Diabetes & Metabolism Journal

Original Articles

Complications
Glycemic Control and Retinal Microvascular Changes in Type 2 Diabetes Mellitus Patients without Clinical Retinopathy: Kangmin Lee, Ga Hye Lee, Seung Eun Lee, Jee Myung Yang, Kunho Bae; Received May 15, 2023 Accepted December 15, 2023 Published online March 13, 2024; DOI: https://doi.org/10.4093/dmj.2023.0149 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
To investigate the association of glycemic control and retinal microvascular changes in patients with type 2 diabetes mellitus (T2DM) without diabetic retinopathy (DR).
Methods
This retrospective, observational, cohort study included patients with T2DM without DR. The patients were categorized into intensive control (IC; mean glycosylated hemoglobin [HbA1c] ≤7.0%) and moderate control (MC; mean HbA1c >7.0%) groups. Optical coherence tomography (OCT) and swept-source OCT angiography (OCTA) image parameters were compared between three groups, including healthy controls.
Results
In total, 259 eyes of 259 participants (88 IC, 81 MC, and 90 controls) were included. The foveal avascular zone area was significantly larger in the MC group than IC and control groups (all P<0.05). The IC group had lower vessel density in the superficial retinal layer and deep retinal layer than the controls (all P<0.05). The choriocapillaris (CC) flow deficit (FD) was significantly greater in the MC group than in the IC and control groups (18.2%, 16.7%, and 14.2%, respectively; all P<0.01). In multivariate regression analysis, CC-FD was associated with the mean HbA1c level (P=0.008). There were no significant differences in OCT parameters among the groups.
Conclusion
OCTA revealed that early CC impairment is associated with HbA1c levels; the CC changes precede clinically apparent DR. The OCTA parameters differed among the groups according to the degree of glycemic control. Our results suggest that microvascular changes precede DR and are closely related to glycemic control.

Drug/Regimen
Risk of Diabetic Retinopathy between Sodium-Glucose Cotransporter-2 Inhibitors and Glucagon-Like Peptide-1 Receptor Agonists: Tzu-Yi Lin, Eugene Yu-Chuan Kang, Shih-Chieh Shao, Edward Chia-Cheng Lai, Sunir J. Garg, Kuan-Jen Chen, Je-Ho Kang, Wei-Chi Wu, Chi-Chun Lai, Yih-Shiou Hwang; Diabetes Metab J. 2023;47(3):394-404. Published online March 6, 2023; DOI: https://doi.org/10.4093/dmj.2022.0221

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Background
To compare risk of diabetic retinopathy (DR) between patients taking sodium-glucose cotransporter-2 inhibitors (SGLT2is) and those taking glucagon-like peptide-1 receptor agonists (GLP1-RAs) in routine care.
Methods
This retrospective cohort study emulating a target trial included patient data from the multi-institutional Chang Gung Research Database in Taiwan. Totally, 33,021 patients with type 2 diabetes mellitus using SGLT2is and GLP1-RAs between 2016 and 2019 were identified. 3,249 patients were excluded due to missing demographics, age <40 years, prior use of any study drug, a diagnosis of retinal disorders, a history of receiving vitreoretinal procedure, no baseline glycosylated hemoglobin, or no follow-up data. Baseline characteristics were balanced using inverse probability of treatment weighting with propensity scores. DR diagnoses and vitreoretinal interventions served as the primary outcomes. Occurrence of proliferative DR and DR receiving vitreoretinal interventions were regarded as vision-threatening DR.
Results
There were 21,491 SGLT2i and 1,887 GLP1-RA users included for the analysis. Patients receiving SGLT2is and GLP-1 RAs exhibited comparable rate of any DR (subdistribution hazard ratio [SHR], 0.90; 95% confidence interval [CI], 0.79 to 1.03), whereas the rate of proliferative DR (SHR, 0.53; 95% CI, 0.42 to 0.68) was significantly lower in the SGLT2i group. Also, SGLT2i users showed significantly reduced risk of composite surgical outcome (SHR, 0.58; 95% CI, 0.48 to 0.70).
Conclusion
Compared to those taking GLP1-RAs, patients receiving SGLT2is had a lower risk of proliferative DR and vitreoretinal interventions, although the rate of any DR was comparable between the SGLT2i and GLP1-RA groups. Thus, SGLT2is may be associated with a lower risk of vision-threatening DR but not DR development.

