Diabetes & Metabolism Journal

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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Author response to: remission of diabetes mellitus after bariatric surgery: the putative link with worsening diabetic retinopathy and a need for ongoing postoperative follow-up retinal screening
Karl Hage, Omar M. Ghanem
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Ariana Allen, Hemal Patel, Sandra S. Stinnett, Jullia A. Rosdahl, Stefanie Schuman
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S. Feldman-Billard
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The Long-Term Effects of Bariatric Surgery on Type 2 Diabetes Remission, Microvascular and Macrovascular Complications, and Mortality: a Systematic Review and Meta-Analysis
Binwu Sheng, Khoa Truong, Hugh Spitler, Lu Zhang, Xuetao Tong, Liwei Chen
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Current Diabetes Reports.2017;[Epub] CrossRef
The role of bariatric surgery to treat diabetes: current challenges and perspectives
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BMC Endocrine Disorders.2017;[Epub] CrossRef

Original Articles

Correlations between Glucagon Stimulated C-peptide Levels and Microvascular Complications in Type 2 Diabetes Patients: Hye-Jin Yoon, Youn-Zoo Cho, Ji-young Kim, Byung-Joon Kim, Keun-Young Park, Gwan-Pyo Koh, Dae-Ho Lee, Dong-Mee Lim; Diabetes Metab J. 2012;36(5):379-387. Published online October 18, 2012; DOI: https://doi.org/10.4093/dmj.2012.36.5.379

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Abstract PDF PubReader

Background

This study aimed to investigate whether stimulated C-peptide is associated with microvascular complications in type 2 diabetes mellitus (DM).

Methods

A cross-sectional study was conducted in 192 type 2 diabetic patients. Plasma basal C-peptide and stimulated C-peptide were measured before and 6 minutes after intravenous injection of 1 mg glucagon. The relationship between C-peptide and microvascular complications was statistically analyzed.

Results

In patients with retinopathy, basal C-peptide was 1.9±1.2 ng/mL, and stimulated C-peptide was 2.7±1.6 ng/mL; values were significantly lower compared with patients without retinopathy (P=0.031 and P=0.002, respectively). In patients with nephropathy, basal C-peptide was 1.6±0.9 ng/mL, and stimulated C-peptide was 2.8±1.6 ng/mL; values were significantly lower than those recorded in patients without nephropathy (P=0.020 and P=0.026, respectively). Stimulated C-peptide level was associated with increased prevalence of microvascular complications. Age-, DM duration-, and hemoglobin A1c-adjusted odds ratios for retinopathy in stimulated C-peptide value were 4.18 (95% confidence interval [CI], 1.40 to 12.51) and 3.35 (95% CI, 1.09 to 10.25), respectively. The multiple regression analysis between nephropathy and C-peptide showed that stimulated C-peptide was statistically correlated with nephropathy (P=0.03).

Conclusion

In patients with type 2 diabetes, the glucagon stimulation test was a relatively simple method of short duration for stimulating C-peptide response. Stimulated C-peptide values were associated with microvascular complications to a greater extent than basal C-peptides.

