Diabetes & Metabolism Journal

Original Articles

Metabolic Risk/Epidemiology
2023 Diabetic Kidney Disease Fact Sheet in Korea: Nam Hoon Kim, Mi-Hae Seo, Jin Hyung Jung, Kyung Do Han, Mi Kyung Kim, Nan Hee Kim, on Behalf of Diabetic Kidney Disease Research Group of the Korean Diabetes Association; Diabetes Metab J. 2024;48(3):463-472. Published online March 19, 2024; DOI: https://doi.org/10.4093/dmj.2023.0310

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Background
To investigate the prevalence, incidence, comorbidities, and management status of diabetic kidney disease (DKD) and diabetes-related end-stage kidney disease (ESKD) in South Korea.
Methods
We used the Korea National Health and Nutrition Examination Survey data (2019 to 2021, n=2,665) for the evaluation of prevalence, comorbidities, control rate of glycemia and comorbidities in DKD, and the Korean Health Insurance Service-customized database (2008 to 2019, n=3,950,857) for the evaluation of trends in the incidence and prevalence rate of diabetes-related ESKD, renin-angiotensin system (RAS) blockers and sodium glucose cotransporter 2 (SGLT2) inhibitors use for DKD, and the risk of atherosclerotic cardiovascular disease (ASCVD) and mortality according to DKD stages. DKD was defined as albuminuria or low estimated glomerular filtration rate (eGFR) <60 mL/min/1.73 m² in patients with diabetes mellitus.
Results
The prevalence of DKD was 25.4% (albuminuria, 22.0%; low eGFR, 6.73%) in patients with diabetes mellitus aged ≥30 years. Patients with DKD had a higher rate of comorbidities, including hypertension, dyslipidemia, and central obesity; however, their control rates were lower than those without DKD. Prescription rate of SGLT2 inhibitors with reduced eGFR increased steadily, reaching 5.94% in 2019. Approximately 70% of DKD patients were treated with RAS blockers. The prevalence rate of diabetesrelated ESKD has been steadily increasing, with a higher rate in older adults. ASCVD and mortality were significantly associated with an in increase in DKD stage.
Conclusion
DKD is prevalent among Korean patients with diabetes and is an independent risk factor for cardiovascular morbidity and mortality, which requiring intensive management of diabetes and comorbidities. The prevalence of diabetes-related ESKD has been increasing, especially in the older adults, during past decade.

Citations

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Endothelial NOX5 Obliterates the Reno-Protective Effect of Nox4 Deletion by Promoting Renal Fibrosis via Activation of EMT and ROS-Sensitive Pathways in Diabetes
Karin A. M. Jandeleit-Dahm, Haritha R. Kankanamalage, Aozhi Dai, Jaroslawna Meister, Sara Lopez-Trevino, Mark E. Cooper, Rhian M. Touyz, Christopher R. J. Kennedy, Jay C. Jha
Antioxidants.2024; 13(4): 396. CrossRef

Guideline/Fact Sheet
Diabetes Mellitus in the Elderly Adults in Korea: Based on Data from the Korea National Health and Nutrition Examination Survey 2019 to 2020: Seung-Hyun Ko, Kyung Do Han, Yong-Moon Park, Jae-Seung Yun, Kyuho Kim, Jae-Hyun Bae, Hyuk-Sang Kwon, Nan-Hee Kim; Diabetes Metab J. 2023;47(5):643-652. Published online August 7, 2023; DOI: https://doi.org/10.4093/dmj.2023.0041

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Background
We evaluated the prevalence and management of diabetes mellitus (DM) in elderly Korean patients based on data from the Korea National Health and Nutrition Examination Survey (KNHANES).
Methods
A total of 3,068 adults aged 65 years and older (19.8% of total population) were analyzed using KNHANES from 2019 to 2020. Prevalence, awareness, treatment, and control rates, and comorbidities were analyzed. Lifestyle behaviors and energy intake were also measured.
Results
The prevalence of DM and prediabetes was 29.6% and 50.5%, respectively. The awareness, treatment and control rates were 76.4%, 73.3%, and 28.3%, respectively. The control rate was 77.0% if A1C <7.5% criteria was used. The mean A1C value of individuals with known DM was 7.1%, and 14.5% of the known DM patients had A1C ≥8.0%. Abdominal obesity, hypertension, and hypercholesterolemia were combined with DM in 63.9%, 71.7%, and 70.7%, respectively, and the rate of integrated management was 36.0% (A1C <7.5% criteria). A total of 40.1% of those with DM walked regularly. The percentage of energy intake from carbohydrates was higher in those with DM than in those without DM (P=0.044), while those of fat (P=0.003) and protein (P=0.025) were lower in those with DM than in those without DM in women.
Conclusion
In 2019 to 2020, three of 10 adults aged 65 years and older in Korea had DM, and approximately 70% of them had comorbidities. A strategy for more individualized comprehensive care for the elderly patients with DM is urgently needed.

