樱花视频

Skip to main content
Download PDF
  • Research
  • Published:

Lean diabetes: 20-year trends in its prevalence and clinical features among Korean adults

樱花视频 volume听24, Article听number:听3554 (2024) Cite this article

Abstract

Background

We investigated the prevalence and clinical characteristics of type 2 diabetes mellitus in lean Korean adults.

Methods

We analyzed data from the Korea National Health and Nutrition Examination Survey 2001鈥�2021 among adults aged鈥夆墺鈥�19 years. Trend analyses between 2001 and 2019鈥�2021 (n鈥�=鈥�89,720) and comparative analyses of multiple clinical characteristics between patients with type 2 diabetes with and without overweight/obesity were conducted (n鈥�=鈥�2,284).

Results

Between 2001 and 2019鈥�2021, the estimated prevalence of lean type 2 diabetes (body mass index [BMI]鈥�<鈥�23听kg/m2) increased from 6.6 to 8.8%, representing a 33.3% increase. This was a similar extent of increase of type 2 diabetes associated with being overweight or obese (12.1鈥�16.3%, +鈥�34.7%). The increase in the prevalence of lean type 2 diabetes was more pronounced among females, while the increase among those who were overweight or obese was more pronounced among males than their counterparts. Although the overweight/obese type 2 diabetes group (T2DM group) showed more risk factors for cardiovascular disease, the lean T2DM group had lower insulin levels and reduced muscle mass and strength.

Conclusions

The prevalence of lean type 2 diabetes among Korean adults is increasing, at a rate similar to type 2 diabetes in overweight/obese individuals. Patients with lean type 2 diabetes showed decreased beta-cell function and sarcopenia. These findings emphasize the need for tailored management strategies for lean type 2 diabetes given its characteristics and rising prevalence.

Peer Review reports

Background

Type 2 diabetes mellitus is a major global public health concern. The prevalence of type 2 diabetes has rapidly increased globally, and the International Diabetes Federation has estimated that the number of individuals with diabetes will increase to 783听million by 2045 [1]. Obesity is a leading risk factor for type 2 diabetes, and the increasing burden of type 2 diabetes is attributed to its increasing prevalence. Although the pathophysiological and epidemiological links between obesity and type 2 diabetes are well established, a significant fraction of individuals who are not obese or overweight develop type 2 diabetes. This is known as lean type 2 diabetes [2].

Impaired pancreatic insulin secretion has been identified as a key feature of lean type 2 diabetes, although its exact pathophysiology remains unclear [3, 4]. Several clinical and metabolomic profiles appear to differ between obese and non-obese type 2 diabetes [5,6,7,8,9]. The prevalence of lean type 2 diabetes also shows disparities with respect to race and ethnicity and is higher in non-White populations compared with White populations [10, 11]. Although the largest increase in diabetes prevalence was reported in a region with a non-White population, epidemiologic studies have mostly focused on its relationship with obesity [12]. Therefore, monitoring the trends in patients with lean type 2 diabetes may be important for public health surveillance. Furthermore, information about the characteristics of lean diabetes is necessary for the individualized treatment of patients with type 2 diabetes. Hence, these research gaps must be addressed.

We therefore explored secular trends in the prevalence of lean type 2 diabetes among Korean adults (鈮モ��19 years of age) using data from the Korea National Health and Nutrition Examination Survey (KNHANES) 2001鈥�2021. In addition, we compared the clinical features of lean type 2 diabetes and type 2 diabetes in overweight or obese individuals using the KNHANES 2019鈥�2021.

Methods

Data source and study population

The KNHANES, conducted annually by the Korea Disease Control and Prevention Agency (KDCA), is a national cross-sectional health survey that uses a stratified multistage probability sampling design to select a representative sample of the non-institutionalized Korean population. KNHANES data collection consists of health interviews, health examinations, and nutritional surveys administered by trained interviewers and medical staff. Details regarding the KNHANES have been published previously [13]. First, we used data from the KNHANES 2001鈥�2021 to examine temporal trends in lean type 2 diabetes. Among the 101,166 adults aged鈥夆墺鈥�19 years who participated in health interviews and examinations in the 2nd -8th KNHANES (2001鈥�2021), we excluded participants if they had the following conditions: pregnancy or lactation, to exclude gestational diabetes mellitus (n鈥�=鈥�846); diabetes diagnosed before the age of 19 years and taking insulin (n鈥�=鈥�12); and missing information on diabetes definition and body mass index (BMI) (n鈥�=鈥�10,588). The final sample comprised 89,720 adults (Supplemental Fig.听1). Second, we separately analyzed the 8th KNHANES (2019鈥�2021)听data to compare the clinical characteristics between lean type 2 diabetes and type 2 diabetes in overweight or obese individuals. Among 14,768 adults aged鈥夆墺鈥�19 years who participated in health interviews, health examinations, and nutritional surveys in the KNHANES 2019鈥�2021, only those with diabetes were included in the final analyses (n鈥�=鈥�2,284) (Supplemental Fig.听2).