Citations

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A Nomogram for Predicting Vision-Threatening Diabetic Retinopathy Among Mild Diabetic Retinopathy Patients: A Case–Control and Prospective Study of Type 2 Diabetes
Jing Ke, Kun Li, Bin Cao
Diabetes, Metabolic Syndrome and Obesity.2023; Volume 16: 275. CrossRef
The average 30-minute post-prandial C-peptide predicted diabetic retinopathy progress: a retro-prospective study
Ting Pan, Jie Gao, Xinghua Cai, Huihui Zhang, Jun Lu, Tao Lei
BMC Endocrine Disorders.2023;[Epub] CrossRef
Dysregulation of miR-374a is involved in the progression of diabetic retinopathy and regulates the proliferation and migration of retinal microvascular endothelial cells
Zhanhong Wang, Xiao Zhang, Yanjun Wang, Dailing Xiao
Clinical and Experimental Optometry.2022; 105(3): 287. CrossRef
The Relationship between the Lipid Accumulation Product and Beta-cell Function in Korean Adults with or without Type 2 Diabetes Mellitus: The 2015 Korea National Health and Nutrition Examination Survey
Hye Eun Cho, Seung Bum Yang, Mi Young Gi, Ju Ae Cha, so Young Park, Hyun Yoon
Endocrine Research.2022; 47(2): 80. CrossRef
Effects of Serum C-Peptide Level on Blood Lipid and Cardiovascular and Cerebrovascular Injury in Patients with Type 2 Diabetes Mellitus: A Meta-Analysis
Juan Qin, Rongli Sun, Ding Ding, Yuvaraja Teekaraman
Contrast Media & Molecular Imaging.2022; 2022: 1. CrossRef
Investigation of Diabetes Complication Risk Perception and Diabetes Self-Management Skills in Individuals with Diabetes
Mehmet AYTEMUR, Bahar İNKAYA
Turkish Journal of Diabetes and Obesity.2022; 6(2): 121. CrossRef
Diabetic Retinopathy and Insulin Insufficiency: Beta Cell Replacement as a Strategy to Prevent Blindness
Eli Ipp
Frontiers in Endocrinology.2021;[Epub] CrossRef
Association of C-peptide with diabetic vascular complications in type 2 diabetes
Y. Wang, H. Wan, Y. Chen, F. Xia, W. Zhang, C. Wang, S. Fang, K. Zhang, Q. Li, N. Wang, Y. Lu
Diabetes & Metabolism.2020; 46(1): 33. CrossRef
Variations in glucose/C-peptide ratio in patients with type 2 diabetes associated with renal function
John A. D'Elia, Christopher Mulla, Jiankang Liu, Larry A. Weinrauch
Diabetes Research and Clinical Practice.2019; 150: 1. CrossRef
The pharmacokinetics of porcine C‐peptide after intraperitoneal injection
Naho Iizuka, Masuhiro Nishimura, Yasutaka Fujita, Osamu Sawamoto, Shinichi Matsumoto
Xenotransplantation.2019;[Epub] CrossRef
Association of KCNJ11(RS5219) gene polymorphism with biochemical markers of glycemic status and insulin resistance in gestational diabetes mellitus
Lenin M, Ramesh Ramasamy, Sweta Kulkarani, Seetesh Ghose, Srinivasan A.R.S., Sathish Babu M
Meta Gene.2018; 16: 134. CrossRef
Glucagon secretion is increased in patients with Type 2 diabetic nephropathy
Xiaoyu Wang, Juhong Yang, Baocheng Chang, Chunyan Shan, Yanguang Xu, Miaoyan Zheng, Ying Wang, Huizhu Ren, Liming Chen
Journal of Diabetes and its Complications.2016; 30(3): 488. CrossRef
Relationship between serum C-peptide level and diabetic retinopathy according to estimated glomerular filtration rate in patients with type 2 diabetes
Jin Ook Chung, Dong Hyeok Cho, Dong Jin Chung, Min Young Chung
Journal of Diabetes and its Complications.2015; 29(3): 350. CrossRef
Independent association between serum C‐peptide levels and fat mass‐to‐lean mass ratio in the aging process
Ying Li, Lian Shun Zheng, Yue Li, Duo Duo Zhao, Lu Meng
Geriatrics & Gerontology International.2015; 15(7): 918. CrossRef
Relationship Between β-Cell Function, Metabolic Control, and Microvascular Complications in Type 2 Diabetes Mellitus
Lihua Zhao, Jing Ma, Shaoxin Wang, Yun Xie
Diabetes Technology & Therapeutics.2015; 17(1): 29. CrossRef
Association of fasting insulin and C peptide with diabetic retinopathy in Latinos with type 2 diabetes
Jane Z Kuo, Xiuqing Guo, Ronald Klein, Barbara E Klein, Robert N Weinreb, Pauline Genter, Fone-Ching Hsiao, Mark O Goodarzi, Jerome I Rotter, Yii-Der Ida Chen, Eli Ipp
BMJ Open Diabetes Research & Care.2014; 2(1): e000027. CrossRef
Association between physical activity and serum C‐peptide levels among the elderly
Ying Li, Lu Meng, QianQian Miao, Yasuto Sato
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Age at Diagnosis and C-Peptide Level Are Associated with Diabetic Retinopathy in Chinese
Xiaoling Cai, Xueyao Han, Simin Zhang, Yingying Luo, Yingli Chen, Linong Ji, Alfred S. Lewin
PLoS ONE.2014; 9(3): e91174. CrossRef
Prevalence and risk factors for diabetic retinopathy in Asian Indians with young onset Type 1 and Type 2 Diabetes
Ramachandran Rajalakshmi, Anandakumar Amutha, Harish Ranjani, Mohammed K. Ali, Ranjit Unnikrishnan, Ranjit Mohan Anjana, K.M. Venkat Narayan, Viswanathan Mohan
Journal of Diabetes and its Complications.2014; 28(3): 291. CrossRef
Prediction of response to GLP-1 receptor agonist therapy in Japanese patients with type 2 diabetes
Kenjiro Imai, Tetsuro Tsujimoto, Atsushi Goto, Maki Goto, Miyako Kishimoto, Ritsuko Yamamoto-Honda, Hiroshi Noto, Hiroshi Kajio, Mitsuhiko Noda
Diabetology & Metabolic Syndrome.2014;[Epub] CrossRef
The Association between the Serum C-Peptide Level and Bone Mineral Density
Ying Li, Hua Liu, Yasuto Sato, Bin He
PLoS ONE.2013; 8(12): e83107. CrossRef
C-Peptide and Its Career from Innocent Bystander to Active Player in Diabetic Atherogenesis
Corinna Lebherz, Nikolaus Marx
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C-Peptide and Vascular Complications in Type 2 Diabetic Subjects
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Inflammatory Markers are Associated with Microvascular Complications in Type 2 Diabetes.: Sun Mee Yang, Sung Yong Kim, Ki Young Lee, Yeun Sun Kim, Moon Suk Nam, Ie Byung Park; Korean Diabetes J. 2007;31(6):472-479. Published online November 1, 2007; DOI: https://doi.org/10.4093/jkda.2007.31.6.472

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Abstract PDF

BACKGROUND
Inflammatory markers are known to be sensitive predictors of atherosclerotic disease such as coronary heart disease. Diabetic patients have higher level of inflammatory markers such as fibrinogen, high sensitivity C-reactive protein (hsCRP) or IL-6. We investigated the association of inflammatory markers with microvascular complications in type 2 diabetes. METHODS: We studied cross-sectionally 244 consecutive patients with type 2 diabetes without macrovascular disease such as cerebral infarct, coronary heart disease and peripheral arterial disease. The urinary albumin/creatinine ratio was determined in a morning, untimed, urine specimen. Ophthalmoscopic examinations were performed to evaluate diabetic retinopathy. Diabetic neuropathy was examined by 10-g monofilament, Neuropathic Disability Score and Michigan Neuropathy Screening Instrument. RESULTS: 47 patients (23.5%) had diabetic retinopathy, 81 (34.6%) had nephropathy and 132 (54.2%) had neuropathy. Fibrinogen and erythrocyte sedimentation rate (ESR) were significantly higher in the patients with nephropathy, retinopathy and neuropathy than in those without (P = 0.009, 0.003 and 0.047; P = 0.011, 0.02 and 0.006 , respectively). There were no differences in the hsCRP and IL-6 level between in patients with microvascular complications and in those without. Inflammatory parameters were correlated with each other. The hsCRP was correlated with IL-6 (r = 0.40, P < 0.001) and fibrinogen (r = 0.45, P < 0.001), but fibrinogen was not significantly correlated with IL-6 (r = 0.13, P = 0.08). CONCLUSION: Although IL-6, hsCRP and fibrinogen may be associated with microvascular complications in type 2 diabetes, we show that fibrinogen is a strong marker of microvascular complications.