Citations

Citations to this article as recorded by

Incretin‐based drugs and the risk of diabetic retinopathy among individuals with type 2 diabetes: A systematic review and meta‐analysis of observational studies
Samuel Igweokpala, Naheemot Olaoluwa Sule, Antonios Douros, Oriana H. Y. Yu, Kristian B. Filion
Diabetes, Obesity and Metabolism.2024; 26(2): 721. CrossRef
Association of sodium–glucose cotransporter‐2 inhibitors and the risk of retinal vascular occlusion: A real‐world retrospective cohort study in Taiwan
Tzu‐Yi Lin, Eugene Yu‐Chuan Kang, Shih‐Chieh Shao, Edward Chia‐Cheng Lai, Nan‐Kai Wang, Sunir J. Garg, Kuan‐Jen Chen, Je‐Ho Kang, Wei‐Chi Wu, Chi‐Chun Lai, Yih‐Shiou Hwang
Diabetes/Metabolism Research and Reviews.2024;[Epub] CrossRef
Risk of rotator cuff tear and rotator cuff repair surgery comparison between sodium-glucose cotransporter 2 inhibitors and glucagon like peptide-1 receptor agonists: A real-world study
Yu-Chi Su, Pei-Chun Hsieh, Edward Chia-Cheng Lai, Yu-Ching Lin
Diabetes & Metabolism.2024; 50(2): 101522. CrossRef
Optimising renal risk parameters in type 2 diabetes mellitus: Perspectives from a retinal viewpoint
Sarita Jacob, George I. Varughese
Clinical Medicine.2024; 24(2): 100031. CrossRef
Risk of diabetic retinopathy and diabetic macular oedema with sodium–glucose cotransporter 2 inhibitors and glucagon-like peptide 1 receptor agonists in type 2 diabetes: a real-world data study from a global federated database
Aikaterini Eleftheriadou, David Riley, Sizheng S. Zhao, Philip Austin, Gema Hernández, Gregory Y. H. Lip, Timothy L. Jackson, John P. H. Wilding, Uazman Alam
Diabetologia.2024;[Epub] CrossRef
Impact of GLP-1 Agonists and SGLT-2 Inhibitors on Diabetic Retinopathy Progression: An Aggregated Electronic Health Record Data Study
Karen M. Wai, Kapil Mishra, Euna Koo, Cassie Ann Ludwig, Ravi Parikh, Prithvi Mruthyunjaya, Ehsan Rahimy
American Journal of Ophthalmology.2024;[Epub] CrossRef
Risk of Diabetic Retinopathy between Sodium-Glucose Cotransporter-2 Inhibitors and Glucagon-Like Peptide-1 Receptor Agonists (Diabetes Metab J 2023;47:394-404)
Tzu-Yi Lin, Eugene Yu-Chuan Kang, Shih-Chieh Shao, Edward Chia-Cheng Lai, Yih-Shiou Hwang
Diabetes & Metabolism Journal.2023; 47(4): 573. CrossRef
Risk of Diabetic Retinopathy between Sodium-Glucose Cotransporter-2 Inhibitors and Glucagon-Like Peptide-1 Receptor Agonists (Diabetes Metab J 2023;47:394-404)
Jihee Ko, Sun Joon Moon
Diabetes & Metabolism Journal.2023; 47(4): 571. CrossRef
Sodium-Glucose Cotransporter 2 Inhibitors and Risk of Retinopathy in Patients With Type 2 Diabetes
Fu-Shun Yen, James Cheng-Chung Wei, Teng-Shun Yu, Yu-Tung Hung, Chih-Cheng Hsu, Chii-Min Hwu
JAMA Network Open.2023; 6(12): e2348431. CrossRef

Complications
Fatty Acid-Binding Protein 4 in Patients with and without Diabetic Retinopathy: Ping Huang, Xiaoqin Zhao, Yi Sun, Xinlei Wang, Rong Ouyang, Yanqiu Jiang, Xiaoquan Zhang, Renyue Hu, Zhuqi Tang, Yunjuan Gu; Diabetes Metab J. 2022;46(4):640-649. Published online April 28, 2022; DOI: https://doi.org/10.4093/dmj.2021.0195

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Background
Fatty acid-binding protein 4 (FABP4) has been demonstrated to be a predictor of early diabetic nephropathy. However, little is known about the relationship between FABP4 and diabetic retinopathy (DR). This study explored the value of FABP4 as a biomarker of DR in patients with type 2 diabetes mellitus (T2DM).
Methods
A total of 238 subjects were enrolled, including 20 healthy controls and 218 T2DM patients. Serum FABP4 levels were measured using a sandwich enzyme-linked immunosorbent assay. The grade of DR was determined using fundus fluorescence angiography. Based on the international classification of DR, all T2DM patients were classified into the following three subgroups: non-DR group, non-proliferative diabetic retinopathy (NPDR) group, and proliferative diabetic retinopathy (PDR) group. Multivariate logistic regression analyses were employed to assess the correlation between FABP4 levels and DR severity.
Results
FABP4 correlated positively with DR severity (r=0.225, P=0.001). Receiver operating characteristic curve analysis was used to assess the diagnostic potential of FABP4 in identifying DR, with an area under the curve of 0.624 (37% sensitivity, 83.6% specificity) and an optimum cut-off value of 76.4 μg/L. Multivariate logistic regression model including FABP4 as a categorized binary variable using the cut-off value of 76.4 μg/L showed that the concentration of FABP4 above the cut-off value increased the risk of NPDR (odds ratio [OR], 3.231; 95% confidence interval [CI], 1.574 to 6.632; P=0.001) and PDR (OR, 3.689; 95% CI, 1.306 to 10.424; P=0.014).
Conclusion
FABP4 may be used as a serum biomarker for the diagnosis of DR.

Citations

Citations to this article as recorded by

Circulating AFABP, FGF21, and PEDF Levels as Prognostic Biomarkers of Sight-threatening Diabetic Retinopathy
Chi-Ho Lee, David Tak-Wai Lui, Chloe Yu-Yan Cheung, Carol Ho-Yi Fong, Michele Mae-Ann Yuen, Yu-Cho Woo, Wing-Sun Chow, Ian Yat-Hin Wong, Aimin Xu, Karen Siu-Ling Lam
The Journal of Clinical Endocrinology & Metabolism.2023; 108(9): e799. CrossRef
A Prediction Model for Sight-Threatening Diabetic Retinopathy Based on Plasma Adipokines among Patients with Mild Diabetic Retinopathy
Yaxin An, Bin Cao, Kun Li, Yongsong Xu, Wenying Zhao, Dong Zhao, Jing Ke, Takayuki Masaki
Journal of Diabetes Research.2023; 2023: 1. CrossRef

Complications
Prevalence of Diabetic Retinopathy in Undiagnosed Diabetic Patients: A Nationwide Population-Based Study: Han Na Jang, Min Kyong Moon, Bo Kyung Koo; Diabetes Metab J. 2022;46(4):620-629. Published online February 23, 2022; DOI: https://doi.org/10.4093/dmj.2021.0099

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Background
We investigated the prevalence of diabetic retinopathy (DR) in patients with undiagnosed diabetes through a nationwide survey, compared to those with known diabetes.
Methods
Among the participants of the Korean National Health and Nutrition Examination Surveys (KNHANES) from 2017 to 2018, individuals aged ≥40 years with diabetes and fundus exam results were enrolled. Sampling weights were applied to represent the entire Korean population. Newly detected diabetes patients through KNHANES were classified under “undiagnosed diabetes.”
Results
Among a total of 9,108 participants aged ≥40 years, 951 were selected for analysis. Of them, 31.3% (standard error, ±2.0%) were classified under “undiagnosed diabetes.” The prevalence of DR in patients with known and undiagnosed diabetes was 24.5%±2.0% and 10.7%±2.2%, respectively (P<0.001). The DR prevalence increased with rising glycosylated hemoglobin (HbA1c) levels in patients with known and undiagnosed diabetes (P for trend=0.001 in both). Among those with undiagnosed diabetes, the prevalence of DR was 6.9%±2.1%, 8.0%±3.4%, 5.6%±5.7%, 16.7%±9.4%, and 42.6%±14.8% for HbA1c levels of <7.0%, 7.0%–7.9%, 8.0%–8.9%, 9.0%–9.9%, and ≥10.0% respectively. There was no difference in the prevalence of hypertension, dyslipidemia, hypertriglyceridemia, or obesity according to the presence or absence of DR.
Conclusion
About one-third of patients with diabetes were unaware of their diabetes, and 10% of them have already developed DR. Considering increasing the prevalence of DR according to HbA1c level was found in patients with undiagnosed diabetes like those with known diabetes, screening and early detection of diabetes and DR are important.

Citations

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Risk factors of peripheral occlusive arterial disease in patients with diabetic retinopathy due to type 2 diabetes
Milos Maksimovic
Srpski arhiv za celokupno lekarstvo.2024; 152(1-2): 50. CrossRef
Gene Expression Analysis in T2DM and Its Associated Microvascular Diabetic Complications: Focus on Risk Factor and RAAS Pathway
Laxmipriya Jena, Prabhsimran Kaur, Tashvinder Singh, Kangan Sharma, Sushil Kotru, Anjana Munshi
Molecular Neurobiology.2024;[Epub] CrossRef
Novel Asian-Specific Visceral Adiposity Indices Are Associated with Chronic Kidney Disease in Korean Adults
Jonghwa Jin, Hyein Woo, Youngeun Jang, Won-Ki Lee, Jung-Guk Kim, In-Kyu Lee, Keun-Gyu Park, Yeon-Kyung Choi
Diabetes & Metabolism Journal.2023; 47(3): 426. CrossRef
Prevalence of osteosarcopenic obesity and related factors among Iranian older people: Bushehr Elderly Health (BEH) program
Mozhgan Ahmadinezhad, Mohammad Ali Mansournia, Noushin Fahimfar, Gita Shafiee, Iraj Nabipour, Mahnaz Sanjari, Kazem Khalagi, Mohammad Javad Mansourzadeh, Bagher Larijani, Afshin Ostovar
Archives of Osteoporosis.2023;[Epub] CrossRef

Type 1 Diabetes
Association between Metabolic Syndrome and Microvascular Complications in Chinese Adults with Type 1 Diabetes Mellitus: Qianwen Huang, Daizhi Yang, Hongrong Deng, Hua Liang, Xueying Zheng, Jinhua Yan, Wen Xu, Xiangwen Liu, Bin Yao, Sihui Luo, Jianping Weng; Diabetes Metab J. 2022;46(1):93-103. Published online August 31, 2021; DOI: https://doi.org/10.4093/dmj.2020.0240

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Background
Both type 1 diabetes mellitus (T1DM) and metabolic syndrome (MetS) are associated with an elevated risk of morbidity and mortality yet with increasing heterogeneity. This study primarily aimed to evaluate the prevalence of MetS among adult patients with T1DM in China and investigate its associated risk factors, and relationship with microvascular complications.
Methods
We included adult patients who had been enrolled in the Guangdong T1DM Translational Medicine Study conducted from June 2010 to June 2015. MetS was defined according to the updated National Cholesterol Education Program criterion. Logistic regression models were used to estimate the odds ratio (OR) for the association between MetS and the risk of diabetic kidney disease (DKD) and diabetic retinopathy (DR).
Results
Among the 569 eligible patients enrolled, the prevalence of MetS was 15.1%. While female gender, longer diabetes duration, higher body mass index, and glycosylated hemoglobin A1c (HbA1c) were risk factors associated with MetS (OR, 2.86, 1.04, 1.14, and 1.23, respectively), received nutrition therapy education was a protective factor (OR, 0.46). After adjustment for gender, age, diabetes duration, HbA1c, socioeconomic and lifestyle variables, MetS status was associated with an increased risk of DKD and DR (OR, 2.14 and 3.72, respectively; both P<0.05).
Conclusion
Although the prevalence of MetS in adult patients with T1DM in China was relatively low, patients with MetS were more likely to have DKD and DR. A comprehensive management including lifestyle modification might reduce their risk of microvascular complications in adults with T1DM.

Citations

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Prevalence of Metabolic Syndrome and Its Risk Factors Influence on Microvascular Complications in Patients With Type 1 and Type 2 Diabetes Mellitus
Asad Riaz, Shoaib Asghar, Salman Shahid, Haider Tanvir, Muhammad Hamza Ejaz, Mamuna Akram
Cureus.2024;[Epub] CrossRef
Simplified integration of optimal self-management behaviors is associated with improved HbA1c in patients with type 1 diabetes
C. Deng, Y. Xie, F. Liu, X. Tang, L. Fan, X. Yang, Y. Chen, Z. Zhou, X. Li
Journal of Endocrinological Investigation.2024;[Epub] CrossRef
Dynamic Changes in Metabolic Status Are Associated With Risk of Ocular Motor Cranial Nerve Palsies
Daye Diana Choi, Kyung-Ah Park, Kyungdo Han, Sei Yeul Oh
Journal of Neuro-Ophthalmology.2023;[Epub] CrossRef
Development and validation of an age-sex-ethnicity-specific metabolic syndrome score in the Chinese adults
Shujuan Yang, Bin Yu, Wanqi Yu, Shaoqing Dai, Chuanteng Feng, Ying Shao, Xing Zhao, Xiaoqing Li, Tianjing He, Peng Jia
Nature Communications.2023;[Epub] CrossRef
Association of Endotoxemia with Low-Grade Inflammation, Metabolic Syndrome and Distinct Response to Lipopolysaccharide in Type 1 Diabetes
Aleksejs Fedulovs, Leonora Pahirko, Kaspars Jekabsons, Liga Kunrade, Jānis Valeinis, Una Riekstina, Valdis Pīrāgs, Jelizaveta Sokolovska
Biomedicines.2023; 11(12): 3269. CrossRef
Association between Metabolic Syndrome and Microvascular Complications in Chinese Adults with Type 1 Diabetes Mellitus (Diabetes Metab J 2022;46:93-103)
Qianwen Huang, Sihui Luo
Diabetes & Metabolism Journal.2022; 46(3): 515. CrossRef
Association between Metabolic Syndrome and Microvascular Complications in Chinese Adults with Type 1 Diabetes Mellitus (Diabetes Metab J 2022;46:93-103)
Gyuri Kim
Diabetes & Metabolism Journal.2022; 46(3): 512. CrossRef
Metabolic syndrome associated with higher glycemic variability in type 1 diabetes: A multicenter cross-sectional study in china
Keyu Guo, Liyin Zhang, Jianan Ye, Xiaohong Niu, Hongwei Jiang, Shenglian Gan, Jian Zhou, Lin Yang, Zhiguang Zhou
Frontiers in Endocrinology.2022;[Epub] CrossRef

Brief Report

Complications
Diabetic Retinopathy and Related Clinical Practice for People with Diabetes in Korea: A 10-Year Trend Analysis: Yoo-Ri Chung, Kyoung Hwa Ha, Kihwang Lee, Dae Jung Kim; Diabetes Metab J. 2020;44(6):928-932. Published online July 10, 2020; DOI: https://doi.org/10.4093/dmj.2020.0096

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We performed a retrospective cohort study including people diagnosed with diabetes from 2006 to 2015 according to the Korean National Health Insurance Service-National Sample Cohort database, to analyze the changes in the prevalence, screening rate, and treatment patterns for diabetic retinopathy (DR) over 10 years. The proportion of people who underwent fundus screening for DR steadily increased over the past decade. The prevalence of DR increased from 13.4% in 2006 to 15.9% in 2015, while that of proliferative DR steadily decreased from 1.29% in 2006 to 1.16% in 2015. The proportion of patients undergoing retinal photocoagulation constantly decreased. The prevalence of DR increased over the past decade, while its severity seemed to have improved, with a decreased rate of proliferative DR and retinal photocoagulation. A higher proportion of patients underwent ophthalmic screening using fundus examination, but still less than 30% of patients with diabetes underwent comprehensive examination in 2015.

Citations

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Variations in Electronic Health Record-Based Definitions of Diabetic Retinopathy Cohorts
Jimmy S. Chen, Ivan A. Copado, Cecilia Vallejos, Fritz Gerald P. Kalaw, Priyanka Soe, Cindy X. Cai, Brian C. Toy, Durga Borkar, Catherine Q. Sun, Jessica G. Shantha, Sally L. Baxter
Ophthalmology Science.2024; 4(4): 100468. CrossRef
Present and future screening programs for diabetic retinopathy: a narrative review
Andreas Abou Taha, Sebastian Dinesen, Anna Stage Vergmann, Jakob Grauslund
International Journal of Retina and Vitreous.2024;[Epub] CrossRef
Chronic disease management program applied to type 2 diabetes patients and prevention of diabetic complications: a retrospective cohort study using nationwide data
Min Kyung Hyun, Jang Won Lee, Seung-Hyun Ko
BMC Public Health.2023;[Epub] CrossRef
Visual Acuity Outcomes in Diseases Associated with Reduced Visual Acuity: An Analysis of the National Health Insurance Service Database in Korea
Sang-Yeob Kim, Byeong-Yeon Moon, Hyun-Gug Cho, Dong-Sik Yu
International Journal of Environmental Research and Public Health.2022; 19(14): 8689. CrossRef
Prevalence of Diabetic Retinopathy in Undiagnosed Diabetic Patients: A Nationwide Population-Based Study
Han Na Jang, Min Kyong Moon, Bo Kyung Koo
Diabetes & Metabolism Journal.2022; 46(4): 620. CrossRef
Prevalence and Risk Factors of Diabetic Retinopathy in Diabetes People using Korean National Health and Nutrition Examination Survey VII
Ihn Sook Jeong, Chan Mi Kang
Journal of Korean Academy of Community Health Nursing.2022; 33(4): 408. CrossRef
Time to Reach Target Glycosylated Hemoglobin Is Associated with Long-Term Durable Glycemic Control and Risk of Diabetic Complications in Patients with Newly Diagnosed Type 2 Diabetes Mellitus: A 6-Year Observational Study (Diabetes Metab J 2021;45:368-78)
Ja Young Jeon
Diabetes & Metabolism Journal.2021; 45(4): 613. CrossRef

Original Article

Complications
Dipeptidyl Peptidase-4 Inhibitors versus Other Antidiabetic Drugs Added to Metformin Monotherapy in Diabetic Retinopathy Progression: A Real World-Based Cohort Study: Yoo-Ri Chung, Kyoung Hwa Ha, Hyeon Chang Kim, Sang Jun Park, Kihwang Lee, Dae Jung Kim; Diabetes Metab J. 2019;43(5):640-648. Published online February 20, 2019; DOI: https://doi.org/10.4093/dmj.2018.0137

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Background

To investigate the effects of dipeptidyl peptidase-4 inhibitor (DPP4i) as add-on medications to metformin on progression of diabetic retinopathy (DR) in patients with type 2 diabetes mellitus, compared with sulfonylurea (SU) or thiazolidinedione (TZD).

Methods

We identified 4,447 patients with DPP4i, 6,136 with SU, and 617 with TZD in addition to metformin therapy from the database of Korean National Health Insurance Service between January 2013 and December 2015. Cox proportional hazards regression models were used to calculate hazard ratios (HRs) for DR progression. The progression of DR was defined by the procedure code of panretinal photocoagulation, intravitreal injection or vitrectomy; or the addition of diagnostic code of vitreous hemorrhage, retinal detachment, or neovascular glaucoma.

Results

The age and sex-adjusted HR of DR progression was 0.74 for DPP4i add-on group compared with SU add-on group (95% confidence interval [CI], 0.62 to 0.89). This lower risk of DR progression remained significant after additional adjustments for comorbidities, duration of metformin therapy, intravitreal injections and calendar index year (HR, 0.80; 95% CI, 0.66 to 0.97).

Conclusion

This population-based cohort study showed that the use of DPP4i as add-on therapy to metformin did not increase the risk of DR progression compared to SU.

Citations

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Effects of newer-generation anti-diabetics on diabetic retinopathy: a critical review
Dimitrios P. Ntentakis, Victor San Martin Carvalho Correa, Anastasia Maria Ntentaki, Eleni Delavogia, Toshio Narimatsu, Nikolaos E. Efstathiou, Demetrios G. Vavvas
Graefe's Archive for Clinical and Experimental Ophthalmology.2024; 262(3): 717. CrossRef
Incretin‐based drugs and the risk of diabetic retinopathy among individuals with type 2 diabetes: A systematic review and meta‐analysis of observational studies
Samuel Igweokpala, Naheemot Olaoluwa Sule, Antonios Douros, Oriana H. Y. Yu, Kristian B. Filion
Diabetes, Obesity and Metabolism.2024; 26(2): 721. CrossRef
Weight loss, bariatric surgery, and novel antidiabetic drugs effects on diabetic retinopathy: a review
Alejandro M. Perez, Emily Neag, Jayanth Sridhar, Basil K. Williams
Current Opinion in Ophthalmology.2024; 35(3): 192. CrossRef
Role of Systemic Factors in Improving the Prognosis of Diabetic Retinal Disease and Predicting Response to Diabetic Retinopathy Treatment
Joe Mellor, Anita Jeyam, Joline W.J. Beulens, Sanjeeb Bhandari, Geoffrey Broadhead, Emily Chew, Ward Fickweiler, Amber van der Heijden, Daniel Gordin, Rafael Simó, Janet Snell-Bergeon, Anniina Tynjälä, Helen Colhoun
Ophthalmology Science.2024; 4(4): 100494. CrossRef
Novel Antidiabetic Drugs and the Risk of Diabetic Retinopathy: A Systematic Review and Meta-Analysis of Randomized Controlled Trials
Artur Małyszczak, Joanna Przeździecka-Dołyk, Urszula Szydełko-Paśko, Marta Misiuk-Hojło
Journal of Clinical Medicine.2024; 13(6): 1797. CrossRef
Prognostic factors for the development and progression of proliferative diabetic retinopathy in people with diabetic retinopathy
Jennifer Perais, Ridhi Agarwal, Jennifer R Evans, Emma Loveman, Jill L Colquitt, David Owens, Ruth E Hogg, John G Lawrenson, Yemisi Takwoingi, Noemi Lois
Cochrane Database of Systematic Reviews.2023;[Epub] CrossRef
Rapid Reduction of HbA1c and Early Worsening of Diabetic Retinopathy: A Real-world Population-Based Study in Subjects With Type 2 Diabetes
Rafael Simó, Josep Franch-Nadal, Bogdan Vlacho, Jordi Real, Ester Amado, Juana Flores, Manel Mata-Cases, Emilio Ortega, Mercedes Rigla, Joan-Anton Vallés, Cristina Hernández, Didac Mauricio
Diabetes Care.2023; 46(9): 1633. CrossRef
Minimum Effective Dose of DPP-4 Inhibitors for Treating Early Stages of Diabetic Retinopathy in an Experimental Model
Patricia Bogdanov, Hugo Ramos, Marta Valeri, Anna Deàs-Just, Jordi Huerta, Rafael Simó, Cristina Hernández
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Glucagon-Like Peptide 1 Receptor Agonists – Potential Game Changers in the Treatment of Glaucoma?
Zaynab Ahmad Mouhammad, Rupali Vohra, Anna Horwitz, Anna-Sophie Thein, Jens Rovelt, Barbara Cvenkel, Pete A. Williams, Augusto Azuara-Blanco, Miriam Kolko
Frontiers in Neuroscience.2022;[Epub] CrossRef
Transcriptomic Analysis Reveals That Retinal Neuromodulation Is a Relevant Mechanism in the Neuroprotective Effect of Sitagliptin in an Experimental Model of Diabetic Retinopathy
Hugo Ramos, Patricia Bogdanov, Rafael Simó, Anna Deàs-Just, Cristina Hernández
International Journal of Molecular Sciences.2022; 24(1): 571. CrossRef
The Safety of Pharmacological and Surgical Treatment of Diabetes in Patients with Diabetic Retinopathy—A Review
Wojciech Matuszewski, Angelika Baranowska-Jurkun, Magdalena Maria Stefanowicz-Rutkowska, Katarzyna Gontarz-Nowak, Ewa Gątarska, Elżbieta Bandurska-Stankiewicz
Journal of Clinical Medicine.2021; 10(4): 705. CrossRef
Effects of Fibrates on Risk of Development of Diabetic Retinopathy in Japanese Working Age Patients with Type 2 Diabetes and Dyslipidemia: a Retrospective Cohort Study
Hayato Akimoto, Yasuo Takahashi, Satoshi Asai
YAKUGAKU ZASSHI.2021; 141(5): 761. CrossRef
Association between Add-On Dipeptidyl Peptidase-4 Inhibitor Therapy and Diabetic Retinopathy Progression
Eugene Yu-Chuan Kang, Chunya Kang, Wei-Chi Wu, Chi-Chin Sun, Kuan-Jen Chen, Chi-Chun Lai, Tien-Hsing Chen, Yih-Shiou Hwang
Journal of Clinical Medicine.2021; 10(13): 2871. CrossRef
Understanding molecular upsets in diabetic nephropathy to identify novel targets and treatment opportunities
Nidhi Raval, Akshant Kumawat, Dnyaneshwar Kalyane, Kiran Kalia, Rakesh K. Tekade
Drug Discovery Today.2020; 25(5): 862. CrossRef
Letter: Dipeptidyl Peptidase-4 Inhibitors versus Other Antidiabetic Drugs Added to Metformin Monotherapy in Diabetic Retinopathy Progression: A Real World-Based Cohort Study (Diabetes Metab J 2019;43:640–8)
Jun Sung Moon
Diabetes & Metabolism Journal.2019; 43(6): 911. CrossRef
Response: Dipeptidyl Peptidase-4 Inhibitors versus Other Antidiabetic Drugs Added to Metformin Monotherapy in Diabetic Retinopathy Progression: A Real World-Based Cohort Study (Diabetes Metab J 2019;43:640–8)
Yoo-Ri Chung, Kyoung Hwa Ha, Kihwang Lee, Dae Jung Kim
Diabetes & Metabolism Journal.2019; 43(6): 917. CrossRef

Review

Complications
Pathophysiology of Diabetic Retinopathy: The Old and the New: Sentaro Kusuhara, Yoko Fukushima, Shuntaro Ogura, Naomi Inoue, Akiyoshi Uemura; Diabetes Metab J. 2018;42(5):364-376. Published online October 22, 2018; DOI: https://doi.org/10.4093/dmj.2018.0182

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Abstract PDF PubReader

Vision loss in diabetic retinopathy (DR) is ascribed primarily to retinal vascular abnormalities—including hyperpermeability, hypoperfusion, and neoangiogenesis—that eventually lead to anatomical and functional alterations in retinal neurons and glial cells. Recent advances in retinal imaging systems using optical coherence tomography technologies and pharmacological treatments using anti-vascular endothelial growth factor drugs and corticosteroids have revolutionized the clinical management of DR. However, the cellular and molecular mechanisms underlying the pathophysiology of DR are not fully determined, largely because hyperglycemic animal models only reproduce limited aspects of subclinical and early DR. Conversely, non-diabetic mouse models that represent the hallmark vascular disorders in DR, such as pericyte deficiency and retinal ischemia, have provided clues toward an understanding of the sequential events that are responsible for vision-impairing conditions. In this review, we summarize the clinical manifestations and treatment modalities of DR, discuss current and emerging concepts with regard to the pathophysiology of DR, and introduce perspectives on the development of new drugs, emphasizing the breakdown of the blood-retina barrier and retinal neovascularization.

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Short Communication

Complications
The Prevalence and Risk Factors for Diabetic Retinopathy in Shiraz, Southern Iran: Haleh Ghaem, Nima Daneshi, Shirin Riahi, Mostafa Dianatinasab; Diabetes Metab J. 2018;42(6):538-543. Published online August 9, 2018; DOI: https://doi.org/10.4093/dmj.2018.0047

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Globally, diabetic retinopathy (DR) is one of the leading causes of blindness, that diminishes quality of life. This study aimed to describe the prevalence of DR, and its associated risk factors. This cross-sectional study was carried out among 478 diabetic patients in a referral center in Fars province, Iran. The mean±standard deviation age of the participants was 56.64±12.45 years old and DR prevalence was 32.8%. In multivariable analysis, lower education levels (adjusted odds ratio [aOR], 0.43; 95% confidence interval [CI], 0.24 to 0.76), being overweight (aOR, 1.70; 95% CI, 1.02 to 2.83) or obese (aOR, 1.88; 95% CI, 1.09 to 3.26), diabetes duration of 10 to 20 years (aOR, 2.35; 95% CI, 1.48 to 3.73) and over 20 years (aOR, 5.63; 95% CI, 2.97 to 10.68), receiving insulin (aOR, 1.99; 95% CI, 1.27 to 3.10), and having chronic diseases (aOR, 1.71; 95% CI, 1.02 to 2.85) were significantly associated with DR. In conclusion, longer diabetes duration and obesity or having chronic diseases are strongly associated with DR suggesting that control of these risk factors may reduce both the prevalence and impact of retinopathy in Iran.

Citations

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Preserving sight: Managing and preventing diabetic retinopathy
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Original Article

Complications
The Association between Pancreatic Steatosis and Diabetic Retinopathy in Type 2 Diabetes Mellitus Patients: Jee Sun Jeong, Mee Kyung Kim, Kyung Do Han, Oak Kee Hong, Ki-Hyun Baek, Ki-Ho Song, Dong Jin Chung, Jung-Min Lee, Hyuk-Sang Kwon; Diabetes Metab J. 2018;42(5):425-432. Published online August 9, 2018; DOI: https://doi.org/10.4093/dmj.2017.0107

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Background

Whether pancreatic steatosis has a local or systemic effect, like ectopic fat of other major organs, remains unknown. Data on the influence of pancreatic steatosis on microvascular complication are rare. Therefore, we investigated the relationship between pancreatic steatosis and diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM).

Methods

The attenuation of three pancreatic regions (head, body, and tail) and the spleen (S) in 186 patients with T2DM was measured using non-enhanced computed tomography imaging. We used three parameters for the assessment of pancreatic steatosis (‘P’ mean: mean attenuation of three pancreatic regions; P–S: difference between ‘P’ mean and ‘S’; P/S: the ‘P’ mean to ‘S’ ratio). The presence of DR was assessed by an expert ophthalmologist using dilated fundoscopy.

Results

The average P mean was 29.02 Hounsfield units (HU), P–S was −18.20 HU, and P/S was 0.61. The three pancreatic steatosis parameters were significantly associated with the prevalence of DR in non-obese T2DM patients. In the non-obese group, the odds ratios of P mean, P–S, and P/S for the prevalence of DR, after adjustment for age, sex, and glycosylated hemoglobin level, were 2.449 (P=0.07), 2.639 (P=0.04), and 2.043 (P=0.02), respectively.

Conclusion

In this study, pancreatic steatosis was significantly associated with DR in non-obese patients with T2DM. Further studies are necessary to clarify the causal relationship between pancreatic steatosis and the development of DR.

Citations

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Intra‐pancreatic fat is associated with continuous glucose monitoring metrics
Yutong Liu, Wandia Kimita, Xiatiguli Shamaitijiang, Loren Skudder‐Hill, Ivana R. Sequeira‐Bisson, Maxim S. Petrov
Diabetes, Obesity and Metabolism.2024;[Epub] CrossRef
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Jianliang Wang, Qingyun Cai, Xiaojuan Wu, Jiaxuan Wang, Xiaona Chang, Xiaoyu Ding, Jia Liu, Guang Wang, Muhittin Yurekli
International Journal of Endocrinology.2023; 2023: 1. CrossRef
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Bedriye Koyuncu Sokmen, Tolga Sahin, Alihan Oral, Erdem Kocak, Nagihan Inan
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Pengtao Sun, Chunzhi Fan, Rengui Wang, Tongwei Chu, Xiaoli Sun, Dongxue Zhang, Xuechao Du
Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy.2021; Volume 14: 1329. CrossRef

Review

Clinical Diabetes & Therapeutics
Past and Current Status of Adult Type 2 Diabetes Mellitus Management in Korea: A National Health Insurance Service Database Analysis: Seung-Hyun Ko, Kyungdo Han, Yong-ho Lee, Junghyun Noh, Cheol-Young Park, Dae-Jung Kim, Chang Hee Jung, Ki-Up Lee, Kyung-Soo Ko; Diabetes Metab J. 2018;42(2):93-100. Published online April 19, 2018; DOI: https://doi.org/10.4093/dmj.2018.42.2.93

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Korea's National Healthcare Program, the National Health Insurance Service (NHIS), a government-affiliated agency under the Korean Ministry of Health and Welfare, covers the entire Korean population. The NHIS supervises all medical services in Korea and establishes a systematic National Health Information database (DB). A health information DB system including all of the claims, medications, death information, and health check-ups, both in the general population and in patients with various diseases, is not common worldwide. On June 9, 2014, the NHIS signed a memorandum of understanding with the Korean Diabetes Association (KDA) to provide limited open access to its DB. By October 31, 2017, seven papers had been published through this collaborative research project. These studies were conducted to investigate the past and current status of type 2 diabetes mellitus and its complications and management in Korea. This review is a brief summary of the collaborative projects between the KDA and the NHIS over the last 3 years. According to the analysis, the national health check-up DB or claim DB were used, and the age category or study period were differentially applied.

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Original Articles

Complications
Features of Long-Standing Korean Type 2 Diabetes Mellitus Patients with Diabetic Retinopathy: A Study Based on Standardized Clinical Data: Sejeong Park, Sang Youl Rhee, Su Jin Jeong, Kiyoung Kim, Suk Chon, Seung-Young Yu, Jeong-Taek Woo; Diabetes Metab J. 2017;41(5):393-404. Published online September 5, 2017; DOI: https://doi.org/10.4093/dmj.2017.41.5.393

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Abstract PDF PubReader

Background

This is part of a prospective study carried out as a national project to secure standardized public resources for type 2 diabetes mellitus (T2DM) patients in Korea. We compared various characteristics of long-standing T2DM patients with diabetic retinopathy (DR) and macular edema (ME).

Methods

From September 2014 to July 2015, T2DM patients with disease duration of at least 15 years were recruited at a single university hospital. Clinical data and samples were collected according to the common data elements and standards of procedure developed by the Korean Diabetes Association Research Council. Each participant was assessed by ophthalmologists for DR and ME.

Results

Among 220 registered patients, 183 completed the ophthalmologic assessment. DR was associated with longer disease duration (odds ratio [OR], 1.071; 95% confidence interval [CI], 1.001 to 1.147 for non-proliferative diabetic retinopathy [NPDR]) (OR, 1.142; 95% CI, 1.051 to 1.242 for proliferative diabetic retinopathy [PDR]) and the use of long-acting insulin (OR, 4.559; 95% CI, 1.672 to 12.427 for NPDR) (OR, 4.783; 95% CI, 1.581 to 14.474 for PDR), but a lower prevalence of a family history of cancer (OR, 0.310; 95% CI, 0.119 to 0.809 for NPDR) (OR, 0.206; 95% CI, 0.063 to 0.673 for PDR). ME was associated with higher glycosylated hemoglobin levels (OR, 1.380; 95% CI, 1.032 to 1.845) and the use of rapid-acting insulin (OR, 5.211; 95% CI, 1.445 to 18.794).

Conclusion

Various clinical features were associated with DR and ME. Additional epidemiological and biorepository-based studies using this cohort are being conducted to deepen our understanding of diabetic complications in Korea.

Citations

Citations to this article as recorded by

Diabetic retinopathy related homeostatic dysregulation and its association with mortality among diabetes patients: A cohort study from NHANES
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Diabetes Research and Clinical Practice.2024; 207: 111081. CrossRef
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Jun Sung Moon
Diabetes & Metabolism Journal.2019; 43(6): 911. CrossRef
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Diabetes & Metabolism Journal.2018; 42(2): 93. CrossRef
Letter: Features of Long-Standing Korean Type 2 Diabetes Mellitus Patients with Diabetic Retinopathy: A Study Based on Standardized Clinical Data (Diabetes Metab J 2017;41:393-404)
Jae-Seung Yun
Diabetes & Metabolism Journal.2017; 41(6): 492. CrossRef
Response: Features of Long-Standing Korean Type 2 Diabetes Mellitus Patients with Diabetic Retinopathy: A Study Based on Standardized Clinical Data (Diabetes Metab J 2017;41:393-404)
Sang Youl Rhee, Jeong-Taek Woo
Diabetes & Metabolism Journal.2017; 41(6): 494. CrossRef

Complications
Clinical Course and Risk Factors of Diabetic Retinopathy in Patients with Type 2 Diabetes Mellitus in Korea: Jae-Seung Yun, Tae-Seok Lim, Seon-Ah Cha, Yu-Bae Ahn, Ki-Ho Song, Jin A Choi, Jinwoo Kwon, Donghyun Jee, Yang Kyung Cho, Yong-Moon Park, Seung-Hyun Ko; Diabetes Metab J. 2016;40(6):482-493. Published online October 5, 2016; DOI: https://doi.org/10.4093/dmj.2016.40.6.482

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63 Download
30 Web of Science
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Abstract PDF Supplementary Material PubReader

Background

We investigated clinical course and risk factors for diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM).

