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Retinal image measurements and their association with chronic kidney disease in Chinese patients with type 2 diabetes: the NCD study

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Abstract

Aims

Retinal and renal microcirculations are known to share similar physiological changes during early diabetes because of abnormal glucose metabolism and other processes. The retinal vasculature therefore may serve as potential biomarker for the early identification of those at high risk of chronic kidney disease (CKD) in diabetes.

Methods

Data from 1925 patients (aged 49.0 ± 10.3) with type 2 diabetes were analyzed. Various retinal image measurements (RIMs) were collected using a validated fully automated computer program. Multiple logistic regressions were performed to investigate the correlation between RIMs and CKD.

Results

In logistic regression adjusting for multiple variables, wider venular calibers in the central and middle zones and narrower arteriolar caliber in the central zone were associated with CKD (p < 0.001, p = 0.020, and p < 0.001, respectively). Increased arteriolar tortuosity was associated with CKD (p = 0.035). Multiple image texture measurements were also significantly associated with CKD.

Conclusions

Renal dysfunction in type 2 diabetes was associated with various retinal image measurements. These non-invasive image measurements may serve as potential biomarkers for the early identification and monitoring of individuals at high risk of CKD in the course of diabetes.

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Availability of data and materials

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

CKD:

Chronic kidney disease

CRAE:

Central retinal arteriolar equivalent

CRVE:

Central retinal venular equivalent

DD:

Disk diameter

DM:

Diabetes mellitus

eGFR:

Estimated glomerular filtration rate

GLCM:

Gray-level co-occurrence matrix

HDL:

High-density lipoprotein

LDL:

Low-density lipoprotein

NCD:

Northwestern China Diabetes

RIM:

Retinal image measurement

References

  1. International Diabetes Federation (2017) IDF Diabetes Atlas (8th Edition). Available from https://www.diabetesatlas.org/. Accessed August 8, 2017

  2. Ravi R, Cull CA, Thorne KI et al. (2006) Risk factors for renal dysfunction in type 2 diabetes: U.K. Prospective Diabetes Study 74. Diabetes 55(6):1832–1839

  3. Colhoun HM, Marcovecchio ML (2018) Biomarkers of diabetic kidney disease. Diabetologia 61(5):996–1011. https://doi.org/10.1007/s00125-018-4567-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Barr EL, Maple-Brown LJ, Barzi F et al (2017) Comparison of creatinine and cystatin C based eGFR in the estimation of glomerular filtration rate in indigenous Australians: the eGFR Study. Clin Biochem 50(6):301–308

    Article  CAS  Google Scholar 

  5. Klein R, Knudtson MD, Klein BE et al (2010) The relationship of retinal vessel diameter to changes in diabetic nephropathy structural variables in patients with type 1 diabetes. Diabetologia 53(8):1638–1646. https://doi.org/10.1007/s00125-010-1763-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Hirsch IB, Michael B (2010) Beyond hemoglobin A1c-need for additional markers of risk for diabetic microvascular complications. J Am Med Assoc 303(22):2291–2292

    Article  CAS  Google Scholar 

  7. Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438(7070):960–966

    Article  CAS  Google Scholar 

  8. Nagaoka T, Yoshida A (2013) Relationship between retinal blood flow and renal function in patients with type 2 diabetes and chronic kidney disease. Diabetes Care 36(4):957–961

    Article  CAS  Google Scholar 

  9. Grauslund J, Hodgson L, Kawasaki R et al (2009) Retinal vessel calibre and micro- and macrovascular complications in type 1 diabetes. Diabetologia 52(10):2213–2217. https://doi.org/10.1007/s00125-009-1459-8

    Article  CAS  PubMed  Google Scholar 

  10. Sasongko MB, Wong TY, Nguyen TT et al (2011) Retinal vascular tortuosity in persons with diabetes and diabetic retinopathy. Diabetologia 54(9):2409–2416

    Article  CAS  Google Scholar 

  11. Broe R, Rasmussen ML, Frydkjaer-Olsen U et al (2014) Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987). Diabetologia 57(10):2215–2221

    Article  CAS  Google Scholar 

  12. Cheung CY, Ikram MK, Klein R et al (2015) The clinical implications of recent studies on the structure and function of the retinal microvasculature in diabetes. Diabetologia 58(5):871–885. https://doi.org/10.1007/s00125-015-3511-1

    Article  CAS  PubMed  Google Scholar 

  13. Sabanayagam C, Shankar A, Klein BEK et al (2011) Bidirectional association of retinal vessel diameters and estimated GFR decline: the Beaver Dam CKD Study. Am J Kidney Dis 57(5):682–691. https://doi.org/10.1053/j.ajkd.2010.11.025

    Article  PubMed  PubMed Central  Google Scholar 

  14. Benitez-Aguirre PZ, Wong TY, Craig ME et al (2018) The adolescent cardio-renal intervention trial (AdDIT): retinal vascular geometry and renal function in adolescents with type 1 diabetes. Diabetologia 7(10):1–9

    Google Scholar 

  15. Poplin R, Varadarajan AV, Blumer K et al. (2017) Predicting cardiovascular risk factors from retinal fundus photographs using deep learning. 2(3)

  16. Lim LS, Cheung CY, Sabanayagam C et al (2013) Structural changes in the retinal microvasculature and renal function. Invest Ophthalmol Vis Sci 54(4):2970–2976

    Article  Google Scholar 

  17. Aerts HJWL, Velazquez ER, Leijenaar RTH et al (2014) Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun 5:4006

    Article  CAS  Google Scholar 

  18. Itakura H, Achrol AS, Mitchell LA et al. (2015) Magnetic resonance image features identify glioblastoma phenotypic subtypes with distinct molecular pathway activities. Sci Translational Med 7(303):303ra138

    Article  Google Scholar 

  19. Levey AS, Bosch JP, Lewis JB et al. (1999) A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Internal Med 130

  20. National Kidney Foundation (2002) K/DOQI clinical practice guidelines for chronic kidney disease: evaluation, classification, and stratification. Am J Kidney Dis 39:S1-266

    Google Scholar 

  21. Xu X, Wang R, Lv P et al (2018) Simultaneous arteriole and venule segmentation with domain-specific loss function on a new public database. Biomed Opt Express 9(7):3153–3166. https://doi.org/10.1364/BOE.9.003153

    Article  PubMed  PubMed Central  Google Scholar 

  22. Xu X, Niemeijer M, Song Q et al (2011) Vessel boundary delineation on fundus images using graph-based approach. IEEE Trans Med Imaging 30(6):1184–1191

    Article  Google Scholar 

  23. Xu X, Sun F, Wang Q et al (2020) Comprehensive retinal vascular measurements: a novel association with renal function in type 2 diabetic patients in China. Scientific Reports 10(1):13737. https://doi.org/10.1038/s41598-020-70408-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Stosic T, Stosic BD (2006) Multifractal analysis of human retinal vessels. IEEE Trans Med Imaging 25(8):1101–1107. https://doi.org/10.1109/TMI.2006.879316

    Article  PubMed  Google Scholar 

  25. Hart WE, Goldbaum M, Côté B et al (1999) Measurement and classification of retinal vascular tortuosity. Int J Med Informatics 53(2–3):239–252

    Article  CAS  Google Scholar 

  26. Zenere BM, Arcaro G, Saggiani F et al (1995) Noninvasive detection of functional alterations of the arterial wall in IDDM patients with and without microalbuminuria. Diabetes Care 18(7):975

    Article  CAS  Google Scholar 

  27. Hubbard LD, Brothers RJ, King WN et al (1999) Methods for evaluation of retinal microvascular abnormalities associated with hypertension/sclerosis in the atherosclerosis risk in communities Study11 the authors have no proprietary interest in the equipment and techniques described in this article. Ophthalmology 106(12):2269–2280. https://doi.org/10.1016/s0161-6420(99)90525-0

    Article  CAS  PubMed  Google Scholar 

  28. Knudtson MD, Lee KE, Hubbard LD et al (2003) Revised formulas for summarizing retinal vessel diameters. Curr Eye Res 27(3):143–149

    Article  Google Scholar 

  29. Sasongko MB, Wong TY, Donaghue KC et al (2012) Retinal arteriolar tortuosity is associated with retinopathy and early kidney dysfunction in type 1 diabetes. Am J Ophthalmol 153(1):176–183. https://doi.org/10.1016/j.ajo.2011.06.005

    Article  PubMed  Google Scholar 

  30. Yau JWY, Xie J, Kawasaki R et al (2011) Retinal arteriolar narrowing and subsequent development of CKD Stage 3: the multi-ethnic study of atherosclerosis (MESA). Am J Kidney Dis 58(1):39–46

    Article  Google Scholar 

  31. Yip W, Sabanayagam C, Teo BW et al (2015) Retinal microvascular abnormalities and risk of renal failure in Asian populations. PLoS ONE 10(2):e0118076. https://doi.org/10.1371/journal.pone.0118076

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was financially supported by Shaanxi National Science Foundation (2020JQ-071), National Natural Science Foundation of China (81401480), Top talent fund of Tangdu Hospital and Innovation fund of Tangdu Hospital.

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Authors and Affiliations

Authors

Contributions

XX and BG designed the study and interpreted the results. XX, BG, and FX wrote the manuscript. WD analyzed the images and performed statistical analysis. BG, MZ, QW, and QJ collected the clinical data. QJ supervised the data quality control and statistical analysis. JL, TT, and FS contributed to the discussion and edited the manuscript. XX and BG had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding authors

Correspondence to Qiuhe Ji or Feng Xu.

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Conflict of interest

No potential conflicts of interests relevant to this article were reported.

Ethics approval and consent to participate

All data were collected with approval by the Institutional Review Board of Chinese Air Force Medical University in accordance with the tenets of the Declaration of Helsinki. Informed consent was obtained from all participants.

Informed consent

Written informed consent was obtained from all participants.

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This article belongs to the topical collection Diabetic Nephropathy, managed by Giuseppe Pugliese.

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Xu, X., Gao, B., Ding, W. et al. Retinal image measurements and their association with chronic kidney disease in Chinese patients with type 2 diabetes: the NCD study. Acta Diabetol 58, 363–370 (2021). https://doi.org/10.1007/s00592-020-01621-6

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  • DOI: https://doi.org/10.1007/s00592-020-01621-6

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