Klin Monbl Augenheilkd 2018; 235(04): 377-384
DOI: 10.1055/s-0044-101827
Übersicht
Georg Thieme Verlag KG Stuttgart · New York

The Use of Optical Coherence Tomography for the Detection of Early Diabetic Retinopathy

Optische Kohärenztomografie in der Diagnose der frühen diabetischen Retinopathie
Gabor Mark Somfai
1   Retinology Unit, Pallas Kliniken, Olten, Switzerland (Chair: Prof. Heinrich Gerding)
2   Department of Ophthalmology, Semmelweis University, Budapest, Hungary (Chair: Prof. Zoltan Zsolt Nagy)
,
Heinrich Gerding
1   Retinology Unit, Pallas Kliniken, Olten, Switzerland (Chair: Prof. Heinrich Gerding)
3   Department of Ophthalmology, University of Münster, Münster, Germany (Chair: Prof. Nicole Eter)
,
Delia Cabrera DeBuc
4   Bascom Palmer Eye Institute, Miller School of Medicine, University of Miami, Miami, FL, USA (Chair: Prof. Eduardo C. Alfonso)
› Author Affiliations
Further Information

Publication History

received 04 October 2017

accepted 21 January 2018

Publication Date:
18 April 2018 (online)

Abstract

Diabetic retinopathy (DR) is one of the leading causes of vision loss globally with a severe burden on all societies due to its high treatment and rehabilitation costs. The early diagnosis of DR may provide preventive steps (including retinal laser therapy and tight carbohydrate, blood pressure, and cholesterol control) that could in turn help to avoid progression of the pathology with the resultant vision loss. Optical coherence tomography (OCT) enables the in vivo structural imaging of the retina, providing both qualitative (structure) and quantitative (thickness) information. In the past decades, extensive OCT research has been done in the field of DR. In the present review, we are focusing on those that were aiming at detection of the earliest retinal changes before DR could be diagnosed funduscopically. The latest, widely available technology of spectral-domain (SD-)OCT comes with a fast and reliable retinal imaging, which, together with the most recent developments in image processing and artificial intelligence, holds the promise of developing a quick and efficient, state-of-the-art screening tool for DR.

Zusammenfassung

Diabetische Retinopathie (DR) ist eine der führenden Ursachen des Sehverlustes weltweit und stellt wegen der hohen Behandlungs- und Rehabilitationskosten eine hohe Belastung für alle Gesellschaftsebenen dar. Durch eine früh gestellte Diagnose der DR kann die Feineinstellung von Blutzucker, Blutdruck und Cholesterin erzielt und eine frühzeitige Laserbehandlung der Netzhaut durchgeführt werden, welche die Progression und den dadurch auftretenden Sehverlust vermeiden. Die optische Kohärenztomografie (OCT) ist ein bildgebendes Verfahren, mit welchem die Netzhautstruktur in vivo dargestellt werden kann und das wichtige qualitative (Struktur) und quantitative (Dicke) Informationen über die Netzhaut liefert. In der letzten Zeit wurde Vieles im Bereich der OCT-Diagnostik von diabetischer Retinopathie erforscht. In unserem Review wollen wir uns auf die frühestmögliche Diagnosestellung mithilfe der OCT-Technologie fokussieren. Die neueste, auf dem Markt weitgehend erhältliche Spektral-Domänen-OCT-Technologie (SD-OCT) bietet ein schnelles und genaues Imaging der Netzhaut, das zusammen mit den neuesten Entwicklungen im Bereich Bildbearbeitung und künstlicher Intelligenz sehr vielversprechend in Bezug auf ein schnelles und effizientes Screening der frühen diabetischen Retinopathie ist.

 
  • References

  • 1 Leasher JL, Bourne RR, Flaxman SR. et al. Global estimates on the number of people blind or visually impaired by diabetic retinopathy: a meta-analysis from 1990 to 2010. Diabetes Care 2016; 39: 1643-1649 doi:10.2337/dc15-2171
  • 2 Hutton DW, Stein JD, Bressler NM. et al. Cost-effectiveness of intravitreous ranibizumab compared with panretinal photocoagulation for proliferative diabetic retinopathy: secondary analysis from a diabetic retinopathy clinical research network randomized clinical trial. JAMA Ophthalmol 2017; 135: 576-584 doi:10.1001/jamaophthalmol.2017.0837
  • 3 Ross EL, Hutton DW, Stein JD. et al. Cost-effectiveness of aflibercept, bevacizumab, and ranibizumab for diabetic macular edema treatment: analysis from the Diabetic Retinopathy Clinical Research Network Comparative Effectiveness Trial. JAMA Ophthalmol 2016; 134: 888-896 doi:10.1001/jamaophthalmol.2016.1669
  • 4 Huang D, Swanson EA, Lin CP. et al. Optical coherence tomography. Science 1991; 254: 1178-1181
  • 5 Puliafito CA. Optical coherence tomography: 20 years after. Ophthalmic Surg Lasers Imaging 2010; 41 (Suppl. 05)
  • 6 Luu CD, Szental JA, Lee SY. et al. Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci 2010; 51: 482-486 doi:10.1167/iovs.09-4069
  • 7 Aung MH, Kim MK, Olson DE. et al. Early visual deficits in streptozotocin-induced diabetic long evans rats. Invest Ophthalmol Vis Sci 2013; 54: 1370-1377 doi:10.1167/iovs.12-10927
  • 8 Kern TS, Barber AJ. Retinal ganglion cells in diabetes. J Physiol 2008; 586: 4401-4408 doi:10.1113/jphysiol.2008.156695
  • 9 Enzsoly A, Szabo A, Kantor O. et al. Pathologic alterations of the outer retina in streptozotocin-induced diabetes. Invest Ophthalmol Vis Sci 2014; 55: 3686-3699 doi:10.1167/iovs.13-13562
  • 10 Enzsoly A, Szabo A, Szabo K. et al. Novel features of neurodegeneration in the inner retina of early diabetic rats. Histol Histopathol 2015; 30: 971-985 doi:10.14670/HH-11-602
  • 11 Szabo K, Enzsoly A, Dekany B. et al. Histological evaluation of diabetic neurodegeneration in the retina of zucker diabetic fatty (ZDF) rats. Sci Rep 2017; 7: 8891 doi:10.1038/s41598-017-09068-6
  • 12 Hammoum I, Benlarbi M, Dellaa A. et al. Study of retinal neurodegeneration and maculopathy in diabetic Meriones shawi: A particular animal model with human-like macula. J Comp Neurol 2017; 525: 2890-2914 doi:10.1002/cne.24245
  • 13 Barber AJ, Gardner TW, Abcouwer SF. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci 2011; 52: 1156-1163 doi:10.1167/iovs.10-6293
  • 14 Biallosterski C, van Velthoven ME, Michels RP. et al. Decreased optical coherence tomography-measured pericentral retinal thickness in patients with diabetes mellitus type 1 with minimal diabetic retinopathy. Br J Ophthalmol 2007; 91: 1135-1138 doi:10.1136/bjo.2006.111534
  • 15 Nilsson M, von Wendt G, Wanger P. et al. Early detection of macular changes in patients with diabetes using Rarebit Fovea Test and optical coherence tomography. Br J Ophthalmol 2007; 91: 1596-1598 doi:10.1136/bjo.2007.124461
  • 16 Cabrera Fernandez D, Salinas HM, Puliafito CA. Automated detection of retinal layer structures on optical coherence tomography images. Opt Express 2005; 13: 10200-10216
  • 17 Ishikawa H, Stein DM, Wollstein G. et al. Macular segmentation with optical coherence tomography. Invest Ophthalmol Vis Sci 2005; 46: 2012-2017 doi:10.1167/iovs.04-0335
  • 18 Cabrera DeBuc D, Somfai GM. Early detection of retinal thickness changes in diabetes using Optical Coherence Tomography. Med Sci Monit 2010; 16: MT15-MT21
  • 19 van Dijk HW, Kok PH, Garvin M. et al. Selective loss of inner retinal layer thickness in type 1 diabetic patients with minimal diabetic retinopathy. Invest Ophthalmol Vis Sci 2009; 50: 3404-3409 doi:10.1167/iovs.08-3143
  • 20 Chalam KV, Bressler SB, Edwards AR. et al. Retinal thickness in people with diabetes and minimal or no diabetic retinopathy: Heidelberg Spectralis optical coherence tomography. Invest Ophthalmol Vis Sci 2012; 53: 8154-8161 doi:10.1167/iovs.12-10290
  • 21 Tatrai E, Ranganathan S, Ferencz M. et al. Comparison of retinal thickness by Fourier-domain optical coherence tomography and OCT retinal image analysis software segmentation analysis derived from Stratus optical coherence tomography images. J Biomed Opt 2011; 16: 056004 doi:10.1117/1.3573817
  • 22 van Dijk HW, Verbraak FD, Kok PH. et al. Decreased retinal ganglion cell layer thickness in patients with type 1 diabetes. Invest Ophthalmol Vis Sci 2010; 51: 3660-3665 doi:10.1167/iovs.09-5041
  • 23 van Dijk HW, Verbraak FD, Kok PH. et al. Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci 2012; 53: 2715-2719 doi:10.1167/iovs.11-8997
  • 24 Vujosevic S, Midena E. Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Muller cells alterations. J Diabetes Res 2013; 2013: 905058 doi:10.1155/2013/905058
  • 25 Scarinci F, Picconi F, Virgili G. et al. Single retinal layer evaluation in patients with type 1 diabetes with no or early signs of diabetic retinopathy: the first hint of neurovascular crosstalk damage between neurons and capillaries?. Ophthalmologica 2017; 237: 223-231 doi:10.1159/000453551
  • 26 Wanek J, Blair NP, Chau FY. et al. Alterations in retinal layer thickness and reflectance at different stages of diabetic retinopathy by en face optical coherence tomography. Invest Ophthalmol Vis Sci 2016; 57: OCT341-OCT347 doi:10.1167/iovs.15-18715
  • 27 Gundogan FC, Akay F, Uzun S. et al. Early neurodegeneration of the inner retinal layers in type 1 diabetes mellitus. Ophthalmologica 2016; 235: 125-132 doi:10.1159/000442826
  • 28 El-Fayoumi D, Badr Eldine NM, Esmael AF. et al. Retinal nerve fiber layer and ganglion cell complex thicknesses are reduced in children with type 1 diabetes with no evidence of vascular retinopathy. Invest Ophthalmol Vis Sci 2016; 57: 5355-5360 doi:10.1167/iovs.16-19988
  • 29 Karti O, Nalbantoglu O, Abali S. et al. Retinal ganglion cell loss in children with type 1 diabetes mellitus without diabetic retinopathy. Ophthalmic Surg Lasers Imaging Retina 2017; 48: 473-477 doi:10.3928/23258160-20170601-05
  • 30 Chen Y, Li J, Yan Y. et al. Diabetic macular morphology changes may occur in the early stage of diabetes. BMC Ophthalmol 2016; 16: 12 doi:10.1186/s12886-016-0186-4
  • 31 Carpineto P, Toto L, Aloia R. et al. Neuroretinal alterations in the early stages of diabetic retinopathy in patients with type 2 diabetes mellitus. Eye (Lond) 2016; 30: 673-679 doi:10.1038/eye.2016.13
  • 32 Ng DS, Chiang PP, Tan G. et al. Retinal ganglion cell neuronal damage in diabetes and diabetic retinopathy. Clin Exp Ophthalmol 2016; 44: 243-250 doi:10.1111/ceo.12724
  • 33 Pierro L, Iuliano L, Cicinelli MV. et al. Retinal neurovascular changes appear earlier in type 2 diabetic patients. Eur J Ophthalmol 2017; 27: 346-351 doi:10.5301/ejo.5000887
  • 34 Tavares Ferreira J, Alves M, Dias-Santos A. et al. Retinal neurodegeneration in diabetic patients without diabetic retinopathy. Invest Ophthalmol Vis Sci 2016; 57: 6455-6460 doi:10.1167/iovs.16-20215
  • 35 Shelton R, Taibl J, Shemonski N. et al. Subretinal layer thickness ratio changes for early detection of diabetes. Invest Ophthalmol Vis Sci 2013; 54: 2428
  • 36 Bhaduri B, Shelton RL, Nolan RM. et al. Ratiometric analysis of optical coherence tomography-measured in vivo retinal layer thicknesses for the detection of early diabetic retinopathy. J Biophotonics 2017; 10: 1430-1441 doi:10.1002/jbio.201600282
  • 37 Ribeiro L, Bandello F, Tejerina AN. et al. Characterization of retinal disease progression in a 1-year longitudinal study of eyes with mild nonproliferative retinopathy in diabetes type 2. Invest Ophthalmol Vis Sci 2015; 56: 5698-5705 doi:10.1167/iovs.15-16708
  • 38 Sohn EH, van Dijk HW, Jiao C. et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus. Proc Natl Acad Sci U S A 2016; 113: E2655-E2664 doi:10.1073/pnas.1522014113
  • 39 Somfai GM, Tian J, Lee WH. et al. Outer retinal changes in patients with diabetes and no or mild non-proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci 2017; 58: 101
  • 40 Simo R, Bandello F, Grauslund J. et al. Topical administration of somatostatin and brimonidine in the early stages of diabetic retinopathy: results of the EUROCONDOR study. Diabetologia 2017; 60: 1 Available at https://doi.org/10.1007/s00125-017-4350-z Accessed January 17, 2018
  • 41 Dehghani C, Srinivasan S, Edwards K. et al. Presence of peripheral neuropathy is associated with progressive thinning of retinal nerve fiber layer in type 1 diabetes. Invest Ophthalmol Vis Sci 2017; 58: BIO234-BIO239 doi:10.1167/iovs.17-21801
  • 42 Srinivasan S, Dehghani C, Pritchard N. et al. Optical coherence tomography predicts 4-year incident diabetic neuropathy. Ophthalmic Physiol Opt 2017; 37: 451-459 doi:10.1111/opo.12391
  • 43 Cunha-Vaz J, Ribeiro L, Costa M. et al. Diabetic retinopathy phenotypes of progression to macular edema: pooled analysis from independent longitudinal studies of up to 2 yearsʼ duration. Invest Ophthalmol Vis Sci 2017; 58: BIO206-BIO210 doi:10.1167/iovs.17-21780
  • 44 Schmitt JM, Knuttel A, Bonner RF. Measurement of optical properties of biological tissues by low-coherence reflectometry. Appl Opt 1993; 32: 6032-6042 doi:10.1364/AO.32.006032
  • 45 Gao W, Tátrai E, Ölvedy V. et al. Investigation of changes in thickness and reflectivity from layered retinal structures of healthy and diabetic eyes with optical coherence tomography. J Biomed Sci Eng 2011; 4: 657-665 doi:10.4236/jbise.2011.410082
  • 46 Baroni M, Fortunato P, La Torre A. Towards quantitative analysis of retinal features in optical coherence tomography. Med Eng Phys 2007; 29: 432-441 doi:10.1016/j.medengphy.2006.06.003
  • 47 DeBuc D, Tátrai E, Laurik KL. et al. Identifying local structural and optical derangement in the neural retina of individuals with type 1 diabetes. J Clin Exp Ophthalmol 2013; 4: 289
  • 48 Somfai GM, Tatrai E, Laurik L. et al. Fractal-based analysis of optical coherence tomography data to quantify retinal tissue damage. BMC Bioinformatics 2014; 15: 295 doi:10.1186/1471-2105-15-295
  • 49 Gao W, DeBuc DC, Zakharov VP. et al. Two-dimensional fractal analysis of retinal tissue of healthy and diabetic eyes with optical coherence tomography. J Biomed Photonics Eng 2016; 2: 040302
  • 50 Toprak I, Yildirim C, Yaylali V. Impaired photoreceptor inner segment ellipsoid layer reflectivity in mild diabetic retinopathy. Can J Ophthalmol 2015; 50: 438-441 doi:10.1016/j.jcjo.2015.07.009
  • 51 Newell A, Simon HA. Computer science as empirical inquiry: symbols and search. Commun ACM 1976; 19: 113-126 doi:10.1145/360018.360022
  • 52 Dhar V. The future of artificial intelligence. Big Data 2016; 4: 5-9 doi:10.1089/big.2016.29004.vda
  • 53 Somfai GM, Tatrai E, Laurik L. et al. Automated classifiers for early detection and diagnosis of retinopathy in diabetic eyes. BMC Bioinformatics 2014; 15: 106 doi:10.1186/1471-2105-15-106
  • 54 Fang L, Cunefare D, Wang C. et al. Automatic segmentation of nine retinal layer boundaries in OCT images of non-exudative AMD patients using deep learning and graph search. Biomed Opt Express 2017; 8: 2732-2744 doi:10.1364/BOE.8.002732
  • 55 ElTanboly A, Ismail M, Shalaby A. et al. A computer-aided diagnostic system for detecting diabetic retinopathy in optical coherence tomography images. Med Phys 2017; 44: 914-923 doi:10.1002/mp.12071
  • 56 DeBuc DC. The role of retinal imaging and portable screening devices in tele-ophthalmology applications for diabetic retinopathy management. Curr Diab Rep 2016; 16: 132 doi:10.1007/s11892-016-0827-2
  • 57 Windsor MA, Sun SJJ, Frick KD. et al. Estimating public and patient savings from basic research – a study of optical coherence tomography in managing antiangiogenic therapy. Am J Ophthalmol 2018; 185: 115-122 doi:10.1016/j.ajo.2017.09.027
  • 58 Yurtsever G, Povazay B, Alex A. et al. Photonic integrated Mach-Zehnder interferometer with an on-chip reference arm for optical coherence tomography. Biomed Opt Express 2014; 5: 1050-1061 doi:10.1364/BOE.5.001050
  • 59 Dsouza R, Subhash H, Neuhaus K. et al. Dermascope guided multiple reference optical coherence tomography. Biomed Opt Express 2014; 5: 2870-2882 doi:10.1364/BOE.5.002870
  • 60 Shelton RL, Jung W, Sayegh SI. et al. Optical coherence tomography for advanced screening in the primary care office. J Biophotonics 2014; 7: 525-533 doi:10.1002/jbio.201200243
  • 61 Yang J, Liu L, Campbell JP. et al. Handheld optical coherence tomography angiography. Biomed Opt Express 2017; 8: 2287-2300 doi:10.1364/BOE.8.002287
  • 62 Chakravarthy U, Goldenberg D, Young G. et al. Automated identification of lesion activity in neovascular age-related macular degeneration. Ophthalmology 2016; 123: 1731-1736 doi:10.1016/j.ophtha.2016.04.005