The KDCA obtained written informed consent from all participants before participating in the KNHANES. This study was reviewed and deemed exempt by the Institutional Review Board (IRB) of the Chungnam National University Sejong Hospital (IRB number: 2023-09-005) because only publicly available and anonymized data were used.

Measurements

During the household interview, information on demographics (e.g., age, sex, and residential area), socioeconomic status (e.g., household income, educational status), and health behaviors (e.g., smoking, drinking, and physical activity [metabolic equivalent of tasks, METs]) were obtained from the standardized questionnaire. Total daily energy intake (kcal) and the proportion of energy from carbohydrates, proteins, and fats were estimated using dietary data collected from a 24-h dietary recall interview.

Anthropometric factors were measured by trained examiners using standardized examination procedures and calibrated equipment. With the participants wearing light clothing, standing height (cm) and body weight (kg) were measured using a stadiometer and metric weight scale, respectively. BMI was calculated as the ratio of measured weight to standing height squared (kg/m2). Waist circumference (cm) was measured midway between the highest ridge of the iliac crest and the lowest rib border using an inelastic tape [13]. We used a validated prediction equation [14] comprising age, height, weight, waist circumference, blood creatinine level, physical activity, smoking status, and alcohol use to estimate body composition (e.g., percent lean body mass, body fat mass, and appendicular skeletal muscle mass). Handgrip strength was measured three times in each hand using a grip strength dynamometer (T.K.K 5401; Takei, Tokyo, Japan). For this study, laboratory variables include fasting plasma glucose (FPG) (mg/dL), glycated hemoglobin (HbA1c) (%), insulin (碌U/mL), the homeostasis model assessment of insulin resistance (HOMA-IR) and beta-cell function (HOMA-尾), blood urea nitrogen (mg/dL), total cholesterol (mg/dL), high-density lipoprotein (HDL)-cholesterol (mg/dL), triglyceride (mg/dL), low-density lipoprotein (LDL)-cholesterol (mg/dL), and positive urine glucose and protein (%). Blood and urine samples were collected after an 8听h overnight fast. The HOMA-IR and HOMA-尾 were calculated using the following formulas: HOMA-IR = (fasting insulin [碌U/mL] 脳 FPG [mg/dL])/405; HOMA- 尾鈥�=鈥�360 脳 fasting insulin (碌U/mL)/(FPG [mg/dL] 鈥� 63) [15].

During the health interview, the participants provided a history of several diseases (myocardial infarction, angina, stroke, any type of cancer, kidney disease, liver cirrhosis, and diabetic retinopathy), diabetes-related factors (family history of diabetes, age at diagnosis, recognition, treatment, control of diabetes, and insulin use), and weight control attempts. Hypertension was defined as an affirmative answer to whether they were taking prescribed medicine for high blood pressure (BP) or hypertension, or a systolic BP of 鈮モ��140 mmHg or a diastolic BP of 鈮モ��90 mmHg [16]. Dyslipidemia was defined as a total cholesterol of 鈮モ��240听mg/dL or an affirmative answer to whether the patient was taking prescribed medication for high cholesterol [17]. Metabolic syndrome was defined as having at least three out of five clinical risk factors (abdominal obesity, hypertension, diabetes, elevated serum triglycerides, and low serum HDL cholesterol) based on the criteria of the National Cholesterol Education Program Adult Treatment Panel (NCEP-ATP III) [18].

Definition of lean type 2 diabetes

The presence of type 2 diabetes was defined as at least one of the following: an affirmative answer to 鈥渉ave you ever been told by a doctor that you have diabetes?鈥� (physician-diagnosis); an affirmative answer to 鈥淎re you currently taking prescribed hypoglycemic medications?鈥�; FPG levels of 126听mg/dL (7.0 mmol/L) or more; and HbA1c levels of 鈮モ��6.5% based on the health examination results.

In this study, we used the Asian criteria as defined by the World Health Organization (WHO) to define being overweight (23听kg/m2鈥夆墹鈥塀MI鈥�<鈥�25听kg/ m2) or obese (BMI鈥夆墺鈥�25听kg/m2) [19]. Lean type 2 diabetes was defined as diabetes with a BMI of <鈥�23听kg/m2.

