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The average 30-minute post-prandial C-peptide predicted diabetic retinopathy progress: a retro-prospective study

BMC Endocrine Disorders volume 23, Article number: 63 (2023) Cite this article

Abstract

Background

The conclusion between Connecting peptide (C-peptide) and diabetic chronic complication was controversial. The purpose of this study is to explore the possible association between average C-peptide with diabetic retinopathy (DR) progression in Chinese patients with type 2 diabetes.

Methods

This is a retro-prospective study. 622 patients with type 2 diabetes were included. DR was evaluated using non-mydriatic fundus photography and DR progression was defined as any deterioration of either eye. Fasting and postprandial c-peptide levels were assayed at baseline and follow-up period. Differences between continuous variables were compared using the Mann–Whitney U test; and categorical variables were analyzed by the chi-square test. Correlation between parameters and 30-minute postprandial C-peptide were determined by Spearman correlation test. The relationship between C-peptide and DR progression was evaluated by multivariable binary logistic regression. Two-tailed P-values < 0.05 were regarded as statistically significant.

Results

DR was present in 162 (26.0%) patients at baseline, and 26.4% of patients were found progression of DR at follow-up. Patients with progression of DR had lower average levels of 30-minute postprandial C-peptide (2.01 ng/ml vs. 2.6 ng/ml, p = 0.015) and 120-minute postprandial C-peptide (3.17 ng/ml vs. 3.92 ng/ml, p < 0.029), as well as average increment of 30-minute (0.41 ng/ml vs. 0.64 ng/ml, p = 0.015) and 120-minute postprandial C-peptide (1.48 ng/ml vs. 1.93 ng/ml, p < 0.017), than those without DR aggravation. Multivariate logistic regression analysis determined that 30-minute postprandial C-peptide and its increment were related to reduced odds ratios for DR progression (odds ratios [OR] = 0.83 and 0.74, respectively).

Conclusion

Our results suggest that the Average 30-minute post-prandial C-peptide and increment were negatively correlated with DR progression, which further demonstrates the importance to preserve β-cell residual function in the prevention for DR progression.

Trial registration

Not applicable.

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Background

Impaired pancreatic islet β-cell compensatory function along with insulin resistance make a valuable contribution towards the occurrence of type 2 diabetes in Eastern Asia [1, 2]. In comparison to basic insulin secretion which was related to fasting plasma glucose, decreased early phase insulin secretion was associated with elevated post-load glucose [3]. Hyperglycemic clamp study indicated first phase insulin infusion inhibited hepatic glucose production by 90% [4, 5]. C-peptide is split from proinsulin, composed of 31 amino acids, and secreted in an equimolar pattern with insulin under stimulation by elevated glycemia. As a result, C-peptide was used as an alternative marker of β-cell function in clinical practice [6]. Similarly, numerous evidences indicated that C-peptide was closely associated with fasting and post-load glucose [7]. Moreover, in oral glucose tolerance test (OGTT), early and late C-peptide reactions have opposite predictive effects on type 1 diabetes in autoantibody positive individuals [8]. Recently, several studies indicated that postprandial C-peptide is a useful predictor of future insulin therapy in patients with type 2 diabetes [9,10,11,12].

The conclusion between C-peptide and chronic complication was controversial [6]. Some trials have demonstrated that C-peptide is positively correlated with macrovascular complications and negatively related to microvascular complications [6]. Diminished glucose/C-peptide ratios are associated with reduced renal function [13]. Among microvascular complications, DR affected 20% of patients with diabetes, and caused millions of new blindness cases in adults ranging 20 to 74 years old [14, 15]. Fasting C-peptide has been verified to be negatively associated with DR [15, 16]. Although researchers pointed out that post-load glucose was independently associated with urine albumin excretion, cardiovascular diseases (CVD), cancer, and mortality in the multivariable models [17, 18], the association between post-load C-peptide and DR progression was seldomly involved.

In the present study, we aimed to find out the relationship between C-peptide and DR in the Cohort including 622 type 2 diabetes patients, and to explore the connection between post-load C-peptide and DR progression.

