Diabetes & Metabolism Journal

Original Article

Metabolic Risk/Epidemiology
Current Status of Low-Density Lipoprotein Cholesterol Target Achievement in Patients with Type 2 Diabetes Mellitus in Korea Compared with Recent Guidelines: Soo Jin Yun, In-Kyung Jeong, Jin-Hye Cha, Juneyoung Lee, Ho Chan Cho, Sung Hee Choi, SungWan Chun, Hyun Jeong Jeon, Ho-Cheol Kang, Sang Soo Kim, Seung-Hyun Ko, Gwanpyo Koh, Su Kyoung Kwon, Jae Hyuk Lee, Min Kyong Moon, Junghyun Noh, Cheol-Young Park, Sungrae Kim; Diabetes Metab J. 2022;46(3):464-475. Published online March 3, 2022; DOI: https://doi.org/10.4093/dmj.2021.0088

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Background
We evaluated the achievement of low-density lipoprotein cholesterol (LDL-C) targets in patients with type 2 diabetes mellitus (T2DM) according to up-to-date Korean Diabetes Association (KDA), European Society of Cardiology (ESC)/European Atherosclerosis Society (EAS), and American Diabetes Association (ADA) guidelines.
Methods
This retrospective cohort study collected electronic medical record data from patients with T2DM (≥20 years) managed by endocrinologists from 15 hospitals in Korea (January to December 2019). Patients were categorized according to guidelines to assess LDL-C target achievement. KDA (2019): Very High-I (atherosclerotic cardiovascular disease [ASCVD]) <70 mg/dL; Very High-II (target organ damage [TOD], or cardiovascular risk factors [CVRFs]) <70 mg/dL; high (others) <100 mg/dL. ESC/EAS (2019): Very High-I (ASCVD): <55 mg/dL; Very High-II (TOD or ≥3-CVRF) <55 mg/dL; high (diabetes ≥10 years without TOD plus any CVRF) <70 mg/dL; moderate (diabetes <10 years without CVRF) <100 mg/dL. ADA (2019): Very High-I (ASCVD); Very High-II (age ≥40+ TOD, or any CVRF), for high intensity statin or statin combined with ezetimibe.
Results
Among 2,000 T2DM patients (mean age 62.6 years; male 55.9%; mean glycosylated hemoglobin 7.2%) ASCVD prevalence was 24.7%. Of 1,455 (72.8%) patients treated with statins, 73.9% received monotherapy. According to KDA guidelines, LDL-C target achievement rates were 55.2% in Very High-I and 34.9% in Very High-II patients. With ESC/EAS guidelines, target attainment rates were 26.6% in Very High-I, 15.7% in Very High-II, and 25.9% in high risk patients. Based on ADA guidelines, most patients (78.9%) were very-high risk; however, only 15.5% received high-intensity statin or combination therapy.
Conclusion
According to current dyslipidemia management guidelines, LDL-C goal achievement remains suboptimal in Korean patients with T2DM.

Citations

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Kyung Ae Lee
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Association between carotid atherosclerosis and presence of intracranial atherosclerosis using three-dimensional high-resolution vessel wall magnetic resonance imaging in asymptomatic patients with type 2 diabetes
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Response

Status of Diabetic Neuropathy in Korea: A National Health Insurance Service-National Sample Cohort Analysis (2006 to 2015) (Diabetes Metab J 2021;45:115-9): Seong-Su Moon, Chong Hwa Kim, Seon Mee Kang, Eun Sook Kim, Tae Jung Oh, Jae-Seung Yun, Ho Chan Cho, Dae Jung Kim, Tae Sun Park; Diabetes Metab J. 2021;45(3):459-460. Published online May 25, 2021; DOI: https://doi.org/10.4093/dmj.2021.0084

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Comorbidity Patterns and Management in Inpatients with Endocrine Diseases by Age Groups in South Korea: Nationwide Data
Sung-Soo Kim, Hun-Sung Kim
Journal of Personalized Medicine.2023; 14(1): 42. CrossRef

