Diabetes & Metabolism Journal

Original Articles

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

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

Metabolic Risk/Epidemiology
Sex Differences of Visceral Fat Area and Visceral-to-Subcutaneous Fat Ratio for the Risk of Incident Type 2 Diabetes Mellitus: Eun Hee Kim, Hong-Kyu Kim, Min Jung Lee, Sung-Jin Bae, Jaewon Choe, Chang Hee Jung, Chul-Hee Kim, Joong-Yeol Park, Woo Je Lee; Diabetes Metab J. 2022;46(3):486-498. Published online November 18, 2021; DOI: https://doi.org/10.4093/dmj.2021.0095

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Background
This study aimed to determine the optimal cut-off values of visceral fat area (VFA) and visceral-to-subcutaneous fat ratio (VSR) for predicting incident type 2 diabetes mellitus (T2DM).
Methods
A total of 10,882 individuals (6,835 men; 4,047 women) free of T2DM at baseline aged between 30 and 79 years who underwent abdominal computed tomography scan between 2012 and 2013 as a part of routine health check-ups were included and followed. VFA, subcutaneous fat area, and VSR on L3 vertebral level were measured at baseline.
Results
During a median follow-up of 4.8 years, 730 (8.1% for men; 4.3% for women) incident cases of T2DM were identified. Receiver operating characteristic curve analysis showed that the optimal cut-off values of VFA and VSR for predicting incident T2DM were 130.03 cm² and 1.08 in men, respectively, and 85.7 cm² and 0.48 in women, respectively. Regardless of sex, higher VFA and VSR were significantly associated with a higher risk of incident T2DM. Compared with the lowest quartiles of VFA and VSR, the highest quartiles had adjusted odds ratios of 2.62 (95% confidence interval [CI], 1.73 to 3.97) and 1.55 (95% CI, 1.14 to 2.11) in men, respectively, and 32.49 (95% CI, 7.42 to 142.02) and 11.07 (95% CI, 3.89 to 31.50) in women, respectively.
Conclusion
Higher VFA and VSR at baseline were independent risk factors for the development of T2DM. Sex-specific reference values for visceral fat obesity (VFA ≥130 cm² or VSR ≥1.0 in men; VFA ≥85 cm² or VSR ≥0.5 in women) are proposed for the prediction of incident T2DM.

Citations

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Mohammad Jalali, Zahra Bahadoran, Parvin Mirmiran, Fereidoun Azizi, Farhad Hosseinpanah
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Huan Hu, Tohru Nakagawa, Toru Honda, Shuichiro Yamamoto, Tetsuya Mizoue
BMJ Open Diabetes Research & Care.2024; 12(1): e003680. CrossRef
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Zahra Bahadoran, Parvin Mirmiran, Asghar Ghasemi
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Yu‐Hsuan Chang, Chin‐Sung Chang, Chieh‐Yu Liu, Yin‐Fan Chang, Shiow‐Ching Shun
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Fan Wu, Yanlan Liu, Chenying Lin, Nahal Haghbin, Longfei Xia, Yaoshuang Li, Tong Chen, Huina Qiu, Weiran Jiang, Jingbo Li, Jingna Lin
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Cancers.2023; 15(4): 1156. CrossRef
MEDICINAL BIOMAGNETISM FOR THE TREATMENT OF OBESITY
Ana Vergínia Campagnollo Bueno, Michelli Gonçalves Seneda, Ângela Mara Rambo, Ana Clara Campagnolo Gonçalves Toledo, Caroline Cabral de Azevedo, Adriane Viapiana Bossa
Health and Society.2023; 3(01): 411. CrossRef
Cumulative exposure to metabolic syndrome in a national population-based cohort of young adults and sex-specific risk for type 2 diabetes
Min-Kyung Lee, Jae-Hyuk Lee, Seo Young Sohn, Jiyeon Ahn, Oak-Kee Hong, Mee-Kyoung Kim, Ki-Hyun Baek, Ki-Ho Song, Kyungdo Han, Hyuk-Sang Kwon
Diabetology & Metabolic Syndrome.2023;[Epub] CrossRef
The correlation between visceral fat/subcutaneous fat area ratio and monocyte/high-density lipoprotein ratio in patients with type 2 diabetes mellitus and albuminuria
Haiyan Lin, Jun Zhu, Chen Zheng, Xiaoming Xu, Shandong Ye
Journal of Diabetes and its Complications.2023; 37(11): 108521. CrossRef
Effects of the abdominal fat distribution on the relationship between exposure to air pollutants and thyroid hormones among Korean adult males
Hyun-Jin Kim, Byungmi Kim, Seyoung Kim, Hyuktae Kwon, Jae Moon Yun, Belong Cho, Jin-Ho Park
European Journal of Medical Research.2023;[Epub] CrossRef
Association of Visceral Fat Obesity, Sarcopenia, and Myosteatosis with Non-Alcoholic Fatty Liver Disease without Obesity
Hong-Kyu Kim, Sung-Jin Bae, Min Jung Lee, Eun Hee Kim, Hana Park, Hwi Seung Kim, Yun Kyung Cho, Chang Hee Jung, Woo Je Lee, Jaewon Choe
Clinical and Molecular Hepatology.2023; 29(4): 987. CrossRef
Visceral adipose tissue reference data computed for GE HealthCare DXA from the National Health and Nutrition Examination Survey data set
Jonathan P. Bennett, Brandon K. Quon, Bo Fan, En Liu, Leila Kazemi, Rosa C. Villegas‐Valle, Raj Ahgun, Xian‐pin Wu, Hou‐De Zhou, Ying Lu, John A. Shepherd
Obesity.2023; 31(12): 2947. CrossRef
Comparison of bioelectrical body and visceral fat indices and anthropometric measures in relation to type 2 diabetes by sex among Chinese adults, a cross-sectional study
Jiangshan He, Binbin Zhang, Yaqi Fan, Yuxue Wang, Mianzhi Zhang, Chunjun Li, Li Zhang, Pei Guo, Minying Zhang
Frontiers in Public Health.2023;[Epub] CrossRef
The predictive significance of lipid accumulation products for future diabetes in a non-diabetic population from a gender perspective: an analysis using time-dependent receiver operating characteristics
Jiajun Qiu, Maobin Kuang, Yang Zou, Ruijuan Yang, Qing Shangguan, Dingyang Liu, Guotai Sheng, Wei Wang
Frontiers in Endocrinology.2023;[Epub] CrossRef
Cellular interplay between cardiomyocytes and non-myocytes in diabetic cardiomyopathy
Ren Jie Phang, Rebecca H. Ritchie, Derek J. Hausenloy, Jarmon G. Lees, Shiang Y. Lim
Cardiovascular Research.2022;[Epub] CrossRef
Implication of Sex Differences in Visceral Fat for the Assessment of Incidence Risk of Type 2 Diabetes Mellitus
Sang Hyeon Ju, Hyon-Seung Yi
Diabetes & Metabolism Journal.2022; 46(3): 414. CrossRef
Visceral fat area and body fat percentage measured by bioelectrical impedance analysis correlate with glycometabolism
Shuying Li, Shaoping Li, Jie Ding, Weihong Zhou
BMC Endocrine Disorders.2022;[Epub] CrossRef
The Demographic Specific Abdominal Fat Composition and Distribution Trends in US Adults from 2011 to 2018
Furong Xu, Jacob E. Earp, Bryan J. Blissmer, Ingrid E. Lofgren, Matthew J. Delmonico, Geoffrey W. Greene
International Journal of Environmental Research and Public Health.2022; 19(19): 12103. CrossRef
Visceral Obesity Is a More Important Factor for Colorectal Adenomas than Skeletal Muscle or Body Fat
Ji Yeon Seo, Yoo Min Han, Su Jin Chung, Seon Hee Lim, Jung Ho Bae, Goh Eun Chung
Cancers.2022; 14(21): 5256. CrossRef
Recent Advances in Visceral Obesity and Related Diseases
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Advances in Clinical Medicine.2022; 12(12): 11686. CrossRef
Gender differences in the ideal cutoffs of visceral fat area for predicting MAFLD in China
Pingping Yu, Huachao Yang, Xiaoya Qi, Ruixue Bai, Shouqin Zhang, Jianping Gong, Ying Mei, Peng Hu
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Cardiovascular Risk/Epidemiology
Clinical Significance of Body Fat Distribution in Coronary Artery Calcification Progression in Korean Population: Heesun Lee, Hyo Eun Park, Ji Won Yoon, Su-Yeon Choi; Diabetes Metab J. 2021;45(2):219-230. Published online October 28, 2020; DOI: https://doi.org/10.4093/dmj.2019.0161; Correction in: Diabetes Metab J 2021;45(6):974

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Graphical Abstract Abstract PDF Supplementary Material PubReader ePub

Background
Although obesity differs according to ethnicity, it is globally established as a solid risk factor for cardiovascular disease. However, it is not fully understood how obesity parameters affect the progression of coronary artery calcification (CAC) in Korean population. We sought to evaluate the association of obesity-related parameters including visceral adipose tissue (VAT) measurement and CAC progression.
Methods
This retrospective observational cohort study investigated 1,015 asymptomatic Korean subjects who underwent serial CAC scoring by computed tomography (CT) with at least 1-year interval and adipose tissue measurement using non-contrast CT at baseline for a routine checkup between 2003 and 2015. CAC progression, the main outcome, was defined as a difference of ≥2.5 between the square roots of the baseline and follow-up CAC scores using Agatston units.
Results
During follow-up (median 39 months), 37.5% of subjects showed CAC progression of a total population (56.4 years, 80.6% male). Body mass index (BMI) ≥25 kg/m², increasing waist circumferences (WC), and higher VAT/subcutaneous adipose tissue (SAT) area ratio were independently associated with CAC progression. Particularly, predominance of VAT over SAT at ≥30% showed the strongest prediction for CAC progression (adjusted hazard ratio, 2.20; P<0.001) and remained of prognostic value regardless of BMI or WC status. Further, it provided improved risk stratification of CAC progression beyond known prognosticators.
Conclusion
Predominant VAT area on CT is the strongest predictor of CAC progression regardless of BMI or WC in apparently healthy Korean population. Assessment of body fat distribution may be helpful to identify subjects at higher risk.

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Metabolic Risk/Epidemiology
Association between the Thigh Muscle and Insulin Resistance According to Body Mass Index in Middle-Aged Korean Adults: Ji Eun Heo, Jee-Seon Shim, Hokyou Lee, Hyeon Chang Kim; Diabetes Metab J. 2020;44(3):446-457. Published online April 16, 2020; DOI: https://doi.org/10.4093/dmj.2019.0110

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Background

We examined the associations between thigh muscle area (TMA) and insulin resistance (IR) according to body mass index (BMI) in middle-aged Korean general population.

Methods

TMA was measured using quantitative computed tomography and corrected by body weight (TMA/Wt) in 1,263 men, 788 premenopausal women, and 1,476 postmenopausal women all aged 30 to 64 years. The tertiles of TMA/Wt were calculated separately for men and for premenopausal and postmenopausal women. Homeostatic model assessment for insulin resistance (HOMA-IR) was performed using fasting blood glucose and insulin levels, and increased IR was defined according to sex-specific, top quartiles of HOMA-IR. Associations between the TMA/Wt tertiles and increased IR according to the BMI categories (<25 and ≥25 kg/m²) were assessed using multivariable logistic regression analysis.

Results

In men with higher BMIs, but not in those with lower BMIs, the presence of an increased IR had significantly higher odds ratios in the lower TMA/Wt tertiles, even after adjustment for visceral fat area. However, in premenopausal and postmenopausal women, there was no significant inverse association between TMA/Wt tertiles and increased IR, regardless of BMI category.

Conclusion

Our findings suggest that the thigh muscle is inversely associated with IR in men, particularly in those with higher BMIs.

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Review

Clinical Diabetes & Therapeutics
Diabetes and Subclinical Coronary Atherosclerosis: Chang Hoon Lee, Seung-Whan Lee, Seong-Wook Park; Diabetes Metab J. 2018;42(5):355-363. Published online October 22, 2018; DOI: https://doi.org/10.4093/dmj.2018.0041

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Abstract PDF PubReader

It is well known that diabetic patients have a high risk of cardiovascular events, and although there has been a tremendous effort to reduce these cardiovascular risks, the incidence of cardiovascular morbidity and mortality in diabetic patients remains high. Therefore, the early detection of coronary artery disease (CAD) is necessary in those diabetic patients who are at risk of cardiovascular events. Significant medical and radiological advancements, including coronary computed tomography angiography (CCTA), mean that it is now possible to investigate the characteristics of plaques, instead of solely evaluating the calcium level of the coronary artery. Recently, several studies reported that the prevalence of subclinical coronary atherosclerosis (SCA) is higher than expected, and this could impact on CAD progression in asymptomatic diabetic patients. In addition, several reports suggest the potential benefit of using CCTA for screening for SCA in asymptomatic diabetic patients, which might dramatically decrease the incidence of cardiovascular events. For these reasons, the medical interest in SCA in diabetic patients is increasing. In this article, we sought to review the results of studies on CAD in asymptomatic diabetic patients and discuss the clinical significance and possibility of using CCTA to screen for SCA.

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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
Ji Eun Jun, You-Cheol Hwang, Kyu Jeong Ahn, Ho Yeon Chung, Geon-Ho Jahng, Soonchan Park, In-Kyung Jeong, Chang-Woo Ryu
Diabetes Research and Clinical Practice.2022; 191: 110067. CrossRef
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Original Articles

Complications
Serum Total Bilirubin Levels Provide Additive Risk Information over the Framingham Risk Score for Identifying Asymptomatic Diabetic Patients at Higher Risk for Coronary Artery Stenosis: Jaechan Leem, Eun Hee Koh, Jung Eun Jang, Chang-Yun Woo, Jin Sun Oh, Min Jung Lee, Joon-Won Kang, Tae-Hwan Lim, Chang Hee Jung, Woo Je Lee, Joong-Yeol Park, Ki-Up Lee; Diabetes Metab J. 2015;39(5):414-423. Published online October 22, 2015; DOI: https://doi.org/10.4093/dmj.2015.39.5.414

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Background

The diagnosis of coronary artery disease (CAD) is often delayed in patients with type 2 diabetes. Serum total bilirubin levels are inversely associated with CAD. However, no studies have examined whether this can be used as a biochemical marker for identifying asymptomatic diabetic patients at higher risk for having obstructive CAD.

Methods

We performed a cross-sectional study of 460 consecutive asymptomatic patients with type 2 diabetes. All patients underwent coronary computed tomographic angiography, and their serum total bilirubin levels were measured. Obstructive CAD was defined as ≥50% diameter stenosis in at least one coronary artery.

Results

Serum total bilirubin tertiles showed an inverse association with the prevalence of obstructive CAD. In multivariate logistic regression analysis, the odds ratio for the highest versus the lowest tertile of total bilirubin was 0.227 (95% confidence interval [CI], 0.130 to 0.398), and an increment of 1 µmol/L in serum total bilirubin level was associated with a 14.6% decrease in obstructive CAD after adjustment for confounding variables. Receiver operating characteristic curve analysis showed that the area under the curve for the Framingham Risk Score (FRS) plus serum total bilirubin level was 0.712 (95% CI, 0.668 to 0.753), which is significantly greater than that of the FRS alone (P=0.0028).

Conclusion

Serum total bilirubin level is inversely associated with obstructive CAD and provides additive risk information over the FRS. Serum total bilirubin may be helpful for identifying asymptomatic patients with type 2 diabetes who are at higher risk for obstructive CAD.

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Diagnostic Accuracy of 64-Slice MDCT Coronary Angiography for the Assessment of Coronary Artery Disease in Korean Patients with Type 2 Diabetes: Jun Sung Moon, Ji Sung Yoon, Kyu Chang Won, Ihn-Ho Cho, Hyoung Woo Lee; Diabetes Metab J. 2013;37(1):54-62. Published online February 15, 2013; DOI: https://doi.org/10.4093/dmj.2013.37.1.54

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Background

A 64-slice multidetector computed tomography (MDCT) is well known to be a useful noninvasive form of angiography for the general population, but not for certain patients with diabetes. The aim of this study was to investigate the diagnostic accuracy and usefulness of 64-slice MDCT coronary angiography for detecting coronary artery disease in Korean patients with type 2 diabetes mellitus (T2DM).

Methods

A total of 240 patients were included, 74 of whom had type 2 diabetes (M:F=40:33; 41.8±9.5 years). We compared significant coronary stenosis (>50% luminal narrowing) in MDCT with invasive coronary angiography (ICA) by segment, artery, and patient. We also evaluated the influence of obesity and coronary calcium score on MDCT accuracy.

Results

Of the 4,064 coronary segments studied, 4,062 segments (T2DM=1,109) were assessed quantitatively by both MDCT and ICA, and 706 segments (T2DM=226) were detected as a significant lesion by ICA in all patients. Sensitivity, specificity, as well as positive and negative predictive values for the presence of significant stenosis in T2DM were: by segment, 89.4%, 96.4%, 85.8%, and 97.4%, respectively; by artery (n=222), 95.1%, 92.9%, 94.4%, and 93.8%, respectively; by patients (n=74), 98.4%, 100.0%, 98.4%, and 90.0%, respectively. Regardless of presence of diabetes, there was no significant difference in diagnostic accuracy. Obesity (≥25 kg/m²) and coronary calcium score did not also affect the diagnostic accuracy of MDCT.

Conclusion

The 64-slice MDCT coronary angiography was found to have similar diagnostic accuracy with ICA, regardless of diabetes. These results suggest MDCT may be helpful to reduce unnecessary invasive studies for patients with diabetes.

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The Correlation Between Visceral Fat Distance Measured by Ultrasonography and Visceral Fat Amount by Computed Tomography in Type 2 Diabetes.: Eui Dal Jung, Duck Soo Chung, Ji Yun Lee; Korean Diabetes J. 2008;32(5):418-427. Published online October 1, 2008; DOI: https://doi.org/10.4093/kdj.2008.32.5.418

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BACKGROUND
Visceral adipose tissue accumulation highly correlates with metabolic abnormalities and cardiovascular disease. Computed tomography (CT) is considered to be the standard method for visceral fat evaluation, but it is not used as a routine procedure. Ultrasonography (US) is a safe method, fairly inexpensive and widely available modality for measuring abdominal fat thickness. The aim of this study was to investigate the correlation between the intra-abdominal fat distance by US measurement and the visceral fat amount by CT and cardiovascular risk factors and to evaluate whether the intra-abdominal fat distance is better correlate with visceral fat amount by CT than other anthropometric parameters and to assess the cut-off value of intra-abdominal fat distance for visceral obesity in type 2 diabetic patients. METHODS: We obtained abdominal subcutaneous and intra-abdominal fat distance by using a high-resolution US (HDI 5000, ATL, Phillps, USA) at 1 cm above umbilical level in one hundred twenty-eight type 2 diabetic patients. CT scan (Light Speed plus, GE, USA) for the measurement of subcutaneous and intra-abdominal visceral fat area was also performed in the supine position at the L4-5 level. Lean body mass and % body fat were measured in a bioimpedance using DSM (Direct Segmental Measurement by 8-point electrode) method (InBody 3.0, Biospace, Seoul, Korea). We measured patient's height, weight, BMI (Body mass index), waist circumference, WHR(Waist-hip ratio) and blood pressure and also measured fasting blood glucose, HbA1c and lipid profiles. RESULTS: Abdominal subcutaneous and visceral fat distance measured by US is 2.05 +/- 0.52 cm, 4.43 +/- 1.54 cm, respectively. In pearson's correlations, visceral fat distance were correlated with BMI (r = 0.681, P < 0.001), waist circumference (r = 0.661, P < 0.001), WHR (r = 0.571, P < 0.001), triglyceride (r = 0.316, P < 0.001), HDL-cholesterol (r = -0.207, P < 0.004). US-determined visceral fat distance was also correlated with visceral fat amount by CT (r = 0.674, P < 0.001) and BMI (r = 0.610, P < 0.001), waist circumference (r = 0.626, P < 0.001), WHR (r = 0.557, P < 0.001). When we used waist circumference (men: 90 cm, women: 85 cm) as parameters for visceral obesity, the cutoff value of visceral fat distance, obtained by the receiver operating characteristic curve analysis, were 4.670 cm in men, 3.695 cm in women diabetic patients. CONCLUSION: Intra-abdominal fat distance measured by US reveals strongly correlated with visceral fat area, which is determined by CT and also well correlated with anthropometric parameters and lipid profiles. We suggest that US provided a better index compared to anthropometry for the prediction of visceral obesity and could be an alternative method for CT for visceral fat determination in diabetic patients.

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