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Association Between High Blood Folate Levels and Glaucoma in a Representative Korean Population
Ji Young Lee, Jin A. Choi, Sung Pyo Park, Donghyun Jee
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Is the change in longitudinal cognitive function in older adults with diabetes affected by trajectory classes of depressive symptoms?
Gyeong A Kang, Ju Young Yoon
Public Health Nursing.2024; 41(5): 1006. CrossRef
Holistic and Personalized Strategies for Managing in Elderly Type 2 Diabetes Patients
Jae-Seung Yun, Kyuho Kim, Yu-Bae Ahn, Kyungdo Han, Seung-Hyun Ko
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Association and interaction effect of shift work and the risk for obstructive sleep apnea on diabetes mellitus in middle-aged Korean workers
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Benefit and Safety of Sodium-Glucose Co-Transporter 2 Inhibitors in Older Patients with Type 2 Diabetes Mellitus
Ja Young Jeon, Dae Jung Kim
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National trends in type 2 diabetes mellitus stratified by central adiposity using waist-to-height ratio in South Korea, 2005–2022
Hyunjee Kim, Seoyoung Park, Jaeyu Park, Yejun Son, Soeun Kim, Yesol Yim, Hyesu Jo, Kyeongmin Lee, Yi Deun Jeong, Jiyeon Oh, Hanseul Cho, Damiano Pizzol, Jiyoung Hwang, Lee Smith, Dong Keon Yon
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Changes in the Epidemiological Landscape of Diabetes in South Korea: Trends in Prevalence, Incidence, and Healthcare Expenditures
Kyoung Hwa Ha, Dae Jung Kim
Endocrinology and Metabolism.2024; 39(5): 669. CrossRef
Osteoporosis incidence and its associated factors in the older Korean population: findings from a population-based cohort study
Tanmoy Das, Md Abdullah Al Jubayer Biswas, Prosanta Mondal, Sabuj Sarker, Hyun J.“June” Lim
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Association of Uterine Leiomyoma with Type 2 Diabetes Mellitus in Young Women: A Population-Based Cohort Study
Ji-Hee Sung, Kyung-Soo Kim, Kyungdo Han, Cheol-Young Park
Diabetes & Metabolism Journal.2024; 48(6): 1105. CrossRef
Socioeconomic inequalities in the prevalence, non-awareness, non-treatment, and non-control of diabetes among South Korean adults in 2021
Seongju Kim, Dong Jun Kim, Hooyeon Lee, Dong Keon Yon
PLOS ONE.2024; 19(11): e0313988. CrossRef
Trends in prescribing sodium‐glucose cotransporter 2 inhibitors for individuals with type 2 diabetes with and without cardiovascular‐renal disease in South Korea, 2015–2021
Kyoung Hwa Ha, Soyoung Shin, EunJi Na, Dae Jung Kim
Journal of Diabetes Investigation.2024;[Epub] CrossRef
The Growing Challenge of Diabetes Management in an Aging Society
Seung-Hwan Lee
Diabetes & Metabolism Journal.2023; 47(5): 630. CrossRef

Guideline/Fact Sheet
Comparison of Operational Definition of Type 2 Diabetes Mellitus Based on Data from Korean National Health Insurance Service and Korea National Health and Nutrition Examination Survey: Jong Ha Baek, Yong-Moon Park, Kyung Do Han, Min Kyong Moon, Jong Han Choi, Seung-Hyun Ko; Diabetes Metab J. 2023;47(2):201-210. Published online February 8, 2023; DOI: https://doi.org/10.4093/dmj.2022.0375

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Background
We evaluated the validity and reliability of the operational definition of type 2 diabetes mellitus (T2DM) based on the Korean National Health Insurance Service (NHIS) database.
Methods
Adult subjects (≥40 years old) included in the Korea National Health and Nutrition Examination Survey (KNHANES) from 2008 to 2017 were merged with those from the NHIS health check-up database, producing a cross-sectional dataset. We evaluated the sensitivity, specificity, accuracy, and agreement of the NHIS criteria for defining T2DM by comparing them with the KNHANES criteria as a standard reference.
Results
In the study population (n=13,006), two algorithms were devised to determine from the NHIS dataset whether the diagnostic claim codes for T2DM were accompanied by prescription codes for anti-diabetic drugs (algorithm 1) or not (algorithm 2). Using these algorithms, the prevalence of T2DM was 14.9% (n=1,942; algorithm 1) and 20.8% (n=2,707; algorithm 2). Good reliability in defining T2DM was observed for both algorithms (Kappa index, 0.73 [algorithm 1], 0.63 [algorithm 2]). However, the accuracy (0.93 vs. 0.89) and specificity (0.96 vs. 0.90) tended to be higher for algorithm 1 than for algorithm 2. The validity (accuracy, ranging from 0.91 to 0.95) and reliability (Kappa index, ranging from 0.68 to 0.78) of defining T2DM by NHIS criteria were independent of age, sex, socioeconomic status, and accompanied hypertension or dyslipidemia.
Conclusion
The operational definition of T2DM based on population-based NHIS claims data, including diagnostic codes and prescription codes, could be a valid tool to identify individuals with T2DM in the Korean population.

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Association between Age at Diagnosis of Type 2 Diabetes and Subsequent Risk of Dementia and Its Major Subtypes
Da Hea Seo, Mina Kim, Yongin Cho, Seong Hee Ahn, Seongbin Hong, So Hun Kim
Journal of Clinical Medicine.2024; 13(15): 4386. CrossRef
Gamma‐glutamyl transferase and the risk of all‐cause and disease‐specific mortality in patients with diabetes: A nationwide cohort study
Goh Eun Chung, Su‐Min Jeong, Su Jong Yu, Jeong‐Ju Yoo, Yuri Cho, Kyu‐na Lee, Dong Wook Shin, Yoon Jun Kim, Jung‐Hwan Yoon, Kyungdo Han, Eun Ju Cho
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Association between exercise habits and incident type 2 diabetes mellitus in patients with thyroid cancer: nationwide population-based study
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All-cause and cause-specific mortality risks in individuals with diabetes living alone: A large-scale population-based cohort study
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Drug/Regimen
Real-World Prescription Patterns and Barriers Related to the Use of Sodium-Glucose Cotransporter 2 Inhibitors among Korean Patients with Type 2 Diabetes Mellitus and Cardiovascular Disease: Jong Ha Baek, Ye Seul Yang, Seung-Hyun Ko, Kyung Do Han, Jae Hyeon Kim, Min Kyong Moon, Jong Suk Park, Byung-Wan Lee, Tae Jung Oh, Suk Chon, Jong Han Choi, Kyu Yeon Hur, Committee of Clinical Practice Guidelines, Korean Diabetes Association; Diabetes Metab J. 2022;46(5):701-712. Published online June 3, 2022; DOI: https://doi.org/10.4093/dmj.2022.0002

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Background
To evaluate prescription trends and clinical factors of the sodium-glucose cotransporter 2 inhibitors (SGLT2i) use according to the presence of atherosclerotic cardiovascular disease (ASCVD) or heart failure (HF) in Korean patients with type 2 diabetes mellitus (T2DM).
Methods
Prescription patterns of SGLT2i use between 2015 and 2019 were determined using the Korean National Health Insurance Service database of claims.
Results
Of all patients with T2DM (n=4,736,493), the annual prescription rate of SGLT2i increased every year in patients with ASCVD (from 2.2% to 10.7%) or HF (from 2.0% to 11.1%). After the first hospitalization for ASCVD (n=518,572), 13.7% (n=71,259) of patients initiated SGLT2i with a median of 10.6 months. After hospitalization for HF (n=372,853), 11.2% (n=41,717) of patients initiated SGLT2i after a median of 8.8 months. In multivariate regression for hospitalization, older age (per 10 years, odds ratio [OR], 0.57; 95% confidence interval [CI], 0.56 to 0.57), lower household income (OR, 0.93; 95% CI, 0.92 to 0.95), rural residents (OR, 0.95; 95% CI, 0.93 to 0.97), and dipeptidyl peptidase-4 inhibitor (DPP-4i) users (OR, 0.82; 95% CI, 0.81 to 0.84) were associated with lesser initiation of SGLT2i in ASCVD. Additionally, female gender (OR, 0.97; 95% CI, 0.95 to 0.99) was associated with lesser initiation of SGLT2i in HF.
Conclusion
The prescription rate of SGLT2i increased gradually up to 2019 but was suboptimal in patients with ASCVD or HF. After the first hospitalization for ASCVD or HF, older age, female gender, low household income, rural residents, and DPP-4i users were less likely to initiate SGLT2i.

