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Screening for diabetic retinopathy in diabetic patients with a mydriasis-free, full-field flicker electroretinogram recording device

Documenta Ophthalmologica volume 140, pages 211–220 (2020)Cite this article

Abstract

Purpose

To investigate the accuracy of the RETeval full-field flicker ERG in the screening of diabetic retinopathy (DR) and vision-threatening diabetic retinopathy (VTDR) and to determine a suitable range of DR diagnostic reference for patients with type 2 diabetes mellitus (T2DM).

Methods

This was a cross-sectional study involving 172 subjects with T2DM, including 71 subjects without clinically detectable DR (NDR), 25 subjects with mild non-proliferative diabetic retinopathy (NPDR), 24 subjects with moderate NPDR, 27 subjects with severe NPDR and 25 subjects with proliferative diabetic retinopathy (PDR). All the subjects underwent a full-field flicker ERG using the RETeval device (DR assessment protocol), which is a mydriasis-free, full-field electroretinogram (ERG) recording system. The performance of the DR assessment protocol in detecting the DR (including mild NPDR, moderate NPDR, severe NPDR and PDR) and VTDR was analyzed with the receiver operating characteristic (ROC) curve.

Results

For the detection of DR (mild NPDR, moderate NPDR, severe NPDR, PDR), the area under the ROC curve was 0.867 (p < 0.001, 95% CI 0.814–0.920), and the best cutoff value for DR was determined to be 20.75, with a sensitivity of 80.2% and specificity of 81.7%. Meanwhile, for the detection of VTDR, the area under the ROC curve was 0.965 (p < 0.001, 95% CI 0.941–0.989), and the best cutoff value was set to 23.05, with a sensitivity of 94.6% and a specificity of 88.8%.

Conclusion

The DR assessment protocol in RETeval device was effective in screening for DR (mild NPDR, moderate NPDR, severe NPDR, PDR) and VTDR in patients with diabetes. It could be helpful in referring and managing patients with T2DM in primary healthcare setting. However, caution should be taken that optimal cutoff value of DR assessment protocol may vary in different ethnic populations.

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References

  1. Lee R, Wong TY, Sabanayagam C (2015) Epidemiology of diabetic retinopathy, diabetic macular edema and related vision loss. Eye Vis 2(1):17. https://doi.org/10.1186/s40662-015-0026-2

    Article  Google Scholar 

  2. Wild SH, Roglic G, Green A, Sicree R, King H (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27(5):1047–1053

    Article  Google Scholar 

  3. Yau JWY, Rogers S, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen S, Dekker JM, Fletcher AE, Grauslund J (2012) Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35(3):556–564

    Article  Google Scholar 

  4. Ting DSW, Cheung G, Wong TY (2016) Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: a review. Clin Exp Ophthalmol 44(4):260–277

    Article  Google Scholar 

  5. Ting DSW, Pasquale LR, Peng L, Campbell JP, Lee AY, Raman R, Tan G, Schmetterer L, Keane PA, Wong TY (2019) Artificial intelligence and deep learning in ophthalmology. Br J Ophthalmol 103(2):167–175

    Article  Google Scholar 

  6. Fukuo M, Kondo M, Hirose A, Fukushima H, Ikesugi K, Sugimoto M, Kato K, Uchigata Y, Kitano S (2016) Screening for diabetic retinopathy using new mydriasis-free, full-field flicker ERG recording device. Sci Rep 6(1):36591

    CAS  Article  Google Scholar 

  7. Lawrence MG (2004) The accuracy of digital-video retinal imaging to screen for diabetic retinopathy: an analysis of two digital-video retinal imaging systems using standard stereoscopic seven-field photography and dilated clinical examination as reference standards. Trans Am Ophthalmol Soc 102:321–340

    PubMed  PubMed Central  Google Scholar 

  8. Maa AY, Feuer WJ, Davis CQ, Pillow EK, Brown TD, Caywood RM, Chasan JE, Fransen SR (2016) A novel device for accurate and efficient testing for vision-threatening diabetic retinopathy. J Diabetes Complicat 30(3):524–532

    Article  Google Scholar 

  9. Degirmenci MFK, Demirel S, Batioglu F, Ozmert E (2018) Role of a mydriasis-free, full-field flicker ERG device in the detection of diabetic retinopathy. Doc Ophthalmol 137(3):131–141

    Article  Google Scholar 

  10. Basevi V (2011) Diagnosis and classification of diabetes mellitus. Diabetes Care 36:S67–S74

    Google Scholar 

  11. Wilkinson CP, Ferris FL, Klein R, Lee PP, Agardh C, Davis MD, Dills DG, Kampik A, Pararajasegaram R, Verdaguer J (2003) Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110(9):1677–1682

    CAS  Article  Google Scholar 

  12. Grading Diabetic Retinopathy from Stereoscopic Color Fundus Photographs; An Extension of the Modified Airlie House Classification: ETDRS Report Number 10 (1991). Ophthalmology 98(5):786–806. https://doi.org/10.1016/s0161-6420(13)38012-9

  13. Kato K, Kondo M, Sugimoto M, Ikesugi K, Matsubara H (2015) Effect of pupil size on flicker ERGs recorded with RETeval system: new mydriasis-free full-field ERG system. Invest Ophthalmol Vis Sci 56(6):3684–3690. https://doi.org/10.1167/iovs.14-16349

    CAS  Article  PubMed  Google Scholar 

  14. Williams GA, Scott IU, Haller JA, Maguire AM, Marcus DM, Mcdonald HR (2004) Single-field fundus photography for diabetic retinopathy screening: a report by the American Academy of Ophthalmology. Ophthalmology 111(5):1055–1062

    Article  Google Scholar 

  15. Bursell S, Cavallerano JD, Cavallerano AA, Clermont AC, Birkmirepeters DP, Aiello LP, Aiello LM (2001) Stereo nonmydriatic digital-video color retinal imaging compared with Early Treatment Diabetic Retinopathy Study seven standard field 35-mm stereo color photos for determining level of diabetic retinopathy. Ophthalmology 108(3):572–585

    CAS  Article  Google Scholar 

  16. Szeto SKH, Wong R, Lok J, Tang F, Sun Z, Tso T, Lam TCH, Tham CC, Ng DS, Cheung CY (2018) Non-mydriatic ultrawide field scanning laser ophthalmoscopy compared with dilated fundal examination for assessment of diabetic retinopathy and diabetic macular oedema in Chinese individuals with diabetes mellitus. Br J Ophthalmol. https://doi.org/10.1136/bjophthalmol-2018-311924

    Article  PubMed  Google Scholar 

  17. Zeng Y, Cao D, Yu H, Yang D, Zhuang X, Hu Y, Li J, Yang J, Wu Q, Liu B, Zhang L (2019) Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy. Br J Ophthalmol. https://doi.org/10.1136/bjophthalmol-2018-313582

    Article  PubMed  Google Scholar 

  18. Pescosolido N, Barbato A, Stefanucci A, Buomprisco G (2015) Role of electrophysiology in the early diagnosis and follow-up of diabetic retinopathy. Exp Diabetes Res 2015:319692

    Google Scholar 

  19. Jain MK, Devan S, Jaisankar D, Swaminathan G, Pardhan S, Raman R (2018) Pupillary abnormalities with varying severity of diabetic retinopathy. Sci Rep 8(1):5636

    Article  Google Scholar 

  20. Ng JS, Bearse MA, Schneck ME, Barez S, Adams AJ (2008) Local diabetic retinopathy prediction by multifocal ERG delays over 3 years. Invest Ophthalmol Vis Sci 49(4):1622–1628

    Article  Google Scholar 

  21. Harrison WW, Bearse MA, Ng JS, Jewell NP, Barez S, Burger D, Schneck ME, Adams AJ (2011) Multifocal electroretinograms predict onset of diabetic retinopathy in adult patients with diabetes. Invest Ophthalmol Vis Sci 52(2):772–777

    Article  Google Scholar 

  22. Lakhani E, Wright TC, Abdolell M, Westall CA (2010) Multifocal ERG defects associated with insufficient long-term glycemic control in adolescents with type 1 diabetes. Invest Ophthalmol Vis Sci 51(10):5297–5303

    Article  Google Scholar 

  23. Yamamoto S, Takeuchi S, Kamiyama M (1997) The short wavelength-sensitive cone electroretinogram in diabetes: relationship to systemic factors. Doc Ophthalmol 94(3):193–200

    Article  Google Scholar 

  24. Abdlseaed AA, Mctaggart Y, Ramage T, Hamilton R, Mcculloch DL (2010) Light- and dark-adapted electroretinograms (ERGs) and ocular pigmentation: comparison of brown- and blue-eyed cohorts. Doc Ophthalmol 121(2):135–146

    Article  Google Scholar 

  25. Wali N, Leguire LE (1993) Fundus pigmentation and the electroretinographic luminance-response function. Doc Ophthalmol 84(1):61–69

    CAS  Article  Google Scholar 

Download references

Funding

This work was supported by Medical Scientific Research Foundation of Guangdong Province, China (Grant Number B2018096), and National Natural Science Foundation of China (Grant Number 81800829). The sponsors or funding organizations had no role in the design or conduct of this research.

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Author notes

  1. Yunkao Zeng and Dan Cao have contributed equally to the work.

Affiliations

  1. Department of Ophthalmology, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, No. 106, Zhongshan Er Road, Yuexiu District, Guangzhou, Guangdong, China

    Yunkao Zeng, Dan Cao, Dawei Yang, Xuenan Zhuang, Honghua Yu, Yunyan Hu, Yan Zhang, Cheng Yang, Miao He & Liang Zhang

  2. Shantou University Medical College, Shantou, China

    Yunkao Zeng, Dawei Yang, Xuenan Zhuang & Yan Zhang

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  1. Yunkao Zeng
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  2. Dan Cao
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  5. Honghua Yu
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  7. Yan Zhang
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Corresponding author

Correspondence to Liang Zhang.

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Zeng, Y., Cao, D., Yang, D. et al. Screening for diabetic retinopathy in diabetic patients with a mydriasis-free, full-field flicker electroretinogram recording device. Doc Ophthalmol 140, 211–220 (2020). https://doi.org/10.1007/s10633-019-09734-2

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Keywords

  • Diabetic retinopathy
  • Screening
  • Electroretinogram
  • Retinal diagnostic test