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Citations to this article as recorded by

Hesperetin suppresses LPS/high glucose-induced inflammatory responses via TLR/MyD88/NF-κB signaling pathways in THP-1 cells
Aeri Lee, HyunJi Gu, Min-Hee Gwon, Jung-Mi Yun
Nutrition Research and Practice.2021; 15(5): 591. CrossRef

In vivo Corneal Confocal Microscopy and Nerve Growth Factor in Diabetic Microvascular Complications.: Ji Sun Nam, Young Jae Cho, Tae Woong Noh, Chul Sik Kim, Jong Suk Park, Min ho Cho, Hai Jin Kim, Ji Eun Yoon, Han Young Jung, Eun Seok Kang, Yu Mie Rhee, Hyung Keun Lee, Chul Woo Ahn, Bong Soo Cha, Eun Jig Lee, Sung Kil Lim, Kyung Rae Kim, Hyun Chul Lee; Korean Diabetes J. 2007;31(4):351-361. Published online July 1, 2007; DOI: https://doi.org/10.4093/jkda.2007.31.4.351

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Abstract PDF: BACKGROUND
In vivo corneal confocal microscopy (IVCCM) is being recognized as a non-invasive, early diagnostic tool for diabetic neuropathy, for it provides a clear image of corneal subbasal nerve plexus in detail. Nerve growth factors (NGF) are believed to regulate peripheral and central nervous system, neuronal differentiation, and regeneration of damaged nerves, and their role in diabetic neuropathy is being emphasized these days. Moreover, NGFs and receptors are also expressed in retina and renal mesangial cells, suggesting their possible role in the common pathogenesis of diabetic microvascular complications. We plan to examine corneal structures of diabetic patients and compare IVCCM with conventional tools and analyze their serum and tear NGF levels. METHODS: IVCCM, nerve conduction velocity (NCV), and serum, urine, and tear samplings were done to 42 diabetic patients. From IVCCM, we measured corneal nerve density, branch, and tortuosity, total corneal/epithelial thickness, and the number of endothelial/keratocyte cells, and we checked patients' biochemical profiles and serum and tear NGF levels. RESULTS: Patients with more severe neuropathy had less corneal endothelial cells (3105 +/- 218 vs. 2537 +/- 142 vs. 2350 +/- 73/mm3 vs. 1914 +/- 465/mm3, P = 0.02), higher serum NGF (36 +/- 15 vs. 60 +/- 57.66 vs. 80 +/- 57.63 vs. 109 +/- 60.81 pg/mL, P = 0.39) and tear NGF levels (135.00 +/- 11.94 vs. 304.29 +/- 242.44 vs. 538.50 +/- 251.92 vs. 719.50 +/- 92.63 pg/mL, P = 0.01). There was a positive correlation between neuropathy and corneal nerve tortuosity (r2 = 0.479, P = 0.044) and negative correlation between neuropathy and endothelial cell count (r2 = -0.709, P = 0.002). Interestingly, similar changes were seen in other microvascular complications as well. CONCLUSION: Our results provide a possibility of using novel tools, IVCCM and NGF, as common diagnostic tools for diabetic microvascular complications, but it should be followed by a large population study.