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Effectiveness and safety of sodium–glucose cotransporter 2 inhibitors in Asian populations
Kyoung Hwa Ha, Dae Jung Kim
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Real-World Treatment Patterns according to Clinical Practice Guidelines in Patients with Type 2 Diabetes Mellitus and Established Cardiovascular Disease in Korea: Multicenter, Retrospective, Observational Study
Ye Seul Yang, Nam Hoon Kim, Jong Ha Baek, Seung-Hyun Ko, Jang Won Son, Seung-Hwan Lee, Sang Youl Rhee, Soo-Kyung Kim, Tae Seo Sohn, Ji Eun Jun, In-Kyung Jeong, Chong Hwa Kim, Keeho Song, Eun-Jung Rhee, Junghyun Noh, Kyu Yeon Hur
Diabetes & Metabolism Journal.2024; 48(2): 279. CrossRef
Hospital Readmissions for Fluid Overload among Individuals with Diabetes and Diabetic Kidney Disease: Risk Factors and Multivariable Prediction Models
Jiashen Cai, Dorothy Huang, Hanis Binte Abdul Kadir, Zhihua Huang, Li Choo Ng, Andrew Ang, Ngiap Chuan Tan, Yong Mong Bee, Wei Yi Tay, Chieh Suai Tan, Cynthia C. Lim
Nephron.2024; 148(8): 523. CrossRef
Kidney outcomes with SGLT2 inhibitor versus DPP4 inhibitor use in older adults with diabetes
Yuta Suzuki, Hidehiro Kaneko, Akira Okada, Jin Komuro, Toshiyuki Ko, Katsuhito Fujiu, Norifumi Takeda, Hiroyuki Morita, Akira Nishiyama, Masaki Ieda, Koichi Node, Hideo Yasunaga, Masaomi Nangaku, Issei Komuro
Nephrology Dialysis Transplantation.2024;[Epub] CrossRef
Benefit and Safety of Sodium-Glucose Co-Transporter 2 Inhibitors in Older Patients with Type 2 Diabetes Mellitus
Ja Young Jeon, Dae Jung Kim
Diabetes & Metabolism Journal.2024; 48(5): 837. CrossRef
Impact of Chronic Kidney Disease and Gout on End-Stage Renal Disease in Type 2 Diabetes: Population-Based Cohort Study
Inha Jung, Da Young Lee, Seung Min Chung, So Young Park, Ji Hee Yu, Jun Sung Moon, Ji A Seo, Kyungdo Han, Nan Hee Kim
Endocrinology and Metabolism.2024; 39(5): 748. CrossRef
Income-Related Disparities in Mortality Among Young Adults With Type 2 Diabetes
Ji Yoon Kim, Sojeong Park, Minae Park, Nam Hoon Kim, Sin Gon Kim
JAMA Network Open.2024; 7(11): e2443918. CrossRef
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Inha Jung, Seungyoon Nam, Da Young Lee, So Young Park, Ji Hee Yu, Ji A Seo, Dae Ho Lee, Nan Hee Kim
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Evaluating the appropriateness and the factors associated with sodium-glucose co-transporter 2 inhibitors prescribing in a Middle Eastern country: a cross-sectional study
Nancy Zaghloul, Ahmed Awaisu, Ahmed Mahfouz, Zainab Ali, Sumaya Alyafei, Hazem Elewa
International Journal of Clinical Pharmacy.2024;[Epub] CrossRef
Trends in prescribing sodium‐glucose cotransporter 2 inhibitors for individuals with type 2 diabetes with and without cardiovascular‐renal disease in South Korea, 2015–2021
Kyoung Hwa Ha, Soyoung Shin, EunJi Na, Dae Jung Kim
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Risk of developing chronic kidney disease in young-onset Type 2 diabetes in Korea
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Severe hypoglycemia as a risk factor for cardiovascular outcomes in patients with type 2 diabetes: is it preventable?
Seung-Hyun Ko
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Association between the Diabetes Drug Cost and Cardiovascular Events and Death in Korea: A National Health Insurance Service Database Analysis
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Corrigendum

Associations among Obesity Degree, Glycemic Status, and Risk of Heart Failure in 9,720,220 Korean Adults: Eun Jung Rhee, Hyemi Kwon, Se Eun Park, Kyung Do Han, Yong Gyu Park, Yang Hyun Kim, Won Young Lee; Diabetes Metab J. 2020;44(5):783-783. Published online October 21, 2020; DOI: https://doi.org/10.4093/dmj.2020.0245; Corrects: Diabetes Metab J 2020;44(4):592

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Original Articles

Epidemiology
Impact of Cytomegalovirus Disease on New-Onset Type 2 Diabetes Mellitus: Population-Based Matched Case-Control Cohort Study: Seul Gi Yoo, Kyung Do Han, Kyoung Hwa Lee, Yeonju La, Da Eun Kwon, Sang Hoon Han; Diabetes Metab J. 2019;43(6):815-829. Published online January 21, 2019; DOI: https://doi.org/10.4093/dmj.2018.0167

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Background

A latent cytomegalovirus (CMV) cause chronic inflammation through undesirable inflation of cell-mediated immune response. CMV immunoglobulin G has been associated with cardiovascular disease and type 1 diabetes mellitus. We evaluated impact of CMV diseases on new-onset type 2 diabetes mellitus (T2DM).

