A Diabetic Retinopathy Classification Framework Based on Deep-Learning Analysis of OCT Angiography

Purpose Reliable classification of referable and vision threatening diabetic retinopathy (DR) is essential for patients with diabetes to prevent blindness. Optical coherence tomography (OCT) and its angiography (OCTA) have several advantages over fundus photographs. We evaluated a deep-learning-aided DR classification framework using volumetric OCT and OCTA. Methods Four hundred fifty-six OCT and OCTA volumes were scanned from eyes of 50 healthy participants and 305 patients with diabetes. Retina specialists labeled the eyes as non-referable (nrDR), referable (rDR), or vision threatening DR (vtDR). Each eye underwent a 3 × 3-mm scan using a commercial 70 kHz spectral-domain OCT system. We developed a DR classification framework and trained it using volumetric OCT and OCTA to classify eyes into rDR and vtDR. For the scans identified as rDR or vtDR, 3D class activation maps were generated to highlight the subregions which were considered important by the framework for DR classification. Results For rDR classification, the framework achieved a 0.96 ± 0.01 area under the receiver operating characteristic curve (AUC) and 0.83 ± 0.04 quadratic-weighted kappa. For vtDR classification, the framework achieved a 0.92 ± 0.02 AUC and 0.73 ± 0.04 quadratic-weighted kappa. In addition, the multiple DR classification (non-rDR, rDR but non-vtDR, or vtDR) achieved a 0.83 ± 0.03 quadratic-weighted kappa. Conclusions A deep learning framework only based on OCT and OCTA can provide specialist-level DR classification using only a single imaging modality. Translational Relevance The proposed framework can be used to develop clinically valuable automated DR diagnosis system because of the specialist-level performance showed in this study.

[1]  David Huang,et al.  Comparison of Central Macular Fluid Volume With Central Subfield Thickness in Patients With Diabetic Macular Edema Using Optical Coherence Tomography Angiography. , 2021, JAMA ophthalmology.

[2]  Tristan T. Hormel,et al.  Artificial intelligence in OCT angiography , 2021, Progress in Retinal and Eye Research.

[3]  Yali Jia,et al.  DcardNet: Diabetic Retinopathy Classification at Multiple Levels Based on Structural and Angiographic Optical Coherence Tomography , 2020, IEEE Transactions on Biomedical Engineering.

[4]  Xincheng Yao,et al.  QUANTITATIVE OPTICAL COHERENCE TOMOGRAPHY ANGIOGRAPHY FEATURES FOR OBJECTIVE CLASSIFICATION AND STAGING OF DIABETIC RETINOPATHY. , 2020 .

[5]  Mirza Faisal Beg,et al.  Ensemble Deep Learning for Diabetic Retinopathy Detection Using Optical Coherence Tomography Angiography , 2020, Translational vision science & technology.

[6]  David Le,et al.  Transfer Learning for Automated OCTA Detection of Diabetic Retinopathy , 2019, Translational vision science & technology.

[7]  Jennifer I. Lim,et al.  Diabetic Retinopathy Preferred Practice Pattern®. , 2019, Ophthalmology.

[8]  Jie Wang,et al.  Maximum value projection produces better en face OCT angiograms than mean value projection. , 2018, Biomedical optics express.

[9]  Xincheng Yao,et al.  QUANTITATIVE OPTICAL COHERENCE TOMOGRAPHY ANGIOGRAPHY FEATURES FOR OBJECTIVE CLASSIFICATION AND STAGING OF DIABETIC RETINOPATHY. , 2018, Retina.

[10]  David J. Wilson,et al.  Automated Quantification of Nonperfusion Areas in 3 Vascular Plexuses With Optical Coherence Tomography Angiography in Eyes of Patients With Diabetes , 2018, JAMA ophthalmology.

[11]  Ayman El-Baz,et al.  Automated Diagnosis and Grading of Diabetic Retinopathy Using Optical Coherence Tomography , 2018, Investigative ophthalmology & visual science.

[12]  Jennifer K. Sun,et al.  Guidelines on Diabetic Eye Care: The International Council of Ophthalmology Recommendations for Screening, Follow-up, Referral, and Treatment Based on Resource Settings. , 2018, Ophthalmology.

[13]  Ayman El-Baz,et al.  Automated diabetic retinopathy detection using optical coherence tomography angiography: a pilot study , 2018, British Journal of Ophthalmology.

[14]  Jonathan Krause,et al.  Grader variability and the importance of reference standards for evaluating machine learning models for diabetic retinopathy , 2017, Ophthalmology.

[15]  Rishab Gargeya,et al.  Automated Identification of Diabetic Retinopathy Using Deep Learning. , 2017, Ophthalmology.

[16]  Bianca S. Gerendas,et al.  Guidelines for the Management of Diabetic Macular Edema by the European Society of Retina Specialists (EURETINA) , 2017, Ophthalmologica.

[17]  David Huang,et al.  Reflectance-based projection-resolved optical coherence tomography angiography [Invited]. , 2017, Biomedical optics express.

[18]  David J. Wilson,et al.  Detailed Vascular Anatomy of the Human Retina by Projection-Resolved Optical Coherence Tomography Angiography , 2017, Scientific Reports.

[19]  Kuntal Ghosh,et al.  Automatic detection and classification of diabetic retinopathy stages using CNN , 2017, 2017 4th International Conference on Signal Processing and Integrated Networks (SPIN).

