that the difference in choroidal thickness is an independent influencing factor between these two vitreo-macular interface disorders. Our study and most previous studies are cross-sectional, so a causal relationship could not be determined. It has been found that changes in choroidal blood perfusion occur before the complete formation of macular holes [42]. Some authors also conducted a prospective study on patients with macular thinning and found that 86% (6/7) of patients with macular thinning, pigment epithelial window defects and no PVD developed a macular hole [43]. These results show that the structural changes in the macula are closely related to the occurrence of IMH.
In view of the above results, we found that changes in choroidal thickness play an important role in the pathogenesis of IMH and iERM. First, the normal choroidal thickness in patients with iERM indicates that the blood and oxygen supply of the choroid is basically normal. Its effect on the vitreous body may be due to the ageing of the vitreous body caused by the relatively normal metabolism of the choroidal retina and the occurrence of PVD, which may lead to the formation of the iERM. Second, macular choroidal thickness decreased in patients with IMHs. Although there may be compensatory changes in choroidal vessels, they may still affect the metabolism of the macula. The local metabolic abnormality of the macula may lead to the adhesion of the vitreous macula, resulting in a macular hole. Another disease of macular choroidal thickness reduction and abnormal adhesion of the vitreoretinal region is high myopia. The macular complication of high myopia is also due to the adhesion and traction of the vitreous to the macula, resulting in retinoschisis and a macular hole [44, 45].
There are a few limitations in our study. First, this group of cases is a retrospective study of patients who underwent vitrectomy. Most patients are in the later stage of the disease, which may lead to selection bias. Second, there were relatively few cases in this group, which were not compared with the normal control group and need to be supplemented by follow-up research. Thirdly, functional parts of the choroid can be evaluated by using ICGA and OCTA; however, these are not routine examinations in our hospital. Therefore, we did not conduct any such analyses.
In summary, we concluded that the choroidal thickness of an IMH was significantly thinner than that of the ERM, which was mainly manifested in 3Â mm in the macular centre and the MVCL and SVCL layers of the choroid after excluding influencing factors such as age, sex, and axial length. The choroidal vascular index of an IMH was higher than that of the iERM. These findings suggest that the choroid may be involved in the pathogenesis of IMH and iERM.
Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Gass JD. Idiopathic senile macular hole. Its early stages and pathogenesis. Arch Ophthalmol. 1988;106:629–39. https://doi.org/10.1001/archopht.1988.01060130683026.
Kelly NE, Wendel RT. Vitreous surgery for idiopathic macular holes. Results of a pilot study. Arch Ophthalmol. 1991;109:654–9. https://doi.org/10.1001/archopht.1991.01080050068031.
Johnson RN, Gass JD. Idiopathic macular holes. Observations, stages of formation, and implications for surgical intervention. Ophthalmology. 1988;95:917–24. https://doi.org/10.1016/s0161-6420(88)33075-7.
Zhang P, Zhou M, Wu Y, Lu B, Li T, Zhao J, Wang F, Sun X. CHOROIDAL THICKNESS IN UNILATERAL IDIOPATHIC MACULAR HOLE: A Cross-Sectional Study and Meta-Analysis. Retina. 2017;37:60–9. https://doi.org/10.1097/IAE.0000000000001118.
Bu SC, Kuijer R, Li XR, Hooymans JM, Los LI. Idiopathic epiretinal membrane. Retina. 2014;34(12):2317–35. https://doi.org/10.1097/IAE.0000000000000349.
Fraser-Bell S, Ying-Lai M, Klein R, Varma R; Los Angeles Latino Eye Study. Prevalence and associations of epiretinal membranes in latinos: the Los Angeles Latino Eye Study. Invest Ophthalmol Vis Sci. 2004;45:1732–6. https://doi.org/10.1167/iovs.03-1295.
Semeraro F, Morescalchi F, Duse S, Gambicorti E, Russo A, Costagliola C (2015) Current Trends about Inner Limiting Membrane Peeling in Surgery for Epiretinal Membranes. J Ophthalmol. 2015: 671905. https://doi.org/10.1155/2015/671905
Fraser-Bell S, Guzowski M, Rochtchina E, Wang JJ, Mitchell P. Five-year cumulative incidence and progression of epiretinal membranes: the Blue Mountains Eye Study. Ophthalmology. 2003;110:34–40. https://doi.org/10.1016/s0161-6420(02)01443-4.
Ng CH, Cheung N, Wang JJ, Islam AF, Kawasaki R, Meuer SM, Cotch MF, Klein BE, Klein R, Wong TY. Prevalence and risk factors for epiretinal membranes in a multi-ethnic United States population. Ophthalmology. 2011;118:694–9. https://doi.org/10.1016/j.ophtha.2010.08.009.
Klein R, Klein BE, Wang Q, Moss SE. The epidemiology of epiretinal membranes. Trans Am Ophthalmol Soc. 1994;92:403–25 Discussion 425–443.
Kakehashi A, Schepens CL, Trempe CL. Vitreomacular observations. II. Data on the pathogenesis of idiopathic macular breaks. Graefes Arch Clin Exp Ophthalmol. 1996;234:425–33. https://doi.org/10.1007/BF02539408.
Takezawa M, Toyoda F, Kambara C, Yamagami H, Kakehashi A (2011) Clarifying the mechanism of idiopathic macular hole development in fellow eyes using spectral-domain optical coherence tomography. Clin Ophthalmol. 20;5:101–108. https://doi:https://doi.org/10.2147/OPTH.S16549
Woon WH, Greig D, Savage MD, Wilson MC, Grant CA, Mokete B, Bishop F. Movement of the inner retina complex during the development of primary full-thickness macular holes: implications for hypotheses of pathogenesis. Graefes Arch Clin Exp Ophthalmol. 2015;253:2103–9. https://doi.org/10.1007/s00417-015-2951-0.
Hee MR, Puliafito CA, Wong C, Duker JS, Reichel E, Schuman JS, Swanson EA, Fujimoto JG. Optical coherence tomography of macular holes. Ophthalmology. 1995;102:748–56. https://doi.org/10.1016/s0161-6420(95)30959-1.
Spaide RF, Wong D, Fisher Y, Goldbaum M. Correlation of vitreous attachment and foveal deformation in early macular hole states. Am J Ophthalmol. 2002;133:226–9. https://doi.org/10.1016/s0002-9394(01)01377-0.
Kampik A. Pathology of epiretinal membrane, idiopathic macular hole, and vitreomacular traction syndrome. Retina. 2012;32(Suppl 2):S194-198. https://doi.org/10.1097/IAE.0b013e31825bc20a. (discussion S198-9).
Johnson MW. Posterior vitreous detachment: evolution and complications of its early stages. Am J Ophthalmol. 2010;149:371-382.e1. https://doi.org/10.1016/j.ajo.2009.11.022.
Bringmann A, Wiedemann P. Involvement of Müller glial cells in epiretinal membrane formation. Graefes Arch Clin Exp Ophthalmol. 2009;247:865–83. https://doi.org/10.1007/s00417-009-1082-x.
Michalewska Z, Michalewski J, Nawrocka Z, Dulczewska-Cichecka K, Nawrocki J. Suprachoroidal layer and suprachoroidal space delineating the outer margin of the choroid in swept-source optical coherence tomography. Retina. 2015;35:244–9. https://doi.org/10.1097/IAE.0000000000000281.
Ikuno Y, Maruko I, Yasuno Y, Miura M, Sekiryu T, Nishida K, Iida T. Reproducibility of retinal and choroidal thickness measurements in enhanced depth imaging and high-penetration optical coherence tomography. Invest Ophthalmol Vis Sci. 2011;52:5536–40. https://doi.org/10.1167/iovs.10-6811.
Branchini LA, Adhi M, Regatieri CV, Nandakumar N, Liu JJ, Laver N, Fujimoto JG, Duker JS. Analysis of choroidal morphologic features and vasculature in healthy eyes using spectral-domain optical coherence tomography. Ophthalmology. 2013;120:1901–8. https://doi.org/10.1016/j.ophtha.2013.01.066.
