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Automated machine learning–based classification of proliferative and non-proliferative diabetic retinopathy using optical coherence tomography angiography vascular density maps

  • Retinal Disorders
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Abstract

Purpose

The study aims to classify the eyes with proliferative diabetic retinopathy (PDR) and non-proliferative diabetic retinopathy (NPDR) based on the optical coherence tomography angiography (OCTA) vascular density maps using a supervised machine learning algorithm.

Methods

OCTA vascular density maps (at superficial capillary plexus (SCP), deep capillary plexus (DCP), and total retina (R) levels) of 148 eyes from 78 patients with diabetic retinopathy (45 PDR and 103 NPDR) was used to classify the images to NPDR and PDR groups based on a supervised machine learning algorithm known as the support vector machine (SVM) classifier optimized by a genetic evolutionary algorithm.

Results

The implemented algorithm in three different models reached up to 85% accuracy in classifying PDR and NPDR in all three levels of vascular density maps. The deep retinal layer vascular density map demonstrated the best performance with a 90% accuracy in discriminating between PDR and NPDR.

Conclusions

The current study on a limited number of patients with diabetic retinopathy demonstrated that a supervised machine learning–based method known as SVM can be used to differentiate PDR and NPDR patients using OCTA vascular density maps.

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Data availability

The data generated during or/and analyzed during the current study are available from the corresponding author.

References

  1. Solomon SD, Chew E, Duh EJ et al (2017) Diabetic retinopathy: a position statement by the American Diabetes Association. Diabetes Care 40:412–418. https://doi.org/10.2337/dc16-2641

    Article  Google Scholar 

  2. Kobrin Klein BE (2007) Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol 14:179–183. https://doi.org/10.1080/09286580701396720

    Article  Google Scholar 

  3. Antonetti DA, Klein R, Gardner TW (2012) Diabetic retinopathy. N Engl J Med 366:1227–1239. https://doi.org/10.1056/nejmra1005073

    Article  CAS  Google Scholar 

  4. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376:124–136. https://doi.org/10.1016/s0140-6736(09)62124-3

    Article  Google Scholar 

  5. (1976) Preliminary report on effects of photocoagulation therapy. Am J Ophthalmol 81:397–402. https://doi.org/10.1016/0002-9394(76)90292-0

  6. Riaskoff S (1981) Photocoagulation treatment of proliferative diabetic retinopathy. Bull Soc Belge Ophtalmol 197:9–17. https://doi.org/10.1016/s0161-6420(81)34978-1

    Article  CAS  Google Scholar 

  7. (1985) Photocoagulation For Diabetic Macular Edema: Early Treatment Diabetic Retinopathy Study Report Number 1 Early Treatment Diabetic Retinopathy Study Research Group. Arch Ophthalmol 103:1796–1806. https://doi.org/10.1001/archopht.1985.01050120030015

  8. Edwards P (2010) Randomized trial evaluating ranibizumab plus prompt or deferred laser or triamcinolone plus prompt laser for diabetic macular edema. Acta Ophthalmol 88:0. https://doi.org/10.1111/j.1755-3768.2010.4111.x

    Article  CAS  Google Scholar 

  9. Vander JF (2011) A prospective randomized trial of intravitreal bevacizumab or laser therapy in the management of diabetic macular edema (BOLT study): 12-month data: report 2. Yearb Ophthalmol 2011:123–124. https://doi.org/10.1016/j.yoph.2010.12.006

    Article  Google Scholar 

  10. Brucker AJ, Qin H, Antoszyk AN et al (2009) Observational study of the development of diabetic macular edema following panretinal (scatter) photocoagulation given in 1 or 4 sittings. Arch Ophthalmol 127:132–140. https://doi.org/10.1001/archophthalmol.2008.565

    Article  Google Scholar 

  11. Faghihi H, Riazi-Esfahani H, Khodabande A et al (2021) Effect of panretinal photocoagulation on macular vasculature using optical coherence tomography angiography. Eur J Ophthalmol 31:1877–1884

    Article  Google Scholar 

  12. Falavarjani K, Khadamy J, Aghdam K (2018) An update on optical coherence tomography angiography in diabetic retinopathy. J Ophthalmic Vis Res 13:487. https://doi.org/10.4103/jovr.jovr_57_18

    Article  Google Scholar 

  13. Mirshahi R, Riazi-Esfahani H, Khalili Pour E et al (2021) Differentiating features of OCT angiography in diabetic macular edema. Sci Rep 11(1):23398. https://doi.org/10.1038/s41598-021-02859-y

  14. Falavarjani KG, Sarraf D (2017) Optical coherence tomography angiography of the retina and choroid; current applications and future directions. J Curr Ophthalmol 29:1–4. https://doi.org/10.1016/j.joco.2017.02.005

    Article  Google Scholar 

  15. Gulshan V, Peng L, Coram M et al (2016) Development and validation of a deep learning algorithm for detection of diabetic retinopathy in retinal fundus photographs. JAMA 316:2402. https://doi.org/10.1001/jama.2016.17216

    Article  Google Scholar 

  16. Abràmoff MD, Lou Y, Erginay A et al (2016) Improved automated detection of diabetic retinopathy on a publicly available dataset through integration of deep learning. Investig Opthalmology Vis Sci 57:5200. https://doi.org/10.1167/iovs.16-19964

    Article  Google Scholar 

  17. Ghazal M, Ali SS, Mahmoud AH et al (2020) Accurate detection of non-proliferative diabetic retinopathy in optical coherence tomography images using convolutional neural networks. IEEE Access 8:34387–34397. https://doi.org/10.1109/access.2020.2974158

    Article  Google Scholar 

  18. Alam M, Zhang Y, Lim JI et al (2020) Quantitative optical coherence tomography angiography features for objective classification and staging of diabetic retinopathy. Retina 40:322–332. https://doi.org/10.1097/iae.0000000000002373

    Article  Google Scholar 

  19. Heisler M, Karst S, Lo J et al (2020) Ensemble deep learning for diabetic retinopathy detection using optical coherence tomography angiography. Transl Vis Sci Technol 9:20. https://doi.org/10.1167/tvst.9.2.20

    Article  Google Scholar 

  20. Zang P, Gao L, Hormel TT et al (2021) DcardNet: diabetic retinopathy classification at multiple levels based on structural and angiographic optical coherence tomography. IEEE Trans Biomed Eng 68:1859–1870. https://doi.org/10.1109/tbme.2020.3027231

    Article  Google Scholar 

  21. Gargeya R, Leng T (2017) Automated identification of diabetic retinopathy using deep learning. Ophthalmology 124:962–969. https://doi.org/10.1016/j.ophtha.2017.02.008

    Article  Google Scholar 

  22. Usman Akram M, Khalid S, Tariq A et al (2014) Detection and classification of retinal lesions for grading of diabetic retinopathy. Comput Biol Med 45:161–171. https://doi.org/10.1016/j.compbiomed.2013.11.014

    Article  CAS  Google Scholar 

  23. Ruamviboonsuk P, Krause J, Chotcomwongse P, et al (2019) Deep learning versus human graders for classifying diabetic retinopathy severity in a nationwide screening program. npj Digit Med 2:. https://doi.org/10.1038/s41746-019-0099-8

  24. Eladawi N, Elmogy M, Ghazal M et al (2019) Early signs detection of diabetic retinopathy using optical coherence tomography angiography scans based on 3D multi-path convolutional neural network. 2019 IEEE International Conference on Image Processing (ICIP): 1390–1394. https://doi.org/10.1109/ICIP.2019.8803031

  25. Sandhu HS, Eladawi N, Elmogy M et al (2018) Automated diabetic retinopathy detection using optical coherence tomography angiography: a pilot study. Br J Ophthalmol 102:1564–1569. https://doi.org/10.1136/bjophthalmol-2017-311489

    Article  Google Scholar 

  26. Sandhu HS, Elmogy M, Taher Sharafeldeen A et al (2020) Automated diagnosis of diabetic retinopathy using clinical biomarkers, optical coherence tomography, and optical coherence tomography angiography. Am J Ophthalmol 216:201–206. https://doi.org/10.1016/j.ajo.2020.01.016

    Article  Google Scholar 

  27. ElTanboly A, Ismail M, Shalaby A et al (2017) A computer-aided diagnostic system for detecting diabetic retinopathy in optical coherence tomography images. Med Phys 44:914–923. https://doi.org/10.1002/mp.12071

    Article  CAS  Google Scholar 

  28. Sandhu HS, Eltanboly A, Shalaby A et al (2018) Automated diagnosis and grading of diabetic retinopathy using optical coherence tomography. Investig Opthalmology Vis Sci 59:3155. https://doi.org/10.1167/iovs.17-23677

    Article  Google Scholar 

  29. Yang W, Wang K, Zuo W (2012) Neighborhood component feature selection for high-dimensional data. J Comput 7. https://doi.org/10.4304/jcp.7.1.161-168

  30. Suthaharan S (2016) Support vector machine. Machine learning models and algorithms for big data classification. Springer, Boston, pp 207–235. https://doi.org/10.1007/978-1-4899-7641-3_9

  31. Whitley D (1994) A genetic algorithm tutorial. Stat Comput 4:. https://doi.org/10.1007/bf00175354

  32. Flaxel CJ, Adelman RA, Bailey ST et al (2020) Diabetic retinopathy preferred practice pattern®. Ophthalmology 127:66–145. https://doi.org/10.1016/j.ophtha.2019.09.025

    Article  Google Scholar 

  33. Idris I, Sellahewa L, Simpson C et al (2014) Grader agreement, and sensitivity and specificity of digital photography in a community optometry-based diabetic eye screening program. Clin Ophthalmol 8:1345–9. https://doi.org/10.2147/opth.s61483

    Article  Google Scholar 

  34. Ruamviboonsuk P, Teerasuwanajak K, Tiensuwan M, Yuttitham K (2006) Interobserver agreement in the interpretation of single-field digital fundus images for diabetic retinopathy screening. Ophthalmology 113:826–832. https://doi.org/10.1016/j.ophtha.2005.11.021

    Article  Google Scholar 

  35. World Health Organization, PEPFAR & UNAIDS (‎2007)‎ Task shifting: rational redistribution of tasks among health workforce teams: global recommendations and guidelines. World Health Organization. https://apps.who.int/iris/handle/10665/43821

  36. Wang LZ, Cheung CY, Tapp RJ et al (2017) Availability and variability in guidelines on diabetic retinopathy screening in Asian countries. Br J Ophthalmol 101:1352–1360. https://doi.org/10.1136/bjophthalmol-2016-310002

    Article  Google Scholar 

  37. van der Heijden AA, Abramoff MD, Verbraak F et al (2017) Validation of automated screening for referable diabetic retinopathy with the IDx-DR device in the Hoorn Diabetes Care System. Acta Ophthalmol 96:63–68. https://doi.org/10.1111/aos.13613

    Article  Google Scholar 

  38. Ting DSW, Cheung CY-L, Lim G et al (2017) Development and validation of a deep learning system for diabetic retinopathy and related eye diseases using retinal images from multiethnic populations with diabetes. JAMA 318:2211. https://doi.org/10.1001/jama.2017.18152

    Article  Google Scholar 

  39. Esteva A, Kuprel B, Novoa RA et al (2017) Dermatologist-level classification of skin cancer with deep neural networks. Nature 542:115–118. https://doi.org/10.1038/nature21056

    Article  CAS  Google Scholar 

  40. Shen D, Wu G, Suk H-I (2017) Deep learning in medical image analysis. Annu Rev Biomed Eng 19:221–248. https://doi.org/10.1146/annurev-bioeng-071516-044442

    Article  CAS  Google Scholar 

  41. LeCun Y, Bengio Y, Hinton G (2015) Deep learning. Nature 521:436–444. https://doi.org/10.1038/nature14539

    Article  CAS  Google Scholar 

  42. Silver D, Schrittwieser J, Simonyan K et al (2017) Mastering the game of Go without human knowledge. Nature 550:354–359. https://doi.org/10.1038/nature24270

    Article  CAS  Google Scholar 

  43. Sun JK (2019) Clinical applicability of assessing peripheral nonperfusion on ultra-widefield angiography. JAMA Ophthalmol 137:632. https://doi.org/10.1001/jamaophthalmol.2019.0411

    Article  Google Scholar 

  44. Fan W, Wang K, Ghasemi Falavarjani K et al (2017) Distribution of nonperfusion area on ultra-widefield fluorescein angiography in eyes with diabetic macular edema: DAVE study. Am J Ophthalmol 180:110–116. https://doi.org/10.1016/j.ajo.2017.05.024

    Article  Google Scholar 

  45. Pearce E, Sivaprasad S (2020) A review of advancements and evidence gaps in diabetic retinopathy screening models. Clin Ophthalmol 14:3285. https://doi.org/10.2147/OPTH.S267521

    Article  CAS  Google Scholar 

  46. Dai L, Wu L, Li H et al (2021) A deep learning system for detecting diabetic retinopathy across the disease spectrum - Nature Communications. Nat Commun 12:1–11. https://doi.org/10.1038/s41467-021-23458-5

    Article  CAS  Google Scholar 

  47. Saif PS, Salman AE-RG, Omran NAH, Farweez YAT (2020) Assessment of diabetic retinopathy vascular density maps. Clin Ophthalmol 14:3941–3953. https://doi.org/10.2147/OPTH.S256963

    Article  Google Scholar 

  48. Bénédicte Dupas MD (2018) Association between vessel density and visual acuity in patients with diabetic retinopathy and poorly. JAMA Ophthalmol 136:721–728. https://doi.org/10.1001/jamaophthalmol.2018.1319

    Article  Google Scholar 

  49. Lavia C, Couturier A, Erginay A et al (2019) Reduced vessel density in the superficial and deep plexuses in diabetic retinopathy is associated with structural changes in corresponding retinal layers. PLoS One 14:e0219164. https://doi.org/10.1371/journal.pone.0219164

    Article  CAS  Google Scholar 

  50. Lavia C, Mecê P, Nassisi M et al (2020) Retinal capillary plexus pattern and density from fovea to periphery measured in healthy eyes with swept-source optical coherence tomography angiography — scientific reports. Sci Rep 10:1–11. https://doi.org/10.1038/s41598-020-58359-y

    Article  CAS  Google Scholar 

  51. Dupas B, Minvielle W, Bonnin S et al (2018) Association between vessel density and visual acuity in patients with diabetic retinopathy and poorly controlled type 1 diabetes. JAMA Ophthalmol 136:721–728. https://doi.org/10.1001/jamaophthalmol.2018.1319

    Article  Google Scholar 

  52. Falavarjani KG, Mirshahi R, Riazi-Esfahani H et al (2021) Spatial distribution of diabetic capillary non-perfusion. Microcirculation 28:e12719. https://doi.org/10.1111/micc.12719

    Article  CAS  Google Scholar 

  53. Scarinci F, Nesper PL, Fawzi AA (2016) Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol 168:129–138. https://doi.org/10.1016/j.ajo.2016.05.002

    Article  Google Scholar 

  54. Zang P, Gao L, Hormel TT et al (2020) DcardNet: diabetic retinopathy classification at multiple levels based on structural and angiographic optical coherence tomography. IEEE Trans Biomed Eng 68:1859–1870. https://doi.org/10.1109/TBME.2020.3027231

    Article  Google Scholar 

  55. Silva PS, Dela Cruz AJ, Ledesma MG et al (2015) Diabetic retinopathy severity and peripheral lesions are associated with nonperfusion on ultrawide field angiography. Ophthalmology 122:2465–2472. https://doi.org/10.1016/j.ophtha.2015.07.034

    Article  Google Scholar 

  56. Silva PS, Cavallerano JD, Sun JK et al (2013) Peripheral lesions identified by mydriatic ultrawide field imaging: distribution and potential impact on diabetic retinopathy severity. Ophthalmology 120:2587–2595. https://doi.org/10.1016/j.ophtha.2013.05.004

    Article  Google Scholar 

  57. Wessel MM, Aaker GD, Parlitsis G et al (2012) Ultra–wide-field angiography improves the detection and classification of diabetic retinopathy. Retina 32:785–791. https://doi.org/10.1097/iae.0b013e3182278b64

    Article  Google Scholar 

  58. Price L, Au S, Chong V (2015) Optomap ultrawide field imaging identifies additional retinal abnormalities in patients with diabetic retinopathy. Clin Ophthalmol 9:527–531. https://doi.org/10.2147/opth.s79448

    Article  Google Scholar 

  59. Borrelli E, Sacconi R, Querques L et al (2020) Quantification of diabetic macular ischemia using novel three-dimensional optical coherence tomography angiography metrics. J Biophotonics 13:e202000152. https://doi.org/10.1002/jbio.202000152

    Article  CAS  Google Scholar 

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Correspondence to Hamid Riazi-Esfahani.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional review board of Tehran University of Medical Sciences and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards (IRB Code: IR.TUMS.REC.1399.019).

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Khalili Pour, E., Rezaee, K., Azimi, H. et al. Automated machine learning–based classification of proliferative and non-proliferative diabetic retinopathy using optical coherence tomography angiography vascular density maps. Graefes Arch Clin Exp Ophthalmol 261, 391–399 (2023). https://doi.org/10.1007/s00417-022-05818-z

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