Methods

Study design and patients

This retro-prospective study was performed in Putuo hospital, which is affiliated to Shanghai University of Traditional Chinese Medicine. Aim to explore the possible association between average C-peptide with DR progression in Chinese patients with type 2 diabetes. A total of 622 patients with type 2 diabetes underwent non-mydriatic fundus photography were included in our study From February 27th 2003 to April 25th 2012. Patients were excluded in the presence of any of the following conditions: (1) type 1 diabetes mellitus; (2) glaucoma, retinal detachment, vitreous hemorrhage; (3) participants with a history of intraocular surgery or had intraocular surgery at either eye during follow-up; (4) patients who lost to follow-up or had no clinical data recorded during follow-up; (5) renal dysfunction (serum creatinine ≥ 115 µmol/L), hepatic dysfunction (alanine transaminase ≥ 97.5 U/L and/or aspartate aminotransferase ≥ 55.5 U/L), hematological disease, rheumatic diseases, malignant tumors.

The protocol was approved by the institutional review board of Putuo hospital, Shanghai University of Traditional Chinese Medicine. Written informed consent was obtained from all participants in this study.

Anthropometric and laboratory measurements

All anthropometric and biochemical examinations at baseline and follow up used the same study protocol. Measure waist circumference, weight and height according to standard procedures. The Body Mass Index (BMI) was computed using the formula of the weight divided by meters squared (kg/m2). After a 10-minute of calm, the subjects sat down and measured their blood pressure twice with a mercury sphygmomanometer, taking the average value. According to the ingestion of a diabetic diet based on the criteria recommended by the Chinese Diabetes Society [19], peripheral venous blood samples of all subjects were collected at 0, 30, and 120 min after at least 10-hour overnight fasting. Hemoglobin A1c (HbA1c) was detected using the HLC-723G11 (Shunan, Yamaguchi, Japan) high-performance liquid chromatography analyzer; plasma glucose concentrations were measured using the glucose oxidase method (Roche, Mannheim, Germany); an automatic analyzer (Hitachi 7600, Tokyo, Japan) was used to determine the lipid profiles; C-peptide was determined with a radioimmunoassay method (Linco Research, St Charles, MO, USA).

Assessment of diabetic retinopathy

Retina screening was performed using non-mydriatic fundus photography by a professional ophthalmologist. The severity of DR is graded according to the 2003 standard proposed by the American Academy of Ophthalmology[20]: no apparent retinopathy DR (Grade 0); mild non-proliferative DR (Grade I); moderate non-proliferative DR (Grade II); severe non-proliferative DR (Grade III); and proliferative DR (Grade IV). DR progression was defined as participants without baseline DR who developed DR or any greater worsening of DR at any eye during the follow-up.

Statistical analysis

Median (interquartile range) were presented for continuous variables, while frequency (%) for categorical variables. Differences between continuous variables were compared using the Mann–Whitney U test; and categorical variables were analyzed by the chi-square test. Correlation between parameters and 30-minute postprandial C-peptide were determined by Spearman correlation test. The relationship between C-peptide and DR progression was evaluated by multivariable binary logistic regression. SPSS 25.0 (SPSS Inc., Chicago, IL, USA) software was used for all statistical analysis. Two-tailed P-values < 0.05 were regarded as statistically significant.

Results

Baseline clinical characteristics of participants according to DR status

Baseline clinical characteristics of all patients were listed in Table 1. Overall, 162 (26.0%) patients had DR at baseline. Compared to patients without DR, patients with DR were older (60 years versus 57 years, P < 0.05), had longer diabetes duration (10 years versus 4 years, P < 0.001) and higher frequency of insulin therapy. Levels of 120-minute postprandial C-peptide (PCP) and its increment were lower in patients with DR than those without DR. The prevalence of males, hypertension, smoking and alcohol consumption were similar in the two groups. Moreover, there were no difference in BMI, waist circumference (WC), blood pressure, levels of fasting blood glucose, postprandial blood glucose, HbA1c, lipid level, fasting C-peptide, 30-minute PCP and its increment.

Clinical features during follow-up according to the DR progression status

As shown in Table 2, DR progression was detected in 164 (26.4%) of the subjects at follow-up. Patients with DR progression had higher average HbA1c levels (8.9% versus 8.5%, P < 0.05), and lower levels of average 30-minute PCP (median 2.01 ng/ml versus 2.60 ng/ml, P = 0.015), average 120-minute PCP (median 3.17 ng/ml versus 3.92 ng/ml, P = 0.029), average 30-minute PCP increment (median 0.41 ng/ml versus 0.64 ng/ml, P = 0.015) and average 120-minute PCP increment (median 1.48 ng/ml versus 1.93 ng/ml, P = 0.017). The two groups had similar levels of average waist circumstance, blood pressure, blood lipid, fasting and post prandial plasma glucose as well as fasting plasma C-peptide.