[20]  Subhashini Venugopalan,et al.  Development and Validation of a Deep Learning Algorithm for Detection of Diabetic Retinopathy in Retinal Fundus Photographs. , 2016, JAMA.

[21]  David Huang,et al.  Visualization of 3 Distinct Retinal Plexuses by Projection-Resolved Optical Coherence Tomography Angiography in Diabetic Retinopathy. , 2016, JAMA ophthalmology.

[22]  M. Abràmoff,et al.  Improved Automated Detection of Diabetic Retinopathy on a Publicly Available Dataset Through Integration of Deep Learning. , 2016, Investigative ophthalmology & visual science.

[23]  Thomas S. Hwang,et al.  Automated Quantification of Nonperfusion in Three Retinal Plexuses Using Projection-Resolved Optical Coherence Tomography Angiography in Diabetic Retinopathy , 2016, Investigative ophthalmology & visual science.

[24]  T. Lai,et al.  Spectral Domain Optical Coherence Tomography Features and Classification Systems for Diabetic Macular Edema: A Review , 2016, Asia-Pacific journal of ophthalmology.

[25]  David Huang,et al.  Automated Quantification of Capillary Nonperfusion Using Optical Coherence Tomography Angiography in Diabetic Retinopathy. , 2016, JAMA ophthalmology.

[26]  David Huang,et al.  Projection-resolved optical coherence tomographic angiography. , 2016, Biomedical optics express.

[27]  Bolei Zhou,et al.  Learning Deep Features for Discriminative Localization , 2015, 2016 IEEE Conference on Computer Vision and Pattern Recognition (CVPR).

[28]  David Huang,et al.  Advanced image processing for optical coherence tomographic angiography of macular diseases. , 2015, Biomedical optics express.

[29]  David J. Wilson,et al.  OPTICAL COHERENCE TOMOGRAPHY ANGIOGRAPHY FEATURES OF DIABETIC RETINOPATHY , 2015, Retina.

[30]  T. Wong,et al.  Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss , 2015, Eye and Vision.

[31]  Geoffrey E. Hinton,et al.  Deep Learning , 2015, Nature.

[32]  Gangjun Liu,et al.  Optimization of the split-spectrum amplitude-decorrelation angiography algorithm on a spectral optical coherence tomography system. , 2015, Optics letters.

[33]  David J. Wilson,et al.  Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye , 2015, Proceedings of the National Academy of Sciences.

[34]  Sergey Ioffe,et al.  Batch Normalization: Accelerating Deep Network Training by Reducing Internal Covariate Shift , 2015, ICML.

[35]  Gianni Virgili,et al.  Optical coherence tomography (OCT) for detection of macular oedema in patients with diabetic retinopathy. , 2015, The Cochrane database of systematic reviews.

[36]  James G. Fujimoto,et al.  Quantitative 3D-OCT motion correction with tilt and illumination correction, robust similarity measure and regularization , 2014, Biomedical optics express.

[37]  S. Harding,et al.  Improving the cost-effectiveness of photographic screening for diabetic macular oedema: a prospective, multi-centre, UK study , 2014, British Journal of Ophthalmology.

[38]  H Wharton,et al.  Improving the economic value of photographic screening for optical coherence tomography-detectable macular oedema: a prospective, multicentre, UK study. , 2013, Health technology assessment.

[39]  Quantitative Imaging in Medicine and Surgery , 2013 .

[40]  Martin F. Kraus,et al.  Split-spectrum amplitude-decorrelation angiography with optical coherence tomography , 2012, Optics express.

[41]  Jennifer K. Sun,et al.  Observational study of subclinical diabetic macular edema , 2010, Eye.

[42]  R. Klein,et al.  Diabetic retinopathy. , 2012, The New England journal of medicine.

[43]  Yoshua Bengio,et al.  Deep Sparse Rectifier Neural Networks , 2011, AISTATS.

[44]  K. Bhavsar,et al.  Risk factors for progression of subclinical diabetic macular oedema , 2010, British Journal of Ophthalmology.

[45]  S. Haneda,et al.  [International clinical diabetic retinopathy disease severity scale]. , 2010, Nihon rinsho. Japanese journal of clinical medicine.

[46]  Geoffrey E. Hinton,et al.  Rectified Linear Units Improve Restricted Boltzmann Machines , 2010, ICML.

[47]  Ruikang K. Wang,et al.  In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography. , 2008, Optics express.

[48]  D. Browning,et al.  The relationship of macular thickness to clinically graded diabetic retinopathy severity in eyes without clinically detected diabetic macular edema. , 2008, Ophthalmology.

[49]  D. Browning,et al.  The predictive value of patient and eye characteristics on the course of subclinical diabetic macular edema. , 2008, American journal of ophthalmology.

[50]  T. Yatagai,et al.  Optical coherence angiography. , 2006, Optics express.

[51]  Matthew D. Davis,et al.  Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. , 2003, Ophthalmology.

[52]  G. Ripandelli,et al.  Optical coherence tomography. , 1998, Seminars in ophthalmology.

[53]  Fundus photographic risk factors for progression of diabetic retinopathy. ETDRS report number 12. Early Treatment Diabetic Retinopathy Study Research Group. , 1991, Ophthalmology.

[54]  L. Aiello,et al.  Detection of diabetic macular edema. Ophthalmoscopy versus photography--Early Treatment Diabetic Retinopathy Study Report Number 5. The ETDRS Research Group. , 1989, Ophthalmology.

[55]  Jacob Cohen A Coefficient of Agreement for Nominal Scales , 1960 .