Deep-learning-based diagnosis of myopia in children using optical coherence tomography angiography

Wenchao Xiao, Lu Yuxing, Hanpei Miao, Wenting Zhao, David Schanzlin
{"title":"Deep-learning-based diagnosis of myopia in children using optical coherence tomography angiography","authors":"Wenchao Xiao,&nbsp;Lu Yuxing,&nbsp;Hanpei Miao,&nbsp;Wenting Zhao,&nbsp;David Schanzlin","doi":"10.1002/mef2.72","DOIUrl":null,"url":null,"abstract":"<p>As myopia develops and progresses at an accelerated pace during adolescence, a timely diagnosis is beneficial for preventing its further progression. Optical coherence tomography angiography (OCTA) can visualize distinct layers of retinal microvessels, offering valuable insights into structural changes associated with myopia. This capability facilitates the early detection and monitoring of myopia-related complications, such as choroidal neovascularization and myopic maculopathy. Previous research suggests that alterations in the superficial capillary plexus (SCP) vessel density and deep capillary plexus (DCP) of OCTA images occur in myopic eyes, but few studies have focused on myopia in younger children.<span><sup>1</sup></span> A recent study compared retinal microvasculature in the SCP of children and adolescents using OCTA imaging, which indicated that there were no obvious variations in microvessel density, perfusion density (PD), and the size of the foveal avascular zone within the SCP between groups with mild and moderate/high myopia.<span><sup>2</sup></span> Conversely, another study demonstrated a negative correlation between children's myopia diopter and the microvessel density of both the superficial and deep retinal capillary plexus in the macula, as well as retinal thickness.<span><sup>3</sup></span> Nonetheless, these studies only scrutinized a limited number of OCTA image parameters in the macular region and involved a relatively small number of subjects. Further research is warranted to fully understand the potential of OCTA images in assessing myopia during adolescence.</p><p>Deep learning can extract high-dimensional features from images through its multilayer network architecture, leading to improved task performance. However, to our knowledge, there is limited research on the use of artificial intelligence for analyzing OCTA images related to myopia. Our study contributes to addressing this research gap by highlighting the potential of deep learning in OCTA image analysis for myopia assessment. In this study, we aimed to employ end-to-end deep learning models to classify children with mild versus severe myopia. This study aimed to evaluate the potential of deep and superficial blood vessels in the macula and optic disc as indicators of myopia severity in children, utilizing a classification task based on OCTA images.</p><p>Initially, we collected four images from both the superficial and deep retinal capillary plexus in the macula, as well as from the optic disc, of children aged 8–16. Exclusion criteria included poor quality OCTA images, patients with other ocular conditions, or those who had undergone eye surgery. Ultimately, a total of 129 children (242 eyes) were included in this study. The subjects were divided into two groups based on their degree of refractive error: emmetropia/mild myopia (177 eyes, with a mean spherical equivalent between −3.00 and ≤0.50 D) and moderate/high myopia (65 eyes, with a mean spherical equivalent of less than −3.00 D). The average age of participants in this study was 11.14 years, including 63 girls. For more detailed information on the data set, please see File S1: Materials and methods section.</p><p>Next, we utilized the resnet152 model to analyze the performance of different layer images within the macula and optic disc for the classification task. The workflow is illustrated in Figure 1A, and detailed methods are available in the File S1: Materials and methods section. Our results indicate that the four separate OCTA image models (SCP and DCP of macula and optic disc, respectively) exhibit good performance in distinguishing between the emmetropia/mild and moderate/high myopia groups, with the area under the curves (AUCs) ranging from 0.803 to 0.892 (Supporting Information S1: Table S2). The superior discriminatory effect of these models could be attributed to the changes occurring in the retinal microvessels within the optic disc and macula during the period of myopia development in teenagers. These changes may be a consequence of altered blood vessel morphology arising from the elongation of the eye axis in this period. It is worth highlighting that the models utilizing superficial optic disc microvessel images exhibited the most optimal classification effect. Previous studies have suggested that changes in the shape of the optic disc play a significant role in the development and progression of myopia. The elongation of the axial length of the eye could cause remarkable changes in the size of the optic disc, peripapillary scleral flange, and peripapillary choroidal tissue, which may impact the morphology of the fundus blood vessels.<span><sup>4</sup></span> These changes may be particularly noticeable in the superficial blood vessels of the optic disc. To improve interpretability, we utilized the Grad-CAM technique to visualize the areas of the fundus that the model focuses on, represented through heat maps, as shown in Figure 1B. The maps illustrate that not only the blood vessels but also the structure of the optic disc was taken into consideration in the model, specifically in the SVC image of the optic disc. Previous research using OCT for myopia detection achieved an AUC of 0.813 and an accuracy of 71.4%, with inner retinal layers and steepened curvature as key indicators.<span><sup>5</sup></span> These findings are consistent with our study's outcomes, further validating our model's efficacy in myopia assessment.</p><p>Third, we attempted to incorporate the information of both superficial and deep retinal microvessels to investigate whether there exists complementary information across different levels that can enhance the model's performance. However, despite obtaining AUC values exceeding 80 (Figure 1C), the fusion model did not exhibit any superior classification performance compared to the single image models. The training data set size may be insufficient for optimal model training results. Therefore, further improvements in model construction and parameter adjustment are needed to enhance the model's performance. Additionally, a longitudinal observational study in this field would be necessary.</p><p>In summary, our study demonstrated that deep learning is a promising tool for evaluating OCTA images in children with myopia. Additionally, there were observable differences between superficial and deep retinal microvessels in the macula and optic disc for varying degrees of myopia, with the superficial OCTA images of the optic disc displaying the most effective performance. Further research is necessary to refine and optimize model construction and parameter adjustments for myopia assessment utilizing OCTA images. Our study will contribute to a better understanding of the mechanism of myopia development in children and aid the development of more effective interventions to prevent and manage myopia.</p><p><i>Conceptualization</i>: Wenchao Xiao. <i>Data curation</i>: Wenchao Xiao and Wenting Zhao. <i>Formal analysis</i>: Wenchao Xiao, Lu Yuxing, Hanpei Miao, Wenting Zhao, and David Schanzlin. <i>Funding acquisition</i>: Wenchao Xiao. <i>Investigation, methodology; project administration, resources, software, supervision, validation, writing—original draft</i>: Wenchao Xiao and Hanpei Miao. <i>Writing—review and editing</i>: Wenchao Xiao, Hanpei Miao, and David Schanzlin. Wenchao Xiao, Lu Yuxing, Hanpei Miao, Wenting Zhao, and David Schanzlin collected and analyzed data. Wenchao Xiao designed the study and wrote the paper with the help of Hanpei Miao and David Schanzlin. All authors discussed the results and commented on the manuscript. All authors have read and approved the final manuscript.</p><p>The authors declare no conflict of interest.</p><p>Ethical approval for this study was obtained from the institutional ethics committee of the Chinese Academy of Medical Sciences, Zhuhai People's Hospital and adhered to the principles outlined in the Declaration of Helsinki. Written informed consent was obtained from the parents or guardians of all participants. 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引用次数: 0