Brief Report

Complications
Status of Diabetic Neuropathy in Korea: A National Health Insurance Service-National Sample Cohort Analysis (2006 to 2015): Seong-Su Moon, Chong Hwa Kim, Seon Mee Kang, Eun Sook Kim, Tae Jung Oh, Jae-Seung Yun, Ho Chan Cho, Dae Jung Kim, Tae Sun Park; Diabetes Metab J. 2021;45(1):115-119. Published online December 18, 2020; DOI: https://doi.org/10.4093/dmj.2020.0120

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This report presents the status of diabetic neuropathy (DN) in Korea as determined using a National Health Insurance ServiceNational Sample Cohort (NHIS-NSC). Annual prevalences of DN were estimated by age and gender using descriptive statistics. Pharmacological treatments for DN were also analyzed. The annual prevalence of DN increased from 24.9% in 2006 to 26.6% in 2007, and thereafter, gradually subsided to 20.8% in 2015. In most cases, pharmacological treatments involved a single drug, which accounted for 91.6% of total prescriptions in 2015. The most commonly used drugs (in decreasing order) were thioctic acid, an anti-convulsive agent, or a tricyclic antidepressant. In conclusion, the prevalence of DN decreased over the 10-year study period. Thioctic acid monotherapy was usually prescribed for DN. To reduce the socio-economic burden of DN, more attention should be paid to the diagnosis of this condition and to the appropriate management of patients.

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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
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Pharmacological and Nonpharmacological Treatments for Painful Diabetic Peripheral Neuropathy
Han Na Jang, Tae Jung Oh
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Are herbal medicines alone or in combination for diabetic peripheral neuropathy more effective than methylcobalamin alone? A systematic review and meta-analysis
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Complementary Therapies in Clinical Practice.2022; 49: 101657. CrossRef
Pathogenesis and Treatment of Diabetic Peripheral Neuropathy
Seon Mee Kang
The Journal of Korean Diabetes.2022; 23(4): 222. CrossRef
Status of Diabetic Neuropathy in Korea: A National Health Insurance Service-National Sample Cohort Analysis (2006 to 2015) (Diabetes Metab J 2021;45:115-9)
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Status of Diabetic Neuropathy in Korea: A National Health Insurance Service-National Sample Cohort Analysis (2006 to 2015) (Diabetes Metab J 2021;45:115-9)
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Original Articles

The Relationship among Homocysteine, Bilirubin, and Diabetic Retinopathy: Ho Chan Cho; Diabetes Metab J. 2011;35(6):595-601. Published online December 26, 2011; DOI: https://doi.org/10.4093/dmj.2011.35.6.595

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Background

Diabetic retinopathy is a common microvascular complication of diabetes mellitus (DM) and the leading cause of blindness in adults. Homocysteine, a risk factor with toxic effects on vascular endothelial cells, and bilirubin, a protectant with antioxidant and anti-inflammatory properties on the vasculature, have been reported to be linked to vaso-occlusive disorders. Therefore, the author of the present study investigated the association between the levels of plasma homocysteine and serum total bilirubin and the incidence of diabetic retinopathy as a chronic microvascular complication in patients with type 2 diabetes mellitus (T2DM).

Methods

A total of 102 patients with T2DM who visited our hospital from January 2009 to January 2010 were assessed.

Results

Of the 102 patients, the prevalence of diabetic retinopathy was 67 cases (65.7%) according to clinical ophthalmic examination. The duration of DM (P<0.001), age (P=0.003), fasting blood glucose (P=0.045) and urine albumin-creatinine ratio (P=0.015) in univariate analysis and plasma homocysteine level (P=0.038), duration of DM (P=0.001), and total bilirubin level (P=0.012) in multiple logistic regression analysis were statistically significantly associated with the incidence of diabetic retinopathy.

Conclusion

The present study indicates that homocysteine and bilirubin may be useful biomarkers for increased risk of diabetic retinopathy since retinopathy in patients with T2DM was linked to higher plasma homocysteine level and decreased serum total bilirubin level.