Clinical characteristics correlating with 30-minute postprandial C-peptide

As shown in Table 3, average 30-minute PCP as well as its increment was moderately associated with average HbA1c, body weight, WC, BMI, diastolic blood pressure (DBP), High-density lipoprotein cholesterol (HDL-C), triglyceride and total cholesterol (all P < 0.05). There were non-significant associations of average 30-minute PCP with average fasting plasma glucose, average 30-minute post-prandial glucose (PPG) and 120-minute PPG.

Odds ratios for DR progression according to C-peptide levels

As displayed in Table 4, multivariate logistic regression analysis indicated that 30-minute postprandial C-peptide and its increment were significantly related to DR progress risk reduction (OR = 0.83 and 0.74, respectively), this association remained significant after further adjusted for diabetes management including insulin therapy and insulin secretagogue. However, the association of baseline fasting C-peptide (FCP), 30-minute PCP, 120-minute PCP, and average FCP and 120-minute PCP with DR progression was non-significant after adjusting confounding variables.

Table 1 Baseline characteristics of patients
Full size table
Table 2 Clinical characteristics according to diabetic retinopathy progression during follow-up
Full size table
Table 3 Parameters correlated with 30-minute post-prandial C- peptide
Full size table

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Table 4 Association between C peptide and diabetic retinopathy progression
Full size table

Discussion

The present study indicated that in patients with type 2 diabetes, levels of postprandial C-peptide and its increment were lower in patients with DR. Furthermore, 30-minute postprandial C-peptide concentrations and its increment were significantly connected with reduced risk of DR progression. This relationship remained significant after adjusting for confounding risk factors including gender, age, smoking status, alcohol drinking, baseline DR status, hypertension, follow-up period, HbA1c, triglyceride and HDL-C.

DR is the main reason for new cases of blindness in adults aged 20–74 [14]. The DR prevalence of diabetes patients obtained from different studies have shown substantial variability, ranging from 17.6% in an India study [21] to 33.2% in a large U.S. study [22]. A recent report [23] showed that the prevalence of DR in diabetic group was 23.57% in China. In our study, the frequency of DR was 26.0% at baseline.

The link between C-peptide and DR in patients with type 2 diabetes is still controversial. Several previous studies have shown that lower levels of C-peptide are negatively correlated with DR in Type 2 Diabetes Mellitus (T2DM) patients, indicating that C-peptide has a protective effect on microvascular complications of diabetes [24,25,26,27], while other studies did not find the association [28, 29]. The study from Korea demonstrated that patients with lower C-peptide increment (postprandial –fasting C-peptide) had a higher risk of DR and an increased DR severity [27]. In addition, other research studies have shown that the lower postprandial C-peptide concentration may be related to the higher incidence rate of DR. Our results are in agreement with those studies that postprandial C-peptide levels and its increment are negatively associated with DR [23,24,25,26,27]. However, in Australian population, systolic blood pressure, HbA1c and duration of diabetes are independent risk factors for the development of DR, not C-peptide [30]. In this prospective cohort, our data verified that average 30-minute post-prandial C-peptide and its increment was negatively correlated with DR progression.

The relationship between C-peptide and DR was complicated. First, C-peptide reflects the endogenous insulin secretion of diabetes patients [31, 32] and is related to the improvement of blood glucose control and the reduction of blood glucose variability [24, 33,34,35,36], which is conducive to reducing DR risk. Besides, C-peptide can regulate insulin secretion, islet microcirculation and glucose tolerance in rats [37]. Secondly, studies have reported that C-peptide may have its own biological activity and exert some physiological function [6]. Studies have demonstrated that C-peptide may have a direct impact on the development and/or progression of microvascular complications [38, 39]. Thirdly, C-peptide could inhibit the vascular leakage induced by hyperglycemia in the diabetic retina and suppress the function of vascular endothelial growth factor (VEGF), which is a crucial factor that leads to elevated retinal microvascular permeability in diabetes and promotes the progression of DR [40, 41]. In addition, C-peptide could reduce neointimal hyperplasia induced by insulin [42].

Nevertheless, several limitations of our study should be taken into account. First, patients included in this study were from a single center and the sample could not represent the entire patient population. Second, the follow-up period was relatively short and further analysis with a longer follow-up is required. Third, other confounding factors such as osteoporosis may also be considered.