Agrawal R, Gupta P, Tan KA, Cheung CM, Wong TY, Cheng CY. Choroidal vascularity index as a measure of vascular status of the choroid: Measurements in healthy eyes from a population-based study. Sci Rep. 2016;6:21090. https://doi.org/10.1038/srep21090.
Singh SR, Vupparaboina KK, Goud A, Dansingani KK, Chhablani J. Choroidal imaging biomarkers. Surv Ophthalmol. 2019;64:312–33. https://doi.org/10.1016/j.survophthal.2018.11.002.
Reibaldi M, Boscia F, Avitabile T, Uva MG, Russo V, Zagari M, Bonfiglio V, Reibaldi A, Longo A. Enhanced depth imaging optical coherence tomography of the choroid in idiopathic macular hole: A cross-sectional prospective study. Am J Ophthalmol. 2011;151:112-117.e2. https://doi.org/10.1016/j.ajo.2010.07.004.
Zeng J, Li J, Liu R, Chen X, Pan J, Tang S, Ding X. Choroidal thickness in both eyes of patients with unilateral idiopathic macular hole. Ophthalmology. 2012;119:2328–33. https://doi.org/10.1016/j.ophtha.2012.06.008.
Xu LT, Srivastava SK, Ehlers JP, Kaiser PK. Choroidal thickness in macular holes: a case-control study. Ophthalmic Surg Lasers Imaging Retina. 2015;46:33–7. https://doi.org/10.3928/23258160-20150101-05.
Choi EY, Han J, Lee SC, Lee CS. Macular Choroidal Thickness Changes in Development, Progression, and Spontaneous Resolution of Epiretinal Membrane. Ophthalmic Surg Lasers Imaging Retina. 2019;50:627–34. https://doi.org/10.3928/23258160-20191009-05.
Michalewska Z, Michalewski J, Adelman RA, Zawiślak E, Nawrocki J. Choroidal thickness measured with swept source optical coherence tomography before and after vitrectomy with internal limiting membrane peeling for idiopathic epiretinal membranes. Retina. 2015;35:487–91. https://doi.org/10.1097/IAE.0000000000000350.
Michalewska Z, Michalewski J, Ornafel-Sagan K, Nawrocki J. Swept-Source Optical Coherence Tomography Correlations Between Retina and Choroid Before and After Vitrectomy for Epiretinal Membranes. Am J Ophthalmol. 2016;165:100–7. https://doi.org/10.1016/j.ajo.2016.02.003.
Fang IM, Chen LL. Association of macular choroidal thickness with optical coherent tomography morphology in patients with idiopathic epiretinal membrane. PLoS ONE. 2020;15(9):e0239992. https://doi.org/10.1371/journal.pone.0239992.
Gediz BS, Doguizi S, Ozen O, Sekeroglu MA. Is choroidal vascularity index a useful marker in different stages of idiopathic epiretinal membranes? Photodiagnosis Photodyn Ther. 2021;33:102110. https://doi.org/10.1016/j.pdpdt.2020.102110.
Govetto A, Lalane RA 3rd, Sarraf D, Figueroa MS, Hubschman JP. Insights Into Epiretinal Membranes: Presence of Ectopic Inner Foveal Layers and a New Optical Coherence Tomography Staging Scheme. Am J Ophthalmol. 2017;175:99–113. https://doi.org/10.1016/j.ajo.2016.12.006.
Li J, Zhu L, Zhu R, Lu Y, Rong X, Zhang Y, Gu X, Wang Y, Zhang Z, Ren Q, Rong B, Yang L. Automated Analysis of Choroidal Sublayer Morphologic Features in Myopic Children Using EDI-OCT by Deep Learning. Transl Vis Sci Technol. 2021;10:12. https://doi.org/10.1167/tvst.10.13.12.
Kuroda S, Ikuno Y, Yasuno Y, Nakai K, Usui S, Sawa M, Tsujikawa M, Gomi F, Nishida K. Choroidal thickness in central serous chorioretinopathy. Retina. 2013;33:302–8. https://doi.org/10.1097/IAE.0b013e318263d11f.
Kim SW, Oh J, Kwon SS, Yoo J, Huh K. Comparison of choroidal thickness among patients with healthy eyes, early age-related maculopathy, neovascular age-related macular degeneration, central serous chorioretinopathy, and polypoidal choroidal vasculopathy. Retina. 2011;31:1904–11. https://doi.org/10.1097/IAE.0b013e31821801c5.
Nakayama M, Keino H, Okada AA, Watanabe T, Taki W, Inoue M, Hirakata A. Enhanced depth imaging optical coherence tomography of the choroid in Vogt-Koyanagi-Harada disease. Retina. 2012;32:2061–9. https://doi.org/10.1097/IAE.0b013e318256205a.
Jirarattanasopa P, Ooto S, Nakata I, Tsujikawa A, Yamashiro K, Oishi A, Yoshimura N. Choroidal thickness, vascular hyperpermeability, and complement factor H in age-related macular degeneration and polypoidal choroidal vasculopathy. Invest Ophthalmol Vis Sci. 2012;53:3663–72. https://doi.org/10.1167/iovs.12-9619.
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. https://doi.org/10.1097/IAE.0b013e31822f5678.
El Matri L, Bouladi M, Chebil A, Kort F, Bouraoui R, Largueche L, Mghaieth F. Choroidal thickness measurement in highly myopic eyes using SD-OCT. Ophthalmic Surg Lasers Imaging. 2012;43(6 Suppl):S38-43. https://doi.org/10.3928/15428877-20121001-02.
Sodi A, Lenzetti C, Murro V, Caporossi O, Mucciolo DP, Bacherini D, Cipollini F, Passerini I, Virgili G, Rizzo S. EDI-OCT evaluation of choroidal thickness in retinitis pigmentosa. Eur J Ophthalmol. 2018;28:52–7. https://doi.org/10.5301/ejo.5000961.
Yeoh J, Rahman W, Chen F, Hooper C, Patel P, Tufail A, Webster AR, Moore AT, Dacruz L. Choroidal imaging in inherited retinal disease using the technique of enhanced depth imaging optical coherence tomography. Graefes Arch Clin Exp Ophthalmol. 2010;248:1719–28. https://doi.org/10.1007/s00417-010-1437-3.
Aras C, Ocakoglu O, Akova N. Foveolar choroidal blood flow in idiopathic macular hole. Int Ophthalmol. 2004;25:225–31. https://doi.org/10.1007/s10792-005-5014-4.
Morgan CM, Schatz H. Involutional macular thinning A pre-macular hole condition. Ophthalmology. 1986;93:153–61. https://doi.org/10.1016/s0161-6420(86)33767-9.
Cheong KX, Xu L, Ohno-Matsui K, Sabanayagam C, Saw SM, Hoang QV (2022) An evidence-based review of the epidemiology of myopic traction maculopathy. Surv Ophthalmol. 31:S0039–6257(22)00044–3. https://doi.org/10.1016/j.survophthal.2022.03.007 Epub ahead of print
Semeraro F, Morescalchi F, Russo A, Romano MR, Costagliola C. Tamponade or filling effect: changes of forces in myopic eyes. Biomed Res Int. 2014;2014:618382. https://doi.org/10.1155/2014/618382.
Acknowledgments
Not applicable.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
Design & conduction of the study: (SJZ, JML, WBZ YZZ, XPG, YDZ); Data curation (WBZ, YZZ, XPG, YDZ), Formal analysis (SJZ, JML), Writing-original draft, Writing-review & editing (SJZ). The author(s) read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
The study was performed under adherence of the ethical foundations of the Declaration of Helsinki and was approved by the Ethics Commission of Peking University First Hospital (2022-312). The need for informed consent was waived by the Ethics Committee of Peking University First Hospital.
Consent for publication
Not applicable.
Competing interests
The authors have no conflicts of interest to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
About this article
Cite this article
Zhang, S., Li, J., Zhang, W. et al. Comparison of the morphological characteristics of the choroidal sublayer between idiopathic macular holes and epiretinal membranes with automatic analysis. BMC Ophthalmol 23, 277 (2023). https://doi.org/10.1186/s12886-023-03027-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/s12886-023-03027-8