The Relation Between Serum and Intracellular Magnesium Level And Diabetic Microvascular Complications.: Kyung Hoon Min, Ji Hye Kim, Eun Kyung Choi, Ji Hyun Park, Hong Sun Baek, Tian Ze Ma, Bing Zhe Hong, Yong Geun Kwak, Hyung Sub Kang, Tae Sun Park; Korean Diabetes J. 2004;28(4):284-292. Published online August 1, 2004

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Abstract PDF: BACKGROUND
Low serum magnesium levels are related to diabetes mellitus (DM), high blood pressure (HBP) and metabolic syndrome (MS). However, as far as is known, there have been no previous studies analyzing the relevance of the serum and intracellular magnesium concentrations in diabetic microvascular complication individuals compared with healthy individuals. SUBJECTS AND METHODS: A pilot study was performed to compare 35 individuals with DM with 22 disease-free control subjects. The serum and intracellular magnesium levels of each group were measured, and found to be elevated in the diabetic group with diabetic microvascular complications. RESULTS: The mean serum magnesium levels among the subjects with DM and the control subjects were 0.0503 +/- 0.0750 and 0.9166 0.1149 mmol/L (p<0.001), respectively. The mean intracellular magnesium levels among the subjects with DM and the control subjects were 3.3548+/-0.1863 and 3.6732 0.2428 mM/mg protein (p<0.001), respectively. In those diabetic subjects whose serum magnesium concentration was measured, 28 had diabetic retinopathy, 30 diabetic nephropathy and 20 diabetic neuropathy. The mean serum magnesium concentrations of each diabetic microvascular complication were 0.9320 0.2813, 0.9259 0.1188 and 0.9305 0.1293 mmol/L, respectively, which that were significantly lower than those of the healthy subjects (p<0.001, p<0.001 and p<0.01). Also, the diabetic subjects whose intracellular magnesium concentrations were measured, 13 had diabetic retinopathy, 15 diabetic nephropathy and 9 diabetic neuropathy. The mean intracellular magnesium concentrations of each diabetic microvascular complication were 3.3484 0.1607, 3.3289 0.1832 and 3.3768 0.2096 mM/mg protein, respectively, and were also significantly lower than those of the healthy subjects (p<0.001and p<0.01). Each diabetic microvascular complication was also negatively correlated with the serum magnesium and intracellular magnesium levels. CONCLUSION: This study reveals that a significant relation ship exists between low serum and intracellular magnesium levels and diabetic microvascular complications, particularly retinopathy and nephropathy. A large scale study on these subjects will be required to generalize our results.

Microvascular Complications and lts Relationship with Obesity in Outpatient Type 2 Diabetics.: Seong Kyu Lee, Bong Nam Chae, Eun Gyoung Hong, Hye Lim Noh, Hyeon Kyoung Cho, Yoon Jung Kim, Mi Deok Lee, Yoon Sok Chung, Kwan Woo Lee, Nam Han Cho, Hyeon Man Kim; Korean Diabetes J. 2000;24(1):60-70. Published online January 1, 2001