Conclusion

The average 30-minute post-prandial C-peptide and its increment were negatively associated with DR progression, demonstrating the importance of preserving β-cell residual function in the prevention for DR progression. Better residual β-cell function may partly explain the lower risk of DR in patients with type 2 diabetes.

Data availability

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

Abbreviations

BMI:

Body Mass Index

C-peptide:

Connecting peptide

CVD:

Cardiovascular diseases

DR:

Diabetic retinopathy

DBP:

Diastolic blood pressure

FPG:

Fasting plasma glucose

FCP:

Fasting C-peptide

HbA1c:

Hemoglobin A1c

HDL-C:

High-density lipoprotein cholesterol

HTN:

Hypertension

kg/m2 :

Meters squared

OGTT:

Oral glucose tolerance test

PCP:

Postprandial C-peptide

PPG:

Post-prandial glucose

SBP:

Systolic blood pressure

T2DM:

Type 2 Diabetes Mellitus

TG:

Triglyceride

TC:

Total cholesterol

VEGF:

Vascular endothelial growth factor

WC:

waist circumference

References

  1. Yan J, Peng D, Jiang F, et al. Impaired pancreatic beta cell compensatory function is the main cause of type 2 diabetes in individuals with high genetic risk: a 9 year prospective cohort study in the chinese population. Diabetologia. 2016;59:1458–62.

    Article  CAS  PubMed  Google Scholar 

  2. Møller JB, Dalla Man C, Overgaard RV, et al. Ethnic differences in insulin sensitivity, β-cell function, and hepatic extraction between japanese and Caucasians: a minimal model analysis. J Clin Endocrinol Metab. 2014;99:4273–80.

    Article  PubMed  Google Scholar 

  3. Honda M, Tsuboi A, Minato-Inokawa S et al. Reduced Birth Weight, Decreased Early-Phase Insulin Secretion, and Increased Glucose Concentrations after Oral Glucose Tolerance Test in Japanese Women Aged 20 Years with Family History of Type 2 Diabetes. J Diabetes Res. 2020; 2020: 8822135.

  4. Caumo A, Luzi L. First-phase insulin secretion: does it exist in real life? Considerations on shape and function. Am J Physiol Endocrinol Metab. 2004;287:E371–85.

    Article  CAS  PubMed  Google Scholar 

  5. Luzi L, DeFronzo RA. Effect of loss of first-phase insulin secretion on hepatic glucose production and tissue glucose disposal in humans. Am J Physiol. 1989;257:E241–6.

    CAS  PubMed  Google Scholar 

  6. Vejrazkova D, Vankova M, Lukasova P, Vcelak J, Bendlova B. Insights into the physiology of C-peptide. Physiol Res. 2020;69:237–s43.

    Article  Google Scholar 

  7. Tura A, Morbiducci U, Sbrignadello S, et al. Shape of glucose, insulin, C-peptide curves during a 3-h oral glucose tolerance test: any relationship with the degree of glucose tolerance? Am J Physiol Regul Integr Comp Physiol. 2011;300:R941–8.

    Article  CAS  PubMed  Google Scholar 

  8. Ismail HM, Becker DJ, Libman I, et al. Early and late C-peptide responses during oral glucose tolerance testing are oppositely predictive of type 1 diabetes in autoantibody-positive individuals. Diabetes Obes Metab. 2020;22:997–1000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Iwao T, Sakai K, Sata M. Postprandial serum C-peptide is a useful parameter in the prediction of successful switching to liraglutide monotherapy from complex insulin therapy in japanese patients with type 2 diabetes. J Diabetes Complications. 2013;27:87–91.

    Article  PubMed  Google Scholar 

  10. Ohbatake A, Yagi K, Karashima S, et al. C-Peptide area under the curve at Glucagon Stimulation Test predicts glucose improvements by GLP-1 receptor analogue: a retrospective observational study. Diabetes Ther. 2019;10:673–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Uehara R, Yamada E, Nakajima Y, et al. Casual C peptide index: Predicting the subsequent need for insulin therapy in outpatients with type 2 diabetes under primary care. J Diabetes. 2022;14:221–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Saisho Y, Kou K, Tanaka K, et al. Postprandial serum C-peptide to plasma glucose ratio as a predictor of subsequent insulin treatment in patients with type 2 diabetes. Endocr J. 2011;58:315–22.

    Article  CAS  PubMed  Google Scholar 

  13. D’Elia JA, Mulla C, Liu J, Weinrauch LA. Variations in glucose/C-peptide ratio in patients with type 2 diabetes associated with renal function. Diabetes Res Clin Pract. 2019;150:1–7.