Methods

A total of 759 patients with T2DM without DR were included from January 2001 to December 2004. Retinopathy evaluation was performed at least annually by ophthalmologists. The severity of the DR was classified into five categories according to the International Clinical Diabetic Retinopathy Severity Scales.

Results

Of the 759 patients, 523 patients (68.9%) completed the follow-up evaluation. During the follow-up period, 235 patients (44.9%) developed DR, and 32 patients (13.6%) progressed to severe nonproliferative DR (NPDR) or proliferative DR (PDR). The mean duration of diabetes at the first diagnosis of mild NPDR, moderate NPDR, and severe NPDR or PDR were 14.8, 16.7, and 17.3 years, respectively. After adjusting multiple confounding factors, the significant risk factors for the incidence of DR risk in patients with T2DM were old age, longer duration of diabetes, higher mean glycosylated hemoglobin (HbA1c), and albuminuria. Even in the patients who had been diagnosed with diabetes for longer than 10 years at baseline, a decrease in HbA1c led to a significant reduction in the risk of developing DR (hazard ratio, 0.73 per 1% HbA1c decrement; 95% confidence interval, 0.58 to 0.91; P=0.005).

Conclusion

This prospective cohort study demonstrates that glycemic control, diabetes duration, age, and albuminuria are important risk factors for the development of DR. More aggressive retinal screening for T2DM patients diagnosed with DR should be required in order to not miss rapid progression of DR.

Citations

Citations to this article as recorded by

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Review

Complications
The Effect of Bariatric Surgery on Diabetic Retinopathy: Good, Bad, or Both?: Dora M. Gorman, Carel W. le Roux, Neil G. Docherty; Diabetes Metab J. 2016;40(5):354-364. Published online September 27, 2016; DOI: https://doi.org/10.4093/dmj.2016.40.5.354

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Bariatric surgery, initially intended as a weight-loss procedure, is superior to standard lifestyle intervention and pharmacological therapy for type 2 diabetes in obese individuals. Intensive medical management of hyperglycemia is associated with improved microvascular outcomes. Whether or not the reduction in hyperglycemia observed after bariatric surgery translates to improved microvascular outcomes is yet to be determined. There is substantial heterogeneity in the data relating to the impact of bariatric surgery on diabetic retinopathy (DR), the most common microvascular complication of diabetes. This review aims to collate the recent data on retinal outcomes after bariatric surgery. This comprehensive evaluation revealed that the majority of DR cases remain stable after surgery. However, risk of progression of pre-existing DR and the development of new DR is not eliminated by surgery. Instances of regression of DR are also noted. Potential risk factors for deterioration include severity of DR at the time of surgery and the magnitude of glycated hemoglobin reduction. Concerns also exist over the detrimental effects of postprandial hypoglycemia after surgery. In vivo studies evaluating the chronology of DR development and the impact of bariatric surgery could provide clarity on the situation. For now, however, the effect of bariatric surgery on DR remains inconclusive.

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Original Article

Complications
Risk Factors for the Development and Progression of Diabetic Kidney Disease in Patients with Type 2 Diabetes Mellitus and Advanced Diabetic Retinopathy: Kyung-Jin Yun, Hye Ji Kim, Mee Kyoung Kim, Hyuk-Sang Kwon, Ki-Hyun Baek, Young Jung Roh, Ki-Ho Song; Diabetes Metab J. 2016;40(6):473-481. Published online September 20, 2016; DOI: https://doi.org/10.4093/dmj.2016.40.6.473

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Background

Some patients with type 2 diabetes mellitus (T2DM) do not develop diabetic kidney disease (DKD) despite the presence of advanced diabetic retinopathy (DR). We aimed to investigate the presence of DKD and its risk factors in patients with T2DM and advanced DR.

Methods

We conducted a cross-sectional study in 317 patients with T2DM and advanced DR. The phenotypes of DKD were divided into three groups according to the urine albumin/creatinine ratio (uACR, mg/g) and estimated glomerular filtration rate (eGFR, mL/min/1.73 m²): no DKD (uACR <30 and eGFR ≥60), non-severe DKD (uACR ≥30 or eGFR <60), and severe DKD (uACR ≥30 and eGFR <60). Mean systolic and diastolic blood pressure, mean glycosylated hemoglobin (HbA1c) level, and HbA1c variability (standard deviation [SD] of serial HbA1c values or HbA1c-SD) were calculated for the preceding 2 years.

Results

The prevalence of no DKD, non-severe DKD, and severe DKD was 37.2% (n=118), 37.0% (n=117), and 25.8% (n=82), respectively. HbA1c-SD and the triglyceride/high density lipoprotein cholesterol (TG/HDL-C) ratio correlated positively with uACR and negatively with eGFR. Multiple linear regression analyses showed that the HbA1c-SD and TG/HDL-C ratio were significantly related with eGFR. Multiple logistic regression analyses after adjusting for several risk factors showed that HbA1c-SD and the TG/HDL-C ratio were significant risk factors for severe DKD.

Conclusion

The prevalence of DKD was about 60% in patients with T2DM and advanced DR. HbA1c variability and TG/HDL-C ratio may affect the development and progression of DKD in these patients.

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