Methods

From the Korean Health Insurance Review and Assessment Service claim database of entire population with 50 million, we retrieved 576 adult case group with CMV diseases diagnosed with International Statistical Classification of Diseases and Related-Health Problems 10th Revision (ICD-10) B25 code between 2010 and 2014 after exclusion of patients with T2DM to 2006. The 2,880 control patients without T2DM from 2006 to cohort entry point were selected between 2010 and 2014 by age, sex matching with case group. The subjects without new-onset T2DM were followed until 2015. T2DM, hypertension (HTN), dyslipidemia (DYS), and end-stage renal disease (ESRD) were coded as ICD-10.

Results

The frequency of new-onset T2DM in case group was significantly higher than that in control (5.6% vs. 2.2%, P<0.001). The group with T2DM (n=95) had higher incidence of CMV diseases than the group without T2DM (n=3,361) (33.7% vs. 16.2%, P<0.001). In multivariate regression model adjusted by age, sex, lower income, HTN, and DYS, the incidence rate (IR) of T2DM in case group was significantly higher than that in the control group (IR per 1,000, 19.0 vs. 7.3; odds ratio, 2.1; 95% confidence interval, 1.3 to 3.2). The co-existence of HTN, DYS, and ESRD with CMV diseases did not influence the IR of T2DM.

Conclusion

CMV diseases increase the patients' risk of developing T2DM.

Citations

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An analysis of risk factors for spontaneously occurring type 2 diabetes mellitus in rhesus macaques (Macaca mulatta)
John P. Capitanio, Laura A. Del Rosso, JoAnn Yee, Marie‐Josee Marie‐France Lemoy
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Tamara Turk Wensveen, Dora Gašparini, Dario Rahelić, Felix M. Wensveen
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Mia Krapić, Inga Kavazović, Felix M. Wensveen
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Association between cytomegalovirus end-organ diseases and moderate-to-severe dementia: a population-based cohort study
Kyoung Hwa Lee, Da Eun Kwon, Kyung Do Han, Yeonju La, Sang Hoon Han
BMC Neurology.2020;[Epub] CrossRef

Complications
The Association between Pancreatic Steatosis and Diabetic Retinopathy in Type 2 Diabetes Mellitus Patients: Jee Sun Jeong, Mee Kyung Kim, Kyung Do Han, Oak Kee Hong, Ki-Hyun Baek, Ki-Ho Song, Dong Jin Chung, Jung-Min Lee, Hyuk-Sang Kwon; Diabetes Metab J. 2018;42(5):425-432. Published online August 9, 2018; DOI: https://doi.org/10.4093/dmj.2017.0107

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Background

Whether pancreatic steatosis has a local or systemic effect, like ectopic fat of other major organs, remains unknown. Data on the influence of pancreatic steatosis on microvascular complication are rare. Therefore, we investigated the relationship between pancreatic steatosis and diabetic retinopathy (DR) in patients with type 2 diabetes mellitus (T2DM).

Methods

The attenuation of three pancreatic regions (head, body, and tail) and the spleen (S) in 186 patients with T2DM was measured using non-enhanced computed tomography imaging. We used three parameters for the assessment of pancreatic steatosis (‘P’ mean: mean attenuation of three pancreatic regions; P–S: difference between ‘P’ mean and ‘S’; P/S: the ‘P’ mean to ‘S’ ratio). The presence of DR was assessed by an expert ophthalmologist using dilated fundoscopy.

Results

The average P mean was 29.02 Hounsfield units (HU), P–S was −18.20 HU, and P/S was 0.61. The three pancreatic steatosis parameters were significantly associated with the prevalence of DR in non-obese T2DM patients. In the non-obese group, the odds ratios of P mean, P–S, and P/S for the prevalence of DR, after adjustment for age, sex, and glycosylated hemoglobin level, were 2.449 (P=0.07), 2.639 (P=0.04), and 2.043 (P=0.02), respectively.

Conclusion

In this study, pancreatic steatosis was significantly associated with DR in non-obese patients with T2DM. Further studies are necessary to clarify the causal relationship between pancreatic steatosis and the development of DR.

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