    Article  PubMed  Google Scholar 

  14. Yau JW, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35:556–64.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Lu J, Hou X, Zhang L, et al. Association between body mass index and diabetic retinopathy in chinese patients with type 2 diabetes. Acta Diabetol. 2015;52:701–8.

    Article  CAS  PubMed  Google Scholar 

  16. Wang Y, Wan H, Chen Y, et al. Association of C-peptide with diabetic vascular complications in type 2 diabetes. Diabetes Metab. 2020;46:33–40.

    Article  PubMed  Google Scholar 

  17. Lu J, He J, Li M, et al. Predictive value of fasting glucose, postload glucose, and Hemoglobin A(1c) on risk of diabetes and complications in chinese adults. Diabetes Care. 2019;42:1539–48.

    Article  CAS  PubMed  Google Scholar 

  18. Li D, Hou X, Ma X, et al. Association between an increment of 30-minute postchallenge plasma glucose and urine albumin excretion exists in postmenopausal women but not in premenopausal women. Menopause. 2011;18:1303–8.

    Article  PubMed  Google Scholar 

  19. Chinese Diabetes Society. Guidelines for the prevention and treatment of type 2 diabetes in China (2010). Chin J Diabetes. 2012;20:81–117.

    Google Scholar 

  20. Wilkinson CP, Ferris FL 3rd, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.

    Article  CAS  PubMed  Google Scholar 

  21. Rema M, Premkumar S, Anitha B, et al. Prevalence of diabetic retinopathy in urban India: the Chennai Urban Rural Epidemiology Study (CURES) eye study, I. Invest Ophthalmol Vis Sci. 2005;46:2328–33.

    Article  PubMed  Google Scholar 

  22. Wong TY, Klein R, Islam FM, et al. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006;141:446–55.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Cai X, Han X, Zhang S, et al. Age at diagnosis and C-peptide level are associated with diabetic retinopathy in chinese. PLoS ONE. 2014;9:e91174.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Suzuki K, Watanabe K, Motegi T, Kajinuma H. High prevalence of proliferative retinopathy in diabetic patients with low pancreatic B-cell capacity. Diabetes Res Clin Pract. 1989;6:45–52.

    Article  CAS  PubMed  Google Scholar 

  25. Bo S, Gentile L, Castiglione A, et al. C-peptide and the risk for incident complications and mortality in type 2 diabetic patients: a retrospective cohort study after a 14-year follow-up. Eur J Endocrinol. 2012;167:173–80.

    Article  CAS  PubMed  Google Scholar 

  26. Yoon HJ, Cho YZ, Kim JY, et al. Correlations between Glucagon stimulated C-peptide levels and microvascular complications in type 2 diabetes patients. Diabetes Metab J. 2012;36:379–87.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kim BY, Jung CH, Mok JO, Kang SK, Kim CH. Association between serum C-peptide levels and chronic microvascular complications in korean type 2 diabetic patients. Acta Diabetol. 2012;49:9–15.

    Article  CAS  PubMed  Google Scholar 

  28. Snehalatha C, Mohan R, Mohan V, Ramachandran A, Viswanathan M. Pancreatic B-cell function in relation to diabetic retinopathy in asian indian NIDDM patients. Acta Diabetol Lat. 1988;25:95–100.

    Article  CAS  PubMed  Google Scholar 

  29. Sari R, Balci MK. Relationship between C peptide and chronic complications in type-2 diabetes mellitus. J Natl Med Assoc. 2005;97:1113–8.

    PubMed  PubMed Central  Google Scholar 

  30. Tapp RJ, Shaw JE, Harper CA, et al. The prevalence of and factors associated with diabetic retinopathy in the australian population. Diabetes Care. 2003;26:1731–7.

    Article  PubMed  Google Scholar 

  31. Genuth SM. Clinical utility of C-peptide measurement in diabetes mellitus. Endocr Pract. 1996;2:266–8.

    Article  CAS  PubMed  Google Scholar 

  32. Jones AG, Hattersley AT. The clinical utility of C-peptide measurement in the care of patients with diabetes. Diabet Med. 2013;30:803–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Steffes MW, Sibley S, Jackson M, Thomas W. Beta-cell function and the development of diabetes-related complications in the diabetes control and complications trial. Diabetes Care. 2003;26:832–6.

    Article  PubMed  Google Scholar 

  34. Panero F, Novelli G, Zucco C, et al. Fasting plasma C-peptide and micro- and macrovascular complications in a large clinic-based cohort of type 1 diabetic patients. Diabetes Care. 2009;32:301–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Bo S, Cavallo-Perin P, Gentile L, Repetti E, Pagano G. Relationship of residual beta-cell function, metabolic control and chronic complications in type 2 diabetes mellitus. Acta Diabetol. 2000;37:125–9.

    Article  CAS  PubMed  Google Scholar 

  36. Boz M, Scheen AJ, Gerard PL, Castillo MJ, Lefebvre PJ. Retinopathy, but not neuropathy, is influenced by the level of residual endogenous insulin secretion in type 2 diabetes. Diabete Metab. 1995;21:353–9.

    CAS  PubMed  Google Scholar 

  37. Wu L, Olverling A, Huang Z, et al. GLP-1, exendin-4 and C-peptide regulate pancreatic islet microcirculation, insulin secretion and glucose tolerance in rats. Clin Sci (Lond). 2012;122:375–84.

    Article  CAS  PubMed  Google Scholar 

  38. Samnegård B, Jacobson SH, Jaremko G, Johansson BL, Sjöquist M. Effects of C-peptide on glomerular and renal size and renal function in diabetic rats. Kidney Int. 2001;60:1258–65.

    Article  PubMed  Google Scholar 

  39. Djemli-Shipkolye A, Gallice P, Coste T, et al. The effects ex vivo and in vitro of insulin and C-peptide on Na/K adenosine triphosphatase activity in red blood cell membranes of type 1 diabetic patients. Metabolism. 2000;49:868–72.

    Article  CAS  PubMed  Google Scholar 

  40. Lee YJ, Jung SH, Kim SH, et al. Essential role of transglutaminase 2 in vascular endothelial growth Factor-Induced Vascular Leakage in the retina of Diabetic mice. Diabetes. 2016;65:2414–28.

    Article  CAS  PubMed  Google Scholar 

  41. Lim YC, Bhatt MP, Kwon MH, et al. Prevention of VEGF-mediated microvascular permeability by C-peptide in diabetic mice. Cardiovasc Res. 2014;101:155–64.

    Article  CAS  PubMed  Google Scholar 

  42. Mughal RS, Scragg JL, Lister P, et al. Cellular mechanisms by which proinsulin C-peptide prevents insulin-induced neointima formation in human saphenous vein. Diabetologia. 2010;53:1761–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank all the participants and the research team involved in the present project.

Funding

This research was supported by Clinical Characteristic of Health System in Putuo District, Shanghai (2020tszk01), Shanghai Medical Key Specialties (ZK2019B16), Science, Technology Innovation Project of Putuo District Health System (ptkwws202302) and Research Project of Shanghai Municipal Health Care Commission (20204Y0154).

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Author notes

  1. Ting Pan and Jie Gao contributed equally to this article. Co-authors assisted in data collection and collation.

Authors and Affiliations

  1. School of Medical and Life Sciences, Chengdu University of Traditional Chinese Medicine, Chengdu, China

    Ting Pan & Huihui Zhang

  2. Department of Endocrinology, Putuo Hospital, Shanghai University of Traditional Chinese Medicine, 164 LanXi Road, 200062, Shanghai, China

    Ting Pan, Jie Gao, Huihui Zhang, Jun Lu & Tao Lei

  3. Shanghai Putuo Central School of Clinical Medicine, Anhui Medical University, Anhui, China

    Xinghua Cai

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Contributions

All authors contributed to the study conception and design. The research scheme was designed by Tao Lei. Data collection and analysis were performed by Jun Lu. Data collation was completed by Xinghua Cai and Huihui Zhang. The first draft of the manuscript was written by Ting Pan and Jie Gao. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Jun Lu or Tao Lei.

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Ethics approval and consent to participate

The study was approved by the institutional review board of Putuo hospital, Shanghai University of Traditional Chinese Medicine in accordance with the principles of the Helsinki Declaration of 1975, as revised in 1983. Written informed consent was obtained from all participants at baseline and follow-up in this study. All methods were carried out in accordance with relevant guidelines and regulations.

Animal Studies: Not applicable.

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Pan, T., Gao, J., Cai, X. et al. The average 30-minute post-prandial C-peptide predicted diabetic retinopathy progress: a retro-prospective study. BMC Endocr Disord 23, 63 (2023). https://doi.org/10.1186/s12902-023-01300-x

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BMC Endocrine Disorders

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