Citations

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Role of hyperhomocysteinemia in the progression of diabetic retinopathy
Pooja H V, Lakshmi M S
Indian Journal of Clinical and Experimental Ophthalmology.2024; 10(1): 160. CrossRef
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Dima Samer Ali, Samuel O. Sofela, Muhammedin Deliorman, Pavithra Sukumar, Ma-sum Abdulhamid, Sherifa Yakubu, Ciara Rooney, Ryan Garrod, Anoop Menachery, Rabih Hijazi, Hussein Saadi, Mohammad A. Qasaimeh
Lab on a Chip.2024; 24(11): 2906. CrossRef
Serum Total Bilirubin and Oxidative Stress Status in Diabetic Retinopathy – A Hospital-Based Observational Study
Prabhavathi K, Mamatha Kunder, Shashidhar K.N, Kanthamani K, Raveesha A
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Plasma homocysteine is associated with nonproliferative retinopathy in patients with type 2 diabetes without renal disease
Martina Tomić, Romano Vrabec, Spomenka Ljubić, Tomislav Bulum, Dario Rahelić
Diabetes & Metabolic Syndrome: Clinical Research & Reviews.2022; 16(1): 102355. CrossRef
Blood Viscosity in Subjects With Type 2 Diabetes Mellitus: Roles of Hyperglycemia and Elevated Plasma Fibrinogen
Jiehui Sun, Keqin Han, Miao Xu, Lujuan Li, Jin Qian, Li Li, Xuejin Li
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Biliverdin/Bilirubin Redox Pair Protects Lens Epithelial Cells against Oxidative Stress in Age-Related Cataract by Regulating NF-κB/iNOS and Nrf2/HO-1 Pathways
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Oxidative Medicine and Cellular Longevity.2022; 2022: 1. CrossRef
Homocysteine and diabetes: Role in macrovascular and microvascular complications
Emir Muzurović, Ivana Kraljević, Mirsala Solak, Siniša Dragnić, Dimitri P. Mikhailidis
Journal of Diabetes and its Complications.2021; 35(3): 107834. CrossRef
Quantifying Fibrinogen-Dependent Aggregation of Red Blood Cells in Type 2 Diabetes Mellitus
Yixiang Deng, Dimitrios P. Papageorgiou, Xuejin Li, Nikolaos Perakakis, Christos S. Mantzoros, Ming Dao, George Em Karniadakis
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Association between serum total bilirubin levels and the risk of type 2 diabetes mellitus
Min Yang, Changlin Ni, Baocheng Chang, Zhenhuan Jiang, Yanjuan Zhu, Yunzhao Tang, Zhu Li, Chenguang Li, Bin Li
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Elevated Serum Total Bilirubin Concentrations Are Negatively Associated with Diabetic Retinopathy among the Chinese Northeastern Population
Dan Zhang, Wei Zhang, Shi Jin, Wei Wang, Dan Guo, Lu Wang
International Journal of Endocrinology.2018; 2018: 1. CrossRef
Serum bilirubin levels are negatively associated with diabetic retinopathy in patients with type 1 diabetes and normal renal function
Tomislav Bulum, Martina Tomić, Lea Duvnjak
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The Association between Serum Bilirubin Level and Electrochemical Skin Conductance in Chinese Patients with Type 2 Diabetes
Fei Mao, Xiaoming Zhu, Bin Lu, Yiming Li
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F.A. Ganjifrockwala, J.T. Joseph, G. George
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Jiaokun Jia, Anxin Wang, Jing Wang, Jianwei Wu, Xiujuan Yan, Yong Zhou, Shengyun Chen, Xingquan Zhao
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Silvia Gazzin, Libor Vitek, Jon Watchko, Steven M. Shapiro, Claudio Tiribelli
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Bo Zhu, Xiaomei Wu, Kang Ning, Feng Jiang, Lu Zhang, Demetrios G. Vavvas
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Serum total bilirubin concentration is negatively associated with increasing severity of retinopathy in patients with type 2 diabetes mellitus
Risa Sekioka, Masami Tanaka, Takeshi Nishimura, Hiroshi Itoh
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Plasma Homocysteine is Associated with Retinopathy in Type 1 Diabetic Patients in the Absence of Nephropathy
Tomislav Bulum, Kristina Blaslov, Lea Duvnjak
Seminars in Ophthalmology.2014; : 1. CrossRef
Relationship between homocysteine level and diabetic retinopathy: a systematic review and meta-analysis
Chong Xu, Yan Wu, Guodong Liu, Xiaoqiang Liu, Fang Wang, Jing Yu
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Decreased Serum Bilirubin Is Associated With Silent Cerebral Infarction
Rui-Yan Li, Zhi-Gang Cao, Ji-Rong Zhang, Ying Li, Rui-Tao Wang
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Syeda Sadia Najam, Jichao Sun, Jie Zhang, Min Xu, Jieli Lu, Kan Sun, Mian Li, Tiange Wang, Yufang Bi, Guang Ning
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Marc Lapointe, Paul Poirier, Julie Martin, Marjorie Bastien, Audrey Auclair, Katherine Cianflone
Cardiovascular Diabetology.2014;[Epub] CrossRef
Homocysteine Serum Levels in Diabetic Patients with Non Proliferative, Proliferative and without Retinopathy
Giulia Malaguarnera, Caterina Gagliano, Maria Giordano, Salvatore Salomone, Marco Vacante, Claudio Bucolo, Filippo Caraci, Michele Reibaldi, Filippo Drago, Teresio Avitabile, Massimo Motta
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Mechanisms of Diabetic Complications
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The Association between Serum GGT Concentration and Diabetic Peripheral Polyneuropathy in Type 2 Diabetic Patients: Ho Chan Cho; Korean Diabetes J. 2010;34(2):111-118. Published online April 30, 2010; DOI: https://doi.org/10.4093/kdj.2010.34.2.111

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Background

Diabetic peripheral polyneuropathy (DPP) is one of the common complications of diabetes mellitus (DM) and can lead to foot ulcers or amputation. The pathophysiology of DPP includes several factors such as metabolic, vascular, autoimmune, oxidative stress and neurohormonal growth-factor deficiency and recent studies have suggested the use of serum gamma-glutamyl transferase (GGT) as an early marker of oxidative stress. Therefore, we investigated whether serum GGT may be useful in predicting DPP.

Methods

We assessed 90 patients with type 2 DM who were evaluated for the presence of DPP using clnical neurologic examinations including nerve conduction velocity studies. We evaluated the association between serum GGT and the presence of DPP.

Results

The prevalence of DPP was 40% (36 cases) according to clinical neurological examinations. The serum GGT concentration was significantly elevated in type 2 diabetic patients with DPP compared to patients without DPP (P < 0.01). There were other factors significantly associated with DPP including smoking (P = 0.019), retinopathy (P = 0.014), blood pressure (P < 0.05), aspartate aminotransferase (P = 0.022), C-reactive protein (P = 0.036) and urine microalbumin/creatinine ratio (P = 0.004). Serum GGT was independently related with DPP according to multiple logistic analysis (P < 0.01).

Conclusion

This study shows that increased levels of serum GGT may have important clinical implications in the presence of DPP in patients with type 2 diabetes.

Citations

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A Longitudinal Increase in Serum Gamma-Glutamyl Transferase Levels, but Not in Alanine Aminotransferase Levels, Improves the Prediction of Risk of Impaired Fasting Glucose in Male
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Early Biomarkers of Neurodegenerative and Neurovascular Disorders in Diabetes
Aleksandra Gasecka, Dominika Siwik, Magdalena Gajewska, Miłosz J. Jaguszewski, Tomasz Mazurek, Krzysztof J. Filipiak, Marek Postuła, Ceren Eyileten
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Angiotensin-converting enzyme gene single polymorphism as a genetic biomarker of diabetic peripheral neuropathy: longitudinal prospective study
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Y. Lin, Y. Xu, G. Chen, B. Huang, J. Yao, Z. Chen, L. Yao, F. Lin, Y. Qiao, Z. Chen, S. Zhu, H. Huang, J. Wen
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The Effect of Chronic High Glucose Concentration on Endoplasmic Reticulum Stress in INS-1 Cells.: Mi Kyung Kim, Hye Young Seo, Tae Sung Yun, Nam Kyung Kim, Yu Jin Hah, Yun Jung Kim, Ho Chan Cho, Young Yun Jang, Hye Soon Kim, Seong Yeol Ryu, In Kyu Lee, Keun Gyu Park; Korean Diabetes J. 2008;32(2):112-120. Published online April 1, 2008; DOI: https://doi.org/10.4093/kdj.2008.32.2.112

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Abstract PDF: BACKGROUND
The highly developed endoplasmic reticulum (ER) structure is one of the characteristic features of pancreatic beta-cells. Recent study showed that ER stress causes beta-cell dysfunction. However, little is known about the effects of high glucose concentration on induction of ER stress in pancreatic beta-cells. Therefore, this study was designed to evaluate whether exposure of high glucose concentration in rat insulinoma cell line, INS-1 cell induces ER stress and whether ER stress decreases insulin gene expression. METHODS: The effect of 30 mM glucose on insulin expression and secretion in INS-1 cells was evaluated by Northern blot analysis and glucose-stimulated insulin secretion (GSIS). Cell viability was evaluated by XTT assay. The effect of 30 mM glucose on phosphorylation of eIF2alpha and CHOP expression, which are markers of ER stress were evaluated by Western blot analysis. RT-PCR analysis was performed to determine whether high glucose concentration induces XBP-1 splicing. To investigate whether ER stress decreases insulin gene expression, the effect of tunicamycin on insulin mRNA expression was evaluated by Northern blot analysis. RESULTS: The prolonged exposure of INS-1 cells with the 30 mM glucose concentration decreased insulin mRNA expression in a time dependent manner and impaired GSIS while did not influence on cell viability. 30 mM glucose increased phosphorylation of eIF2alpha, XBP-1 splicing and CHOP expression in INS-1 cells. Tunicamycin-treated INS-1 increased XBP-1 splicing and decreased insulin mRNA expression in a dose dependent manner. CONCLUSION: This study showed that prolonged exposure of INS-1 with high glucose concentration induces ER stress and ER stress decreases insulin gene expression. Further studies about underlying molecular mechanism by which ER stress induces beta-cell dysfunction are needed.

Case Report

A Case of Cured Diabetes Mellitus after Occult Malignant Pheochromocytoma Removal.: Ho Chan Cho, Hye Soon Kim, Yoon Jung Kim, Yu Jin Hah, Nam Keong Kim, Mi Kyung Kim, Keun Gyu Park, Yong Hoon Kim, Sun Young Kwon; Korean Diabetes J. 2007;31(6):520-524. Published online November 1, 2007; DOI: https://doi.org/10.4093/jkda.2007.31.6.520

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Abstract PDF

Pheochromocytoma is characterized by a combination of various clinical manifestations that include the classic triad of severe headache, palpitations and diaphoresis. In addition, hyperglycemia can be caused by overproduction of catecholamines, which are secreted by a catecholamine-secreting neoplasm of adrenal or extra-adrenal chromaffin tissue. We encountered a case of diabetes with an occult malignant adrenal pheochromocytoma, who did not have any classic manifestations. A 37-year-old male was admitted because of polydipsia, polyuria, and weight loss. Fasting blood glucose level was 497 mg/dL, hemoglobin A1c level was 15%, and diabetic retinopathy and peripheral polyneuropathy were also accompanied. Incidentally, right adrenal mass was detected by ultrasonography of abdomen. Urinary excretion of total metanephrine and epinephrine were elevated. Adrenal CT showed a 7.1 cm sized right adrenal cystic mass with enhancing solid portion and hemorrhagic content. The scan with 123I-MIBG revealed the cystic mass with increased rim uptake in the region of right adrenal gland. After removal of the tumor, the increased levels of catecholamine were normalized. Moreover, blood glucose level was normalized without administration of insulin or oral hypoglycemic agents. The pathologic examination showed that the neoplasm was a malignant adrenal pheochromocytoma. We report this case that diabetes was cured after removal of malignant tumor with literature review at first in Korea.

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Pheochromocytoma with Markedly Abnormal Liver Function Tests and Severe Leukocytosis
Chai Ryoung Eun, Jae Hee Ahn, Ji A Seo, Nan Hee Kim
Endocrinology and Metabolism.2014; 29(1): 83. CrossRef

Original Articles

The Effect of alpha-lipoic Acid on Endothelial Dysfunction Induced by Intralipid Infusion in Healthy Volunteers.: Dong Wook Lee, Mi Jung Kim, Hye Soon Kim, Tae Sung Yun, Ho Chan Cho, Sang Jun Lee, Seung Ho Hur, Kyo Cheol Mun, Yong Won Cho, Jae Hoon Bae, In Kyu Lee; Korean Diabetes J. 2002;26(5):336-346. Published online October 1, 2002

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Abstract PDF: BACKGROUND
Endothelial dysfunciton has been proposed as an early manifestation of atherogenesis. Recently, emerging evidence suggests that hypertriglyceridemia and elevated free fatty acid are important risk factors in the development of atherosclerosis, probably through an increased oxidative stress. To clarify the hypothesis, we evaluated the effect of alpha-lipoic acid (ALA) on the endothelial dysfunction induced by intralipid infusion in healthy volunteers. METHODS: Hypertriglyceridemia and elevated free fatty acids was induced by infusion of intralipid. FMD (Flow-mediated dilation) of the brachial artery was investigated noninvasively by a high-resolution ultrasound technique in 13 young, healthy men without risk factors for coronary heart disease. RESULTS: Plasma triglyceride, free fatty acid and the superoxide anion were increased from 61.7+/-28.8 to 332.6+/-202.5 mg/dL, from 330.7+/-131.1 to 1267.0+/-486.2 microEq/L and from 6.6+/-2.2 to 8.7+/-1.5 X 10(-7)nmol/10(6)cells/30min (vs. basal p<0.001), respectively, following infusion of the intralipid. The FMD was decreased from 10.1+/-3.3 to 7.7+/-3.7% (vs. basal p<0.01) following infusion of the intralipid. After treatment with ALA, the increase in the FMD and the decrease in superoxide anion were significant. CONCLUSION: Acute hypertriglyceridemia, induced by intralipid infusion, is implicated in endothelial dysfunction. This endothelial dysfunction was reversed by treatment with ALA. These results suggest that chronic and repeated hypertriglyceridemia may play important roles in the development of atherosclerosis probably by increasing oxidative stress.

The Effect of Alpha-lipoic Acid on Endothelial Dysfunction in Postmenopausal Uncomplicated Type 2 Diabetes.: Ho Chan Cho, Sang Jun Lee, Mi Jung Kim, Hye Sun Kim, Tae Sung Yun, Sung Jae Kim, Sang Hyon Kim, Seung Ho Hur, Kyo Chul Moon, Jae Hoon Bae, In Kyu Lee; Korean Diabetes J. 2002;26(4):242-252. Published online August 1, 2002

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Abstract PDF: BACKGROUND
Recently, increased oxidative stress has been proposed as a major cause of vascular complications of patients with diabetes mellitus. Increased generation of oxygen free radicals in patients with diabetes mellitus could deplete cellular antioxidants and inactivate endothelial dependent vasodilating factor (EDRF), such as nitric oxide (NO). The purpose of this study was to evaluate whether the antioxidant alpha-lipoic acid (ALA) is effective in endothelial dysfunction of brachial artery, which induced by increased oxidative stress in postmenopausal diabetic women using high resolution ultrasound technique and initial reaction time (IRT) measurement. METHODS: We enrolled 11 menopausal women (mean age, 56.5+/-5.1 years) with uncomplicated type 2 diabetes. All patients were taking 1200 mg of ALA (Thioctacid(R), Bukwang, Korea). We measured of superoxide anion (O2-) in neutrophils as a marker of oxidative stress. Flow-mediated dilation (FMD) was measured using a high-resolution ultrasound. RESULTS: After treatment of ALA, fasting blood glucose was decreased significantly, the endothelium-dependent vasodilation of the brachial artery was increased, and O2- production was also decreased significantly. CONCLUSION: These results show that short term ALA treatment could improve the endothelial dysfunction in patients with type 2 diabetes mellitus. This improvement might be related with the antioxidants effect of ALA.

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