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Abstract PDF: BACKGROUND
Korean type 2 diabetic patients who are frequently non-obese, may be genetically different from Western type 2 diabetics who are frequently obese. Therefore, the diabetic complications of type 2 diabetes mellitus in Korea may be also different from those of Western countries. Until now, most studies reported in Korea did not analyse the microvascular complications of type 2 diabetes mellitus according to obesity, and also the criteria in the diagnosis of microvascular complications were different in each study. We investigated the microvascular complications and its relationship with obesity, in type 2 diabetic patients visiting an outpatient clinic. METHODS: The study subjects were type 2 diabetic patients visiting an outpatient clinic of Ajou University Hospital. We selected patients participating in a 75 g oral glucose tolerance test, retrospectively. Type 2 diabetes was diagnosed according to the WHO/NDDG classification of diabetes. Biochemical studies including lipid profile, plasma insulin and C-peptide levels were done. Anthropometric measurements were performed. Based on BMI (kg/m2), the patients were divided into the following groups: the lean group, whan the BMI was less than 20kg/m2; the ideal body weight (IBW) group, if the BMI was between 20 kg/m and 25 kg/m in women and 20kg/m and 27 kg/m in men; and the obese group, when the BMI was>25 kg/m in women and >27 kg/m2 in men. RESULTS: 1. Neuropathy (45.2%) was the most frequent among the microvascular complications, and the frequency of retinopathy was 15.1%, and that of nephropathy was 4.9k. Within 5 years of diabetes duration, the frequency of neuropathy, retinopathy, and nephropathy was 43.2%, 11.8%, and 2,9%, respectively. 2. Glycosylated hemoglobin (HbA1c) and fasting blood glucose levels were not different among the three groups. Beta cell function{delta(insulin 30min insulin Omin)/delta(glucose 30min - glucose Omin)} was the highest in the obese group, However, beta cell function(delta/delta G) divided by the basal insulin level, considered insulin resistance, was not different among the three groups. 3. Within 5 years of diabetes duration, retinopathy tended to be the most frequent in the lean group, whereas neuropathy tended to be the most frequent in the obese group, and body mass index influenced the retinopathy and neuropathy, statistically significantly. CONCLUSION: Diabetic neuropathy was the most frequent among microvascular complications of type 2 diabetes mellitus in our study subjects. At the time of presentation within 5 years of diabetes duration, the lean group of type 2 diabetics had a tendency of the more frequent retinopathy, the obese group had a tendency of the more frequent neuropathy. These results suggest that type 2 diabetes mellitus in Korea is also not a singie disease entity, as in Western countries and is a heterogenous group of disorders with a diversity of microvascular complications. However, the more studies about this will be required.

Hyperfibrinogenemia as an Important Risk Factor for Microvascular Complications in NIDDM Patients.: Suk Kyeong Kim, Hyeong Kyu Park, Sun Wook Kim, Do Joon Park, Chan Soo Shin, Seong Yeon Kim, Bo Youn Cho, Hong Kyu Lee; Korean Diabetes J. 1997;21(4):406-413. Published online January 1, 2001

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Abstract PDF: BACKGROUND
Abundant evidences have accumulated to suggest that atherosclerosis is accelerated in both type I and type Il diabetes but, traditional risk factors(hyperlipidemia, hypertension, smoking, age, obesity) do not account fully for the increased prevalence and severity of vascular diseases in diabetes. In this study, we examined the relationship of plasma fibrinogen to microvascular complications in NIDDM patients METHODS: In this cross-sectional study, 104 NIDDM patients were chosen from subjects who were attending the metabolic ward of Seoul National University Hospital. None of them were smokers, nor had any clinical evidences of acute infections, cancers or liver diseases. Arnong 104 patients, 55 patients (male 26, fernale 29) had no evidence of microvascular complications and 49(male 30, female 19) had one or moe microvascular complications. Their mean age(55.7+11.6 and 57.2+8.9 years old) and BMI (23.34+2.98 kg/m and 23.74+3.41 kg/m) were similar between two groups. This study defined microvascular complications as follows: 1) retinopathy classified based on fundoscopic and fluorescein angiographic assessmeot to background and proliferative, 2) nephropathy defined by 24 hour urine protein over 500mg, and 3) pheripheral neuropathy assessed by symptoms or NCV. RESULTS: 1) Clinically, there was no differences between two groups with respect to diastolic BP, C-peptide, HbA1c, and triglyceride level. However statistically significant differences were noted in systolic blood pressure, and total and LDL-cholesterol. Also mean fibrinogen level was more elevated significantly in diabetic patients with microvascular complications than those without microvascular complications. 2) Univariate analysis shows significant correlations between fibrinogen and the other variables such as duration of diabetes, total cholesterol level and systolic blood pressure. 3) However, fibrinogen concentration was higher in NIDDM patients with microvascuiar complications regardless of duration of diabetes, hypertension and HbA1c in multivariate logisric regression analysis (P=0.010). Conclusions: These results indicated that hyperfibrinogenemia were observed in NIDDM patient with microvascular complications regardless of duration of diabetes, systolic BP, and total cholesterol. Therefore our study suggests that hyperfibrogenemia may be one of the important missing links in the pathogenesis of diabetic microvascular diseases.

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