Abstract

As myopia develops and progresses at an accelerated pace during adolescence, a timely diagnosis is beneficial for preventing its further progression. Optical coherence tomography angiography (OCTA) can visualize distinct layers of retinal microvessels, offering valuable insights into structural changes associated with myopia. This capability facilitates the early detection and monitoring of myopia-related complications, such as choroidal neovascularization and myopic maculopathy. Previous research suggests that alterations in the superficial capillary plexus (SCP) vessel density and deep capillary plexus (DCP) of OCTA images occur in myopic eyes, but few studies have focused on myopia in younger children.1 A recent study compared retinal microvasculature in the SCP of children and adolescents using OCTA imaging, which indicated that there were no obvious variations in microvessel density, perfusion density (PD), and the size of the foveal avascular zone within the SCP between groups with mild and moderate/high myopia.2 Conversely, another study demonstrated a negative correlation between children's myopia diopter and the microvessel density of both the superficial and deep retinal capillary plexus in the macula, as well as retinal thickness.3 Nonetheless, these studies only scrutinized a limited number of OCTA image parameters in the macular region and involved a relatively small number of subjects. Further research is warranted to fully understand the potential of OCTA images in assessing myopia during adolescence.

Deep learning can extract high-dimensional features from images through its multilayer network architecture, leading to improved task performance. However, to our knowledge, there is limited research on the use of artificial intelligence for analyzing OCTA images related to myopia. Our study contributes to addressing this research gap by highlighting the potential of deep learning in OCTA image analysis for myopia assessment. In this study, we aimed to employ end-to-end deep learning models to classify children with mild versus severe myopia. This study aimed to evaluate the potential of deep and superficial blood vessels in the macula and optic disc as indicators of myopia severity in children, utilizing a classification task based on OCTA images.

Initially, we collected four images from both the superficial and deep retinal capillary plexus in the macula, as well as from the optic disc, of children aged 8–16. Exclusion criteria included poor quality OCTA images, patients with other ocular conditions, or those who had undergone eye surgery. Ultimately, a total of 129 children (242 eyes) were included in this study. The subjects were divided into two groups based on their degree of refractive error: emmetropia/mild myopia (177 eyes, with a mean spherical equivalent between −3.00 and ≤0.50 D) and moderate/high myopia (65 eyes, with a mean spherical equivalent of less than −3.00 D). The average age of participants in this study was 11.14 years, including 63 girls. For more detailed information on the data set, please see File S1: Materials and methods section.

Next, we utilized the resnet152 model to analyze the performance of different layer images within the macula and optic disc for the classification task. The workflow is illustrated in Figure 1A, and detailed methods are available in the File S1: Materials and methods section. Our results indicate that the four separate OCTA image models (SCP and DCP of macula and optic disc, respectively) exhibit good performance in distinguishing between the emmetropia/mild and moderate/high myopia groups, with the area under the curves (AUCs) ranging from 0.803 to 0.892 (Supporting Information S1: Table S2). The superior discriminatory effect of these models could be attributed to the changes occurring in the retinal microvessels within the optic disc and macula during the period of myopia development in teenagers. These changes may be a consequence of altered blood vessel morphology arising from the elongation of the eye axis in this period. It is worth highlighting that the models utilizing superficial optic disc microvessel images exhibited the most optimal classification effect. Previous studies have suggested that changes in the shape of the optic disc play a significant role in the development and progression of myopia. The elongation of the axial length of the eye could cause remarkable changes in the size of the optic disc, peripapillary scleral flange, and peripapillary choroidal tissue, which may impact the morphology of the fundus blood vessels.4 These changes may be particularly noticeable in the superficial blood vessels of the optic disc. To improve interpretability, we utilized the Grad-CAM technique to visualize the areas of the fundus that the model focuses on, represented through heat maps, as shown in Figure 1B. The maps illustrate that not only the blood vessels but also the structure of the optic disc was taken into consideration in the model, specifically in the SVC image of the optic disc. Previous research using OCT for myopia detection achieved an AUC of 0.813 and an accuracy of 71.4%, with inner retinal layers and steepened curvature as key indicators.5 These findings are consistent with our study's outcomes, further validating our model's efficacy in myopia assessment.

Third, we attempted to incorporate the information of both superficial and deep retinal microvessels to investigate whether there exists complementary information across different levels that can enhance the model's performance. However, despite obtaining AUC values exceeding 80 (Figure 1C), the fusion model did not exhibit any superior classification performance compared to the single image models. The training data set size may be insufficient for optimal model training results. Therefore, further improvements in model construction and parameter adjustment are needed to enhance the model's performance. Additionally, a longitudinal observational study in this field would be necessary.

In summary, our study demonstrated that deep learning is a promising tool for evaluating OCTA images in children with myopia. Additionally, there were observable differences between superficial and deep retinal microvessels in the macula and optic disc for varying degrees of myopia, with the superficial OCTA images of the optic disc displaying the most effective performance. Further research is necessary to refine and optimize model construction and parameter adjustments for myopia assessment utilizing OCTA images. Our study will contribute to a better understanding of the mechanism of myopia development in children and aid the development of more effective interventions to prevent and manage myopia.

Conceptualization: Wenchao Xiao. Data curation: Wenchao Xiao and Wenting Zhao. Formal analysis: Wenchao Xiao, Lu Yuxing, Hanpei Miao, Wenting Zhao, and David Schanzlin. Funding acquisition: Wenchao Xiao. Investigation, methodology; project administration, resources, software, supervision, validation, writing—original draft: Wenchao Xiao and Hanpei Miao. Writing—review and editing: Wenchao Xiao, Hanpei Miao, and David Schanzlin. Wenchao Xiao, Lu Yuxing, Hanpei Miao, Wenting Zhao, and David Schanzlin collected and analyzed data. Wenchao Xiao designed the study and wrote the paper with the help of Hanpei Miao and David Schanzlin. All authors discussed the results and commented on the manuscript. All authors have read and approved the final manuscript.

The authors declare no conflict of interest.

Ethical approval for this study was obtained from the institutional ethics committee of the Chinese Academy of Medical Sciences, Zhuhai People's Hospital and adhered to the principles outlined in the Declaration of Helsinki. Written informed consent was obtained from the parents or guardians of all participants. APPROVAL NUMBER: ZY [2019] Number (20).

Abstract Image

基于深度学习的光学相干断层血管造影诊断儿童近视
由于近视在青春期的发展和进展速度加快,及时诊断有利于防止其进一步发展。光学相干断层血管造影(OCTA)可以观察到视网膜微血管的不同层次,为了解与近视相关的结构变化提供了宝贵的信息。这一功能有助于早期发现和监测近视相关并发症,如脉络膜新生血管和近视性黄斑病变。以往的研究表明,OCTA 图像的浅层毛细血管丛(SCP)血管密度和深层毛细血管丛(DCP)会在近视眼中发生改变,但很少有研究关注低龄儿童的近视情况1。最近的一项研究利用 OCTA 成像比较了儿童和青少年 SCP 的视网膜微血管,结果表明,轻度和中度/高度近视组之间在 SCP 的微血管密度、灌注密度(PD)和眼窝无血管区的大小方面没有明显差异2。相反,另一项研究表明,儿童近视屈光度与黄斑浅层和深层视网膜毛细血管丛的微血管密度以及视网膜厚度之间呈负相关。要想充分了解 OCTA 图像在评估青春期近视方面的潜力,还需要进一步的研究。深度学习可以通过其多层网络架构从图像中提取高维特征,从而提高任务性能。然而,据我们所知,利用人工智能分析与近视相关的 OCTA 图像的研究还很有限。我们的研究强调了深度学习在近视评估的 OCTA 图像分析中的潜力,有助于弥补这一研究空白。在本研究中,我们旨在采用端到端深度学习模型,对儿童轻度和重度近视进行分类。本研究旨在利用基于 OCTA 图像的分类任务,评估黄斑和视盘的深层和浅层血管作为儿童近视严重程度指标的潜力。最初,我们收集了 8-16 岁儿童黄斑浅层和深层视网膜毛细血管丛以及视盘的四幅图像。排除标准包括 OCTA 图像质量差、患有其他眼部疾病或接受过眼部手术的患者。最终,共有 129 名儿童(242 只眼睛)参与了这项研究。受试者根据屈光不正的程度分为两组:散光/轻度近视(177 只眼睛,平均球面等效视力在-3.00 和≤0.50 D 之间)和中度/高度近视(65 只眼睛,平均球面等效视力低于-3.00 D)。研究参与者的平均年龄为 11.14 岁,其中包括 63 名女孩。有关数据集的详细信息,请参见文件 S1:材料和方法部分。接下来,我们利用 resnet152 模型分析了黄斑和视盘内不同层图像在分类任务中的表现。工作流程如图 1A 所示,详细方法请参见文件 S1:材料与方法部分。我们的结果表明,四个独立的 OCTA 图像模型(分别为黄斑和视盘的 SCP 和 DCP)在区分散光/轻度近视组和中度/高度近视组方面表现出良好的性能,曲线下面积(AUC)从 0.803 到 0.892 不等(佐证资料 S1:表 S2)。这些模型的卓越分辨效果可能是由于在青少年近视发展期间,视盘和黄斑内的视网膜微血管发生了变化。这些变化可能是这一时期眼轴拉长导致血管形态改变的结果。值得强调的是,利用浅层视盘微血管图像的模型显示出最理想的分类效果。以往的研究表明,视盘形状的变化在近视的发生和发展过程中起着重要作用。眼球轴向长度的拉长会导致视盘、巩膜周缘和脉络膜周缘组织的大小发生显著变化,从而影响眼底血管的形态。为了提高可解释性,我们利用 Grad-CAM 技术将模型聚焦的眼底区域可视化,通过热图表示,如图 1B 所示。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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