Statistical analysis

All analyses incorporated survey weights, accounting for the complex sampling design of the KNHANES. All tests were two-sided, and the level of significance was set at 0.05, using PROC SURVEY procedures in SAS software version 9.4 (SAS Institute Inc., Cary, NC, USA).

Age-adjusted estimates were produced using the direct standardization method to the 2020 population projections for South Korea using the following categories: males aged 19鈥�39, 40鈥�64, and 65 or more years; females aged 19鈥�39, 40鈥�64, and 65 or more years. We evaluated the prevalence and trends of type 2 diabetes by BMI categories (<鈥�23 as lean and 鈮モ��23 as overweight/obesity). Logistic regression models were used to estimate the prevalence of type 2 diabetes with 95% confidence intervals across the survey year, and we treated the survey year as a continuous variable to test the statistical significance of linear trends over time. Stratified analyses by sociodemographic factors were conducted to assess differences in trends among various subgroups, including age (<鈥�65 and 鈮モ��65 years), sex (male and female), residential area (urban and rural), education level (<鈥塰igh school graduate and 鈮モ�塰igh school graduate), and household income (quartiles of equivalized household income). For sensitivity analysis, the main analyses were repeated using the WHO international criteria for being overweight (BMI of 25听kg/m2) instead of the Asian criteria.

General and clinical characteristics of the study participants with type 2 diabetes according to BMI categories are described as weighted means (standard errors, SEs) for continuous variables and weighted prevalence (SEs) for categorical variables. The statistical significance of the differences between patients with type 2 diabetes with and without overweight/obesity was tested using general linear models after adjusting for age, sex, and duration of diabetes.

Data and resource availability

The datasets generated during and/or analyzed in the current study are available in the KNHANES database, .

Results

The trends and comparison of changes in the overall prevalence of type 2 diabetes, as well as the prevalence in groups with BMI below 23听kg/m2 and those with BMI of 23听kg/m2 or above, are presented in Table听1; Fig.听1. The overall prevalence of type 2 diabetes among adults aged鈥夆墺鈥�19 years increased from 9.8 to 13.3% between 2001 and 2019鈥�2021, representing a 35.7% increase over 20 years. During the same period, the age-standardized prevalence of type 2 diabetes among adults with a BMI of <鈥�23听kg/m2 significantly increased from 6.6 to 8.8%, representing a 33.3% increase. This trend is similar to the increase in type 2 diabetes prevalence among adults with a BMI鈥夆墺鈥�23听kg/m2, which increased from 12.1 to 16.3%, representing a 34.7% increase between 2001 and 2019鈥�2021. In the sensitivity analysis, when a BMI of 25听kg/m2 was used as criteria, we found a consistent increase in type 2 diabetes prevalence among adults with a BMI of less than 25听kg/m2 (7.6鈥�9.8%; +28.9%), although those with a BMI of 鈮モ��25听kg/m2 presented a greater increase (14.2鈥�19.4%; +36.6%) (Supplemental Table 1).

Table 1 Trends in prevalence of diabetes among Korean adults, 2001鈥�2021
Full size table
Fig. 1
figure 1

Changes in prevalence of diabetes among Korean adults by body mass index, 2001鈥�2021. (A) Prevalence of diabetes between 2001 and 2019鈥�2021, (B) changes in prevalence of diabetes, 2019鈥�2021 vs. 2001. Each period represents he Korea National Health and Nutritional Examination Survey (KNHANES) survey cycle, from KNHANES survey II to VIII

Full size image

In the total set, a significant increase in the prevalence of type 2 diabetes between 2001 and 2021 was observed in all subgroups (all p for trend鈥�<鈥�0.05) except for rural residents (p for trend鈥�=鈥�0.7073) (Table听1). Although the prevalence among rural residents significantly increased from 2001 to 2019鈥�2021, there was no statistically significant linear trend observed over the entire study period from 2001 to 2021. Adults aged鈥夆墺鈥�65 years, males, and those with lower education and household income levels showed a greater increase in the prevalence of type 2 diabetes than their counterparts. Among adults with a BMI of less than 23听kg/m2, a significant increase in the prevalence of lean type 2 diabetes between 2001 and 2021 was observed in all subgroups (all p for trend鈥�<鈥�0.05) except for rural residents (p for trend鈥�=鈥�0.2973). However, females (4.7鈥�6.4%; +36.2%) showed a greater increase than males (10.8鈥�9.6%; +24.7%) and those with lower education (8.2鈥�13.8%; +68.3%) showed a similar increase relative to their counterparts (4.6鈥�7.6%; +65.2%) in the prevalence of type 2 diabetes. Among adults with a BMI of 23听kg/m2 or more, a significant increase in the prevalence of type 2 diabetes between 2001 and 2021 was observed in all subgroups (all p for trend鈥�<鈥�0.05) except for rural residents (p for trend鈥�=鈥�0.9677); adults aged 65 years and older, males, and those with lower education and household income levels showed a greater increase in the prevalence of type 2 diabetes than their counterparts.

Table听2 shows a comparison of the sociodemographic, lifestyle, and anthropometric characteristics between the lean and overweight/obese type 2 diabetes mellitus groups (T2DM groups) after adjusting for age, sex, and duration of diabetes. The mean age was higher in the lean T2DM group than in the overweight/obese T2DM group (65.6 vs. 60.5 years, p鈥�<鈥�0.0001). The lean T2DM group had a longer duration of diabetes (11.3 vs. 9.1 years, p鈥�=鈥�0.0002) and a higher proportion of recognition of type 2 diabetes (74.3 vs. 66.4%, p鈥�=鈥�0.0026) than the overweight/obese T2DM group. The lean T2DM group had a lower systolic (124.2 vs. 127.6 mmHg, p鈥�=鈥�0.0014) and diastolic (71.6 vs. 73.7 mmHg, p鈥�=鈥�0.0005) BPs, body weight (55.0 vs. 69.2听kg, p鈥�<鈥�0.0001), waist-to-height ratio (WHtR) (0.50 vs. 0.58, p鈥�<鈥�0.0001), body fat mass (25.6 vs. 31.3%, p鈥�<鈥�0.0001), appendicular skeletal muscle index (ASMI, calculated as ASM/height2) (6.5 vs. 7.5听kg/m2,p鈥�<鈥�0.0001), handgrip strength (26.6 vs. 28.6听kg, p鈥�=鈥�0.0004), and proportion of participants who attempted weight control (12.6 vs. 44.2%, p鈥�<鈥�0.0001) than the overweigh/obese T2DM group. There were no significant differences in other socioeconomic or dietary characteristics between the two groups.

Table 2 Comparison of general characteristics by BMI category among adults with T2DM, KNHANES 2019鈥�2021 (n鈥�=鈥�2,284)
Full size table

Table听3 shows a comparison of the medical history, comorbidities, and biochemical variables between the lean and overweight/obese T2DM groups after adjusting for age, sex, and duration of diabetes. For medical history and comorbidities, the lean T2DM group had a lower prevalence of hypertension (49.3 vs. 71.2%, p鈥�<鈥�0.0001), dyslipidemia (51.2 vs. 61.9%, p鈥�=鈥�0.0022), and metabolic syndrome (52.6 vs. 88.8%, p鈥�<鈥�0.0001) than the overweight/obesity T2DM group. There were no significant differences in the prevalence of other chronic diseases between the two groups. For biochemical variables, the lean T2DM group exhibited a lower triglyceride level (121.1 vs. 150.6听mg/dL, p鈥�<鈥�0.0001), a lower urine protein positivity rate (16.5 vs. 22.0%, p鈥�=鈥�0.0179), and a higher HDL-cholesterol level (49.0 vs. 45.3听mg/dL, p鈥�<鈥�0.0001) than the overweight/obesity T2DM group. The lean T2DM group showed lower fasting insulin levels (6.9 vs. 11.6 碌U/mL, p鈥�<鈥�0.0001), HOMA-IR (2.3 vs. 4.0 p鈥�<鈥�0.0001), and HOMA-尾 (41.3 vs. 69.5, p鈥�<鈥�0.0001), indicating less insulin resistance and more insulin deficiency compared with the overweigh/obese T2DM group. No significant differences were noted in FPG, HbA1c, or LDL-cholesterol levels between the two groups.

Table 3 Comparison of comorbidities and biochemical profiles by BMI category among adults with T2DM, KNHANES 2019鈥�2021 (n鈥�=鈥�2,284)
Full size table

Discussion

The estimated prevalence of lean type 2 diabetes among Korean adults increased by 33.3% between 2001 and 2019鈥�2021, showing a similar extent of increase of type 2 diabetes in overweight and obese individuals (+鈥�33.3% vs. +34.7%, respectively). An increase in the prevalence of lean type 2 diabetes was observed across all subgroups except for rural residents and those with the lowest household income. The rate of increase in the prevalence of lean type 2 diabetes was more pronounced among females, while the rate of increase in the prevalence of type 2 diabetes among those were overweight or obese was more pronounced among males than their counterparts. While the overweight/obese T2DM group showed a higher prevalence of hypertension, dyslipidemia, and metabolic syndrome, the lean T2DM group tended to be older, have a longer diabetes duration, lower insulin levels, and lower ASMI and muscle strength, despite more exercise.

Lean type 2 diabetes is notably more common in Asian populations, accounting for up to 50% of patients with diