Top

BMC Endocrine Disorders

Published in:

Open Access 01-12-2023 | Diabetic Retinopathy | Research article

Retinal microvascular changes in diabetic patients with diabetic nephropathy

Authors: Yujie Yan, Liping Yu, Chuan Sun, Haipeng Zhao, Hongsong Zhang, Zhijun Wang

Published in: BMC Endocrine Disorders | Issue 1/2023

Abstract

Background

To explore the characteristics of retina microvascular changes in patients with diabetic nephropathy (DN) and its risk factors.

Methods

Retrospective, observational study. 145 patients with type 2 diabetic mellitus (DM) and DN were included in the study. Demographic and clinical parameters were obtained from medical records. Presence of diabetic retinopathy (DR), hard exudates (HEs) and diabetic macular edema (DME) were evaluated according to the color fundus images, optical coherence tomography (OCT) and fluorescence angiography (FFA).

Results

DR accounted for 61.4% in type 2 DM patients with DN, of which proliferative diabetic retinopathy (PDR) accounted for 23.6% and sight threatening DR accounted for 35.7%. DR group had significantly higher levels of low-density lipoprotein cholesterol (LDL-C) (p = 0.004), HbA1c (P = 0.037), Urine albumin creatine ratio (ACR) (p < 0.001) and lower level of estimated glomerular filtration rate (eGFR) (P = 0.013). Logistic regression analysis showed DR was significantly associated with ACR stage (p = 0.011). Subjects with ACR stage3 had higher incidence of DR compared with subjects with ACR stage1 (OR = 24.15, 95%CI: 2.06–282.95). 138 eyes of 138 patients were analyzed for HEs and DME, of which 23.2% had HEs in posterior pole and 9.4% had DME. Visual acuity was worse in HEs group than in non-HEs group. There was significant difference in the LDL-C cholesterol level, total cholesterol (CHOL) level and ACR between HEs group and non-HEs group.

Conclusions

A relatively higher prevalence of DR was found in type 2 DM patients with DN. ACR stage could be recognized as a risk factor for DR in DN patients. Patients with DN needs ophthalmic examination more timely and more frequently.

Available only for authorised users

Kerner W, Bruckel J. Definition, classification and diagnosis of diabetes mellitus. Exp Clin Endocrinol Diabetes. 2014;122(7):384–6. https://doi.org/10.1055/s-0034-1366278.CrossRefPubMed

Xu Y, Wang L, He J, et al. Prevalence and control of diabetes in Chinese adults. JAMA. 2013;310(9):948–59. https://doi.org/10.1001/jama.2013.168118.CrossRefPubMed

Deng YX, Ye WQ, Sun YT, et al. A meta-analysis of prevalence of diabetic retinopathy in China. Zhonghua Yi Xue Za Zhi. 2020;100(48):3846–52. https://doi.org/10.3760/cma.j.cn112137-20200925-02720.CrossRefPubMed

Al-Rubeaan K, Youssef AM, Subhani SN, et al. Diabetic nephropathy and its risk factors in a society with a type 2 diabetes epidemic: a Saudi National Diabetes Registry-based study. PLoS ONE. 2014;9(2): e88956. https://doi.org/10.1371/journal.pone.0088956.CrossRefPubMedPubMedCentral

Edwards MS, Wilson DB, Craven TE, et al. Associations between retinal microvascular abnormalities and declining renal function in the elderly population: the Cardiovascular Health Study. Am J Kidney Dis. 2005;46(2):214–24. https://doi.org/10.1053/j.ajkd.2005.05.005.CrossRefPubMed

Jeng CJ, Hsieh YT, Yang CM, et al. Diabetic Retinopathy in Patients with Diabetic Nephropathy: Development and Progression. PLoS ONE. 2016;11(8): e161897. https://doi.org/10.1371/journal.pone.0161897.CrossRef

Park YH, Shin JA, Han JH, et al. The association between chronic kidney disease and diabetic retinopathy: the Korea National Health and Nutrition Examination Survey 2008–2010. PLoS ONE. 2015;10(4): e125338. https://doi.org/10.1371/journal.pone.0125338.CrossRef

Girach A, Vignati L. Diabetic microvascular complications–can the presence of one predict the development of another. J Diabetes Complications. 2006;20(4):228–37. https://doi.org/10.1016/j.jdiacomp.2006.03.001.CrossRefPubMed

Singh A, Stewart JM. Pathophysiology of diabetic macular edema. Int Ophthalmol Clin. 2009;49(2):1–11. https://doi.org/10.1097/IIO.0b013e31819fd164.CrossRefPubMed

10.

Grading diabetic retinopathy from stereoscopic color fundus photographs--an extension of the modified Airlie House classification. ETDRS report number 10. Early Treatment Diabetic Retinopathy Study Research Group - PubMed (nih.gov).

11.

Chew EY, Klein ML, Ferris FR, et al. Association of elevated serum lipid levels with retinal hard exudate in diabetic retinopathy. Early Treatment Diabetic Retinopathy Study (ETDRS) Report 22. Arch Ophthalmol. 1996;114(9):1079–84. https://doi.org/10.1001/archopht.1996.01100140281004.CrossRefPubMed

12.

Domalpally A, Ip MS, Ehrlich JS. Effects of intravitreal ranibizumab on retinal hard exudate in diabetic macular edema: findings from the RIDE and RISE phase III clinical trials. Ophthalmology. 2015;122(4):779–86. https://doi.org/10.1016/j.ophtha.2014.10.028.CrossRefPubMed

13.

Matsuo T. Disappearance of diabetic macular hard exudates after hemodialysis introduction. Acta Med Okayama. 2006;60(3):201–5. https://doi.org/10.18926/AMO/30746.CrossRefPubMed

14.

Wilkinson CP, Ferris FR, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110(9):1677–82. https://doi.org/10.1016/S0161-6420(03)00475-5.CrossRefPubMed

15.

Lee WJ, Sobrin L, Lee MJ, et al. The relationship between diabetic retinopathy and diabetic nephropathy in a population-based study in Korea (KNHANES V-2, 3). Invest Ophthalmol Vis Sci. 2014;55(10):6547–53. https://doi.org/10.1167/iovs.14-15001.CrossRefPubMed

16.

Zhang X, Saaddine JB, Chou CF, et al. Prevalence of diabetic retinopathy in the United States, 2005–2008. JAMA. 2010;304(6):649–56. https://doi.org/10.1001/jama.2010.1111.CrossRefPubMedPubMedCentral

17.

Zhang J, Wang Y, Li L, et al. Diabetic retinopathy may predict the renal outcomes of patients with diabetic nephropathy. Ren Fail. 2018;40(1):243–51. https://doi.org/10.1080/0886022X.2018.1456453.CrossRefPubMedPubMedCentral

18.

Cao X, Gong X, Ma X. Diabetic Nephropathy versus Diabetic Retinopathy in a Chinese Population: A Retrospective Study. Med Sci Monit. 2019;25:6446–53. https://doi.org/10.12659/MSM.915917.CrossRefPubMedPubMedCentral

19.

He F, Xia X, Wu XF, et al. Diabetic retinopathy in predicting diabetic nephropathy in patients with type 2 diabetes and renal disease: a meta-analysis. Diabetologia. 2013;56(3):457–66. https://doi.org/10.1007/s00125-012-2796-6.CrossRefPubMed

20.

Hsieh YT, Hsieh MC. Time-sequential correlations between diabetic kidney disease and diabetic retinopathy in type 2 diabetes - an 8-year prospective cohort study. Acta Ophthalmol. 2021;99(1):e1–6. https://doi.org/10.1111/aos.14487.CrossRefPubMed

21.

Chen D, Sun X, Zhao X, et al. Associations of serum uric acid and urinary albumin with the severity of diabetic retinopathy in individuals with type 2 diabetes. BMC Ophthalmol. 2020;20(1):467. https://doi.org/10.1186/s12886-020-01713-5.CrossRefPubMedPubMedCentral

22.

Carl-Joe M, Maamoun AF, Hani T, et al. Five-Year Incidence and Progression of Diabetic Retinopathy in Patients with Type II Diabetes in a Tertiary Care Center in Lebanon. J Ophthalmol. 2017;2017:9805145. https://doi.org/10.1155/2017/9805145.CrossRef

23.

Mohan VK, Suneetha N, Jyothi I. Microalbuminuria and low hemoglobin as risk factors for the occurrence and increasing severity of diabetic retinopathy. Indian J Ophthalmol. 2011;59(3):207–10. https://doi.org/10.4103/0301-4738.81029.CrossRefPubMedCentral

24.

Kario K, Matsuo T, Kobayashi H, et al. Factor VII hyperactivity and endothelial cell damage are found in elderly hypertensives only when concomitant with microalbuminuria. Arterioscler Thromb Vasc Biol. 1996;16(3):455–61. https://doi.org/10.1161/01.atv.16.3.455.CrossRefPubMed

25.

Tryggestad JB, Shah RD, Braffett BH, et al. Circulating adhesion molecules and associations with HbA1c, hypertension, nephropathy, and retinopathy in the Treatment Options for type 2 Diabetes in Adolescent and Youth study. Pediatr Diabetes. 2020;21(6):923–31. https://doi.org/10.1111/pedi.13062.CrossRefPubMedPubMedCentral

26.

Cha DR, Kang YS, Han SY, et al. Vascular endothelial growth factor is increased during early stage of diabetic nephropathy in type II diabetic rats. J Endocrinol. 2004;183(1):183–94. https://doi.org/10.1677/joe.1.05647.CrossRefPubMed

27.

Pawlak K, Mysliwiec M, Pawlak D. Oxidative stress, phosphate and creatinine levels are independently associated with vascular endothelial growth factor levels in patients with chronic renal failure. Cytokine. 2008;43(1):98–101. https://doi.org/10.1016/j.cyto.2008.03.011.CrossRefPubMed

28.

Lammer J, Bolz M, Baumann B, et al. Detection and analysis of hard exudates by polarization-sensitive optical coherence tomography in patients with diabetic maculopathy. Invest Ophthalmol Vis Sci. 2014;55(3):1564–71. https://doi.org/10.1167/iovs.13-13539.CrossRefPubMed

29.

van Leiden HA, Dekker JM, Moll AC, et al. Blood pressure, lipids, and obesity are associated with retinopathy: the hoorn study. Diabetes Care. 2002;25(8):1320–5. https://doi.org/10.2337/diacare.25.8.1320.CrossRefPubMed

30.

Miljanovic B, Glynn RJ, Nathan DM, et al. A prospective study of serum lipids and risk of diabetic macular edema in type 1 diabetes. Diabetes. 2004;53(11):2883–92. https://doi.org/10.2337/diabetes.53.11.2883.CrossRefPubMed

31.

Sachdev N, Sahni A. Association of systemic risk factors with the severity of retinal hard exudates in a north Indian population with type 2 diabetes. J Postgrad Med. 2010;56(1):3–6. https://doi.org/10.4103/0022-3859.62419.CrossRefPubMed

32.

Sasaki M, Kawasaki R, Noonan JE, et al. Quantitative measurement of hard exudates in patients with diabetes and their associations with serum lipid levels. Invest Ophthalmol Vis Sci. 2013;54(8):5544–50. https://doi.org/10.1167/iovs.13-11849.CrossRefPubMed

Title: Retinal microvascular changes in diabetic patients with diabetic nephropathy
Authors: Yujie Yan
Liping Yu
Chuan Sun
Haipeng Zhao
Hongsong Zhang
Zhijun Wang
Publication date: 01-12-2023
Publisher: BioMed Central
Keywords: Diabetic Retinopathy
Diabetic Retinopathy
Diabetic Nephropathy
Diabetes
Published in: BMC Endocrine Disorders / Issue 1/2023
Electronic ISSN: 1472-6823
DOI: https://doi.org/10.1186/s12902-022-01250-w

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2023

Subacute thyroiditis presenting as simple acute headache was misdiagnosed as meningitis: case report and literature review

Correlation between biochemical and clinical hyperandrogenism parameter in polycystic ovary syndrome in relation to age

Insulinaemic potential of diet and lifestyle and risk of type 2 diabetes in the Iranian adults: result from Yazd health study

Effect of mastication evaluation and intervention on body composition and biochemical indices in female patients with obesity: a randomized controlled trial

Comparing the efficacy of thyroglobulin and thyroglobulin/ thyroid-stimulating hormone ratio models in predicting a successful response to radioactive iodine therapy

Thyroid function, glycemic control, and diabetic nephropathy in patients with type 2 diabetes over 24 months: prospective observational study

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials