Diabetes & Metabolism Journal

Responses

Association of Uterine Leiomyoma with Type 2 Diabetes Mellitus in Young Women: A Population-Based Cohort Study (Diabetes Metab J 2024;48:1105-13): Ji-Hee Sung, Kyung-Soo Kim, Kyungdo Han, Cheol-Young Park; Diabetes Metab J. 2024;48(6):1183-1184. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0681

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Diabetes Promotes Myocardial Fibrosis via AMPK/EZH2/PPAR-γ Signaling Pathway (Diabetes Metab J 2024;48:716-29): Shan-Shan Li, Lu Pan, Shipeng Dang, Ru-Xing Wang; Diabetes Metab J. 2024;48(6):1181-1182. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0675

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Reviews

Lifestyle
Ultra-Processed Foods and the Impact on Cardiometabolic Health: The Role of Diet Quality: Xiaowen Wang, Qi Sun; Diabetes Metab J. 2024;48(6):1047-1055. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0659

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Abstract PDF PubReader ePub: The consumption of ultra-processed foods (UPFs) has surged globally, raising significant public health concerns due to their associations with a range of adverse health outcomes. This review aims to elucidate potential health impacts of UPF intake and underscore the importance of considering diet quality when interpreting study findings. UPF group, as classified by the Nova system based on the extent of industrial processing, contains numerous individual food items with a wide spectrum of nutrient profiles, as well as differential quality as reflected by their potential health effects. The quality of a given food may well misalign with the processing levels so that a UPF food can be nutritious and healthful whereas a non-UPF food can be of low quality and excess intake of which may lead to adverse health consequences. The current review argues that it is critical to focus on the nutritional content and quality of foods and their role within the overall dietary pattern rather than only the level of processing. Further research should dissect health effects of diet quality and food processing, investigate the health impacts of ingredients that render the UPF categorization, understand roles of metabolomics and the gut microbiome in mediating and modulating the health effects of food processing, and consider environmental sustainability in UPF studies. Emphasizing nutrient-dense healthful foods and dietary patterns shall remain the pivotal strategy for promoting overall health and preventing chronic diseases.

Complications
Rate-Dependent Depression of the Hoffmann Reflex: Practical Applications in Painful Diabetic Neuropathy: Lu Han, Nigel A. Calcutt, Xiajun Zhou; Diabetes Metab J. 2024;48(6):1029-1046. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0614

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Abstract PDF PubReader ePub: Measurement of the rate-dependent depression (RDD) of the Hoffmann (H) reflex, a technique developed over half a century ago, is founded on repeated stimulation of the H-reflex with tracking of sequentially evoked H-wave amplitudes in the resulting electromyogram. RDD offers insight into the integrity of spinal reflex pathways and spinal inhibitory regulation. Initially, RDD was predominantly utilized in the mechanistic exploration and evaluation of movement disorders characterized by spasticity symptoms, as may occur following spinal cord injury. However, there is increasing recognition that sensory input from the periphery is modified at the spinal level before ascending to the higher central nervous system and that some pain states can arise from, or be exaggerated by, disruption of spinal processing via a mechanism termed spinal disinhibition. This, along with the urgent clinical need to identify biological markers of pain generator and/or amplifier sites to facilitate targeted pain therapies, has prompted interest in RDD as a biomarker for the contribution of spinal disinhibition to neuropathic pain states. Current research in animals and humans with diabetes has revealed specific disorders of spinal GABAergic function associated with impaired RDD. Future investigations on RDD aim to further elucidate its underlying pathways and enhance its clinical applications.

Letters

Association of Uterine Leiomyoma with Type 2 Diabetes Mellitus in Young Women: A Population-Based Cohort Study (Diabetes Metab J 2024;48:1105-13): Zhenzhi Qin, Yan Xu; Diabetes Metab J. 2024;48(6):1179-1180. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0552

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Targeting Cardiac Fibrosis in Diabetic Heart Failure: The Role of the EZH2, AMPK, and PPAR-γ Pathways (Diabetes Metab J 2024;48:716-29): Jooyeop Lee, Joon Ho Moon; Diabetes Metab J. 2024;48(6):1176-1178. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0551

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Review

Guideline/Fact Sheet
Metabolic Dysfunction-Associated Steatotic Liver Disease in Type 2 Diabetes Mellitus: A Review and Position Statement of the Fatty Liver Research Group of the Korean Diabetes Association: Jaehyun Bae, Eugene Han, Hye Won Lee, Cheol-Young Park, Choon Hee Chung, Dae Ho Lee, Eun-Hee Cho, Eun-Jung Rhee, Ji Hee Yu, Ji Hyun Park, Ji-Cheol Bae, Jung Hwan Park, Kyung Mook Choi, Kyung-Soo Kim, Mi Hae Seo, Minyoung Lee, Nan-Hee Kim, So Hun Kim, Won-Young Lee, Woo Je Lee, Yeon-Kyung Choi, Yong-ho Lee, You-Cheol Hwang, Young Sang Lyu, Byung-Wan Lee, Bong-Soo Cha, on Behalf of the Fatty Liver Research Group of the Korean Diabetes Association; Diabetes Metab J. 2024;48(6):1015-1028. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0541

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Abstract PDF PubReader ePub: Since the role of the liver in metabolic dysfunction, including type 2 diabetes mellitus, was demonstrated, studies on non-alcoholic fatty liver disease (NAFLD) and metabolic dysfunction-associated fatty liver disease (MAFLD) have shown associations between fatty liver disease and other metabolic diseases. Unlike the exclusionary diagnostic criteria of NAFLD, MAFLD diagnosis is based on the presence of metabolic dysregulation in fatty liver disease. Renaming NAFLD as MAFLD also introduced simpler diagnostic criteria. In 2023, a new nomenclature, steatotic liver disease (SLD), was proposed. Similar to MAFLD, SLD diagnosis is based on the presence of hepatic steatosis with at least one cardiometabolic dysfunction. SLD is categorized into metabolic dysfunction-associated steatotic liver disease (MASLD), metabolic dysfunction and alcohol-related/-associated liver disease, alcoholrelated liver disease, specific etiology SLD, and cryptogenic SLD. The term MASLD has been adopted by a number of leading national and international societies due to its concise diagnostic criteria, exclusion of other concomitant liver diseases, and lack of stigmatizing terms. This article reviews the diagnostic criteria, clinical relevance, and differences among NAFLD, MAFLD, and MASLD from a diabetologist’s perspective and provides a rationale for adopting SLD/MASLD in the Fatty Liver Research Group of the Korean Diabetes Association.

Editorial

The Importance of Treating Hyperglycemia in β-Cell Dysfunction of Type 2 Diabetes Mellitus: Arim Choi, Kyung-Soo Kim; Diabetes Metab J. 2024;48(6):1056-1057. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0515

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Original Articles

Cardiovascular Risk/Epidemiology
Cardiovascular Disease & Diabetes Statistics in Korea: Nationwide Data 2010 to 2019: Jin Hwa Kim, Junyeop Lee, Kyungdo Han, Jae-Taek Kim, Hyuk-Sang Kwon, on Behalf of the Diabetic Vascular Disease Research Group of the Korean Diabetes Association; Diabetes Metab J. 2024;48(6):1084-1092. Published online November 21, 2024; DOI: https://doi.org/10.4093/dmj.2024.0275

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Abstract PDF Supplementary Material PubReader ePub: Background
This study aimed to provide updated insights into the incidence and management of cardiovascular disease (CVD) in Korean adults with diabetes.
Methods
Using data from the Korean National Health Insurance Service and Korea National Health and Nutrition Examination Survey, we analyzed the representative national estimates of CVD in adults with diabetes.
Results
The age- and sex-standardized incidence rate of ischemic heart disease (IHD), ischemic stroke, and peripheral artery disease (PAD) decreased from 2010 to 2019 in individuals with type 2 diabetes mellitus (T2DM). However, an increase in the incidence of heart failure (HF) was observed during the same period. Only 4.96% of adults with diabetes and CVD achieved optimal control of all three risk factors (glycemic levels, blood pressure, and lipid control). Additionally, high-intensity statin treatment rates were 8.84% and 9.15% in individuals with IHD and ischemic stroke, respectively. Treatment with a sodium-glucose cotransporter-2 inhibitor (SGLT2i) or a glucagon-like peptide-1 receptor agonist (GLP-1RA) was relatively low in 2019, with only 11.87%, 7.10%, and 11.05% of individuals with IHD, ischemic stroke, and HF, respectively, receiving SGLT2i treatment. Furthermore, only 1.08%, 0.79%, and 1.06% of patients with IHD, ischemic stroke, and HF, respectively, were treated with GLP-1RA.
Conclusion
The incidence of most CVD (IHD, ischemic stroke, and PAD) decreased between 2010 and 2019, whereas the incidence of HF increased. The overall use of high-intensity statins, SGLT2i, and GLP-1RA remained low among individuals with T2DM and CVD.

Metabolic Risk/Epidemiology
Do Time-Dependent Repeated Measures of Anthropometric and Body Composition Indices Improve the Prediction of Incident Diabetes in the Cohort Study? Findings from a Community-Based Korean Genome and Epidemiology Study: Hye Ah Lee, Hyesook Park, Bomi Park; Received July 4, 2024 Accepted September 7, 2024 Published online November 15, 2024; DOI: https://doi.org/10.4093/dmj.2024.0357 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
Cumulative evidence consistently shows that anthropometric and body composition measurements are strongly linked to the risk of incident diabetes, typically based on baseline measurements. This study aims to assess whether repeated measurements enhance the prediction of diabetes risk beyond baseline assessments alone.
Methods
We utilized data from a 16-year population-based follow-up cohort within the Korean Genome and Epidemiology Study, comprising 6,030 individuals aged 40 to 69 years at baseline. We included eight indices: a body shape index (ABSI), body adiposity index (BAI), waist circumference (WC), body mass index (BMI), waist-to-hip ratio (WHR), weight-adjusted skeletal muscle index (SMI), percent body fat, and fat-to-muscle ratio. The effect of these measurements for incident diabetes was estimated using Harrell’s C-indexes and hazard ratios with 95% confidence intervals, employing time-dependent Cox proportional hazard models.
Results
Over the 16-year follow-up, 939 new diabetes cases were identified (cumulative incidence, 15.6%). The median number of indicator measurements per participant was eight. The basic model, including 10 features (sex, age, education levels, physical activity, alcohol intake, current smoking, total energy intake, dietary diversity score, and log-transformed C-reactive protein levels, and quartiles of unweighted genetic risk score at baseline), yielded a Harrell’s C-index of 0.610. The highest C-index in repeated measurements was for WC (0.668) across the general population, weight-adjusted SMI in men, and WHR in women. However, except for ABSI and BAI, the diabetes predictive power of the other indicators was comparable. Additionally, repeated measurements of WC, BMI, and WHR in women were found to contribute to improved discrimination compared to baseline measurements, but not in men.
Conclusion
Utilizing repeated measurements of general and central adiposity to predict diabetes may be helpful in predicting hidden risks, especially in women.

Lifestyle
Impact of Meal Frequency on Insulin Resistance in Middle-Aged and Older Adults: A Prospective Cohort Study: Ha-Eun Ryu, Jong Hee Lee, Byoungjin Park, Seok-Jae Heo, Yu-Jin Kwon; Received July 22, 2024 Accepted September 7, 2024 Published online November 13, 2024; DOI: https://doi.org/10.4093/dmj.2024.0407 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
Insulin resistance (IR) is central to metabolic disorders and significantly influenced by diet. Studies on meal frequency (MF) and metabolic indicators have shown mixed results. This study explores the link between MF and IR in middle-aged and older adults.
Methods
This prospective cohort study included 4,570 adults aged 40 to 69 years from the Korean Genome and Epidemiologic Study. MF were divided into two groups based on whether they consumed three or more, or fewer than three, meals daily. IR was evaluated using the homeostasis model assessment of insulin resistance (HOMA-IR); participants were classified as IR if their HOMA-IR value was ≥2.5. Multiple Cox proportional hazard regression analyses were conducted to examine the association between MF and the incidence of IR.
Results
After adjusting for all variables, individuals in the MF ≥3 group showed a reduced incidence of IR compared to those in the MF <3 group (hazard ratio, 0.880; 95% confidence interval, 0.782 to 0.990). Additionally, subgroup analyses by sex, diabetes mellitus (DM), and body mass index (BMI) showed that this association persisted only in men, individuals without DM, and those with a BMI <25.
Conclusion
Our findings indicate that a higher MF among middle-aged and older adults is associated with a reduced incidence of IR. However, this association was maintained only in men, individuals without DM, and those without obesity.

Genetics
Exon Sequencing of HNF1β in Chinese Patients with Early-Onset Diabetes: Siqian Gong, Hong Lian, Yating Li, Xiaoling Cai, Wei Liu, Yingying Luo, Meng Li, Si-min Zhang, Rui Zhang, Lingli Zhou, Yu Zhu, Qian Ren, Xiuying Zhang, Jing Chen, Jing Wu, Xianghai Zhou, Xirui Wang, Xueyao Han, Linong Ji; Received March 20, 2024 Accepted July 24, 2024 Published online November 13, 2024; DOI: https://doi.org/10.4093/dmj.2024.0159 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
Maturity-onset diabetes of the young (MODY) due to variants of hepatocyte nuclear factor 1-beta (HNF1β) (MODY5) has not been well studied in the Chinese population. This study aimed to estimate its prevalence and evaluate the application of a clinical screening method (Faguer score) in Chinese early-onset diabetes (EOD) patients.
Methods
Among 679 EOD patients clinically diagnosed with type 2 diabetes mellitus (age at diagnosis ≤40 years), the exons of HNF1β were sequenced. Functional impact of rare variants was evaluated using a dual-luciferase reporter system. Faguer scores ≥8 prompted multiplex ligation-dependent probe amplification (MLPA) for large deletions. Pathogenicity of HNF1β variants was assessed following the American College of Medical Genetics and Genomics (ACMG) guidelines.
Results
Two rare HNF1β missense mutations (E105K and G454R) were identified by sequencing in five patients, showing functional impact in vitro. Another patient was found to have a whole-gene deletion by MLPA in 22 patients with the Faguer score above 8. Following ACMG guidelines, six patients carrying pathogenic or likely pathogenic variant were diagnosed with MODY5. The estimated prevalence of MODY5 in Chinese EOD patients was approximately 0.9% or higher.
Conclusion
MODY5 is not uncommon in China. The Faguer score is helpful in deciding whether to perform MLPA analysis on patients with negative sequencing results.

Technology/Device
Efficacy and Safety of Automated Insulin Delivery Systems in Patients with Type 1 Diabetes Mellitus: A Systematic Review and Meta-Analysis: Wenqi Fan, Chao Deng, Ruoyao Xu, Zhenqi Liu, Richard David Leslie, Zhiguang Zhou, Xia Li; Received March 17, 2024 Accepted July 24, 2024 Published online November 13, 2024; DOI: https://doi.org/10.4093/dmj.2024.0130 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
Automated insulin delivery (AID) systems studies are upsurging, half of which were published in the last 5 years. We aimed to evaluate the efficacy and safety of AID systems in patients with type 1 diabetes mellitus (T1DM).
Methods
We searched PubMed, Embase, Cochrane Library, Web of Science, and ClinicalTrials.gov until August 31, 2023. Randomized clinical trials that compared AID systems with other insulin-based treatments in patients with T1DM were considered eligible. Studies characteristics and glycemic metrics was extracted by three researchers independently.
Results
Sixty-five trials (3,623 patients) were included. The percentage of time in range (TIR) was 11.74% (95% confidence interval [CI], 9.37 to 14.12; P<0.001) higher with AID systems compared with control treatments. Patients on AID systems had more pronounced improvement of time below range when diabetes duration was more than 20 years (–1.80% vs. –0.86%, P=0.031) and baseline glycosylated hemoglobin lower than 7.5% (–1.93% vs. –0.87%, P=0.033). Dual-hormone full closed-loop systems revealed a greater improvement in TIR compared with hybrid closed-loop systems (–19.64% vs. –10.87%). Notably, glycemia risk index (GRI) (–3.74; 95% CI, –6.34 to –1.14; P<0.01) was also improved with AID therapy.
Conclusion
AID systems showed significant advantages compared to other insulin-based treatments in improving glucose control represented by TIR and GRI in patients with T1DM, with more favorable effect in euglycemia by dual-hormone full closedloop systems as well as less hypoglycemia for patients who are within target for glycemic control and have longer diabetes duration.

Basic Research
Rbbp6-Mediated Bmal1 Ubiquitination Inhibits YAP1 Signaling Pathway to Promote Ferroptosis in Diabetes-Induced Testicular Damage: Yuan Tian, Zhiqiang Zhu, Jun Qiao, Bei Liu, Yuehai Xiao; Received March 1, 2024 Accepted June 17, 2024 Published online November 6, 2024; DOI: https://doi.org/10.4093/dmj.2024.0099 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
Diabetes-induced testicular damage (DITD) is a common complication of diabetes. We investigated underlying mechanism of retinoblastoma-binding protein 6 (Rbbp6)-mediated brain and muscle ARNT-like 1 (Bmal1) ubiquitination in modulating ferroptosis in DITD.
Methods
Spermatogenic cell apoptosis and viability were measured by flow cytometry and cell counting kit 8 (CCK-8), respectively. The impact of Rbbp6 and Bmal1 on ferroptosis was assessed by determining expression of ferroptosis markers glutathione peroxidase 4 (GPX4) and solute carrier family 7 member 11 (SLC7A11), and levels of malondialdehyde (MDA), glutathione (GSH), iron, and lipid peroxidation. Co-immunoprecipitation was performed to determine the interaction between Rbbp6 and Bmal1, as well as the ubiquitination level of Bmal1. The expression levels of Rbbp6, Bmal1, Yes-associated protein 1 (YAP1), ferroptosis markers, and testicular steroidogenic enzymes were tested by Western blot.
Results
Bmal1 protein expression was significantly downregulated, while Rbbp6 was upregulated in DITD mouse model and high glucose (HG)-induced GC-1 spg cells. Overexpression of Bmal1 improved testicular injury in diabetic mice, reduced 4-hydroxynonenal (4-HNE), MDA, iron levels, and increased expression levels of GPX4, SLC7A11, GSH, as well as testicular steroidogenic enzymes. Rbbp6 decreased Bmal1 level through promoting its ubiquitination. Meanwhile, Rbbp6 knockdown inhibited the ferroptosis of HG-induced GC-1 spg cells, which were abolished by silencing Bmal1. In addition, knockdown of YAP1 or treatment with ferroptosis inducer erastin blocked the above effects caused by Bmal1 overexpression.
Conclusion
Rbbp6-mediated Bmal1 ubiquitination suppressed YAP1 pathway, promoting ferroptosis in DITD. This study highlighted Rbbp6/Bmal1/YAP1 axis as a potential therapeutic target for mitigating DITD.

Complications
To Determine the Risk-Based Screening Interval for Diabetic Retinopathy: Development and Validation of Risk Algorithm from a Retrospective Cohort Study: Jinxiao Lian, Ching So, Sarah Morag McGhee, Thuan-quoc Thach, Cindy Lo Kuen Lam, Colman Siu Cheung Fung, Alfred Siu Kei Kwong, Jonathan Cheuk Hung Chan; Received March 21, 2024 Accepted July 24, 2024 Published online October 31, 2024; DOI: https://doi.org/10.4093/dmj.2024.0142 [Epub ahead of print]

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Abstract PDF Supplementary Material PubReader ePub: Background
The optimal screening interval for diabetic retinopathy (DR) remains controversial. This study aimed to develop a risk algorithm to predict the individual risk of referable sight-threatening diabetic retinopathy (STDR) in a mainly Chinese population and to provide evidence for risk-based screening intervals.
Methods
The retrospective cohort data from 117,418 subjects who received systematic DR screening in Hong Kong between 2010 and 2016 were included to develop and validate the risk algorithm using a parametric survival model. The risk algorithm can be used to predict the individual risk of STDR within a specific time interval, or the time to reach a specific risk margin and thus to allocate a screening interval. The calibration performance was assessed by comparing the cumulative STDR events versus predicted risk over 2 years, and discrimination by using receiver operative characteristics (ROC) curve.
Results
Duration of diabetes, glycosylated hemoglobin, systolic blood pressure, presence of chronic kidney disease, diabetes medication, and age were included in the risk algorithm. The validation of prediction performance showed that there was no significant difference between predicted and observed STDR risks in males (5.6% vs. 5.1%, P=0.724) or females (4.8% vs. 4.6%, P=0.099). The area under the receiver operating characteristic curve was 0.80 (95% confidence interval [CI], 0.78 to 0.81) for males and 0.81 (95% CI, 0.79 to 0.83) for females.
Conclusion
The risk algorithm has good prediction performance for referable STDR. Using a risk-based screening interval allows us to allocate screening visits disproportionally more to those at higher risk, while reducing the frequency of screening of lower risk people.

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