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.

Citations

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Impact of Bariatric Surgery on Treatment Burden and Progression of Diabetic Retinopathy
Ariana Allen, Hemal Patel, Sandra S. Stinnett, Jullia A. Rosdahl, Stefanie Schuman
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Role of Systemic Factors in Improving the Prognosis of Diabetic Retinal Disease and Predicting Response to Diabetic Retinopathy Treatment
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S. Feldman-Billard
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Angela Moh, Kumari Neelam, Xiao Zhang, Chee Fang Sum, Subramaniam Tavintharan, Keven Ang, Simon Biing Ming Lee, Wern Ee Tang, Su Chi Lim
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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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Bariatric Surgery for Adolescents with Type 2 Diabetes: an Emerging Therapeutic Strategy
M. A. Stefater, T. H. Inge
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Original Articles

Epidemiology
The Association between Hypertension Comorbidity and Microvascular Complications in Type 2 Diabetes Patients: A Nationwide Cross-Sectional Study in Thailand: Cameron Hurst, Bandit Thinkhamrop, Hoang The Tran; Diabetes Metab J. 2015;39(5):395-404. Published online October 22, 2015; DOI: https://doi.org/10.4093/dmj.2015.39.5.395

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Abstract PDF PubReader

Background

Type 2 diabetes mellitus (T2DM) is a global pandemic and its prevalence is rapidly increasing in developing countries, including Thailand. The most common comorbidity of T2DM is hypertension. T2DM with a hypertension comorbidity is likely to exacerbate the development of, or more severe microvascular complications. This study aims to determine the association between the hypertension comorbidity and microvascular complication among T2DM patients in Thailand.

Methods

The present study is a nationwide, multicenter, cross-sectional survey of T2DM outpatients across Thailand. Binary logistic mixed effect regression was used to investigate the effect of hypertension and other risk factors on the presence of microvascular complications. Imputation was used to investigate potential bias introduced by missing values.

Results

Of the 55,797 T2DM patients included in our sample, 55.35% were hypertensive. Prevalence of microvascular complication diagnosis in the last 12 months was higher in T2DM patients with hypertension than those without hypertension (12.12% vs. 9.80%, respectively). Patient with a hypertension comorbidity had 1.32 time the odds of developing microvascular complication (adjusted odds ratio [OR], 1.32; 95% confidence interval [CI], 1.20 to 1.46; P<0.001). Older age, longer diabetes duration had 1.07 and 1.21 times the odds of developing microvascular complication, per 10 years (age) and 5 years (duration), respectively (OR_age, 1.07; 95% CI, 1.03 to 1.12; P<0.001; and OR_duration, 1.12; 95% CI, 1.07 to 1.16; P<0.001; respectively). Minimal bias was introduced by missing values, and did not influence to the magnitude of effect of hypertension on the presence microvascular complication.

Conclusion

Hypertension comorbidity is highly associated with microvascular complication among T2DM patients. Patients with T2DM and physicians should pay attention to blood pressure control.

Citations

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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.

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Clinical Characteristics and Direct Medical Costs of Type 2 Diabetic Patients.: Eun Joon Moon, Young Eun Jo, Tae Chin Park, Yun Kyung Kim, Sun Hye Jung, Hae Jin Kim, Dae Jung Kim, Yoon Sok Chung, Kwan Woo Lee; Korean Diabetes J. 2008;32(4):358-365. Published online August 1, 2008; DOI: https://doi.org/10.4093/kdj.2008.32.4.358

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Abstract PDF

BACKGROUND
Type 2 diabetes mellitus is an expensive chronic metabolic disorder and its prevalence has been increasing rapidly in South Korea, owing to a westernized lifestyle. We analyzed the annual direct medical costs attributable to type 2 diabetes and its chronic complications in Korea retrospectively. METHODS: We randomly selected 1,051 patients with type 2 diabetes who visited Ajou University Hospital as an outpatient in 2005. Clinical characteristics, duration of diabetes, and microvascular and macrovascular complications were assessed from a medical chart review. The annual direct medical costs included insurance covered and uncovered medical costs. RESULTS: Of the 1,051 patients with type 2 diabetes, 48.2% had at least one microvascular complication, 5.6% had at least one macrovascular complication, and 12.4% of the patients had both microvascular and macrovascular complications. The average annual direct medical cost was found to be 3,348,488won per patient. In patients with microvascular complications, the total cost of management was increased 1.4 times compared to those without complications. Direct medical costs for patients with macrovascular complications were 2.1-fold as high as patients with no complications. Those patients with both microvascular and macrovascular complications, increased costs by 3.1-fold over those without complications. CONCLUSION: Chronic complications have a substantial impact on the direct medical costs of type 2 diabetes. The prevention of chronic diabetic complications will not only influence the mortality and morbidity of patients with type 2 diabetes, but also potentially reduce medical costs.

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Direct Medical Costs of Type 2 Diabetic Patients in the Tertiary Hospital.: Joo An Hwang, Tae Chin Park, Sun Hye Jung, Hae Jin Kim, Dae Jung Kim, So Hun Kim, Moon Suk Nam, Tae Hyun Kim, Moon Kyu Lee, Kwan Woo Lee; Korean Diabetes J. 2008;32(3):259-268. Published online June 1, 2008; DOI: https://doi.org/10.4093/kdj.2008.32.3.259

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Abstract PDF

BACKGROUND
Type 2 diabetes mellitus is a common, chronic and costly disease. Its prevalence is rapidly increasing worldwide. Diabetes has big economic burden mainly because of its chronic complications. We analyzed the annual direct medical costs of type 2 diabetic patients, including the costs associated with its complications in Korea retrospectively. METHODS: We enrolled 531 type 2 diabetic patients who had been treated in the 3 Tertiary Hospital in 2005. Clinical characteristics, duration of diabetes, modality of glycemic control, and presence of microvascular and macrovascular complications were assessed by the review of medical records. The annual direct medical costs were assessed using the hospital electronic database and included insurance covered and uncovered medical costs. RESULTS: The annual direct medical costs of type 2 diabetic patients without any complications was 1,184,563 won (95% CI for mean: 973,006~1,396,121 won). Compared to diabetic patients without complications, annual total medical costs increased 4.7-fold, 10.7-fold, and 8.8-fold in patients with microvascular complications, macrovascular complications and both complications, respectively. Hospitalization costs largely increased by 78.7-fold and 61.0-fold in patients with macrovascular complications and both complications, respectively. Major complications to increase medical costs were kidney transplantation (23.1-fold), dialysis (21.0-fold), PTCA or CABG (12.4-fold), and leg amputation (11.8-fold). The total medical costs dramatically increased according to the stage of diabetic retinopathy and nephropathy. CONCLUSION: Diabetic complications have a substantial impact on the direct medical costs of type 2 diabetic patients. The prevention of diabetic complications will benefit the patients as well as the overall healthcare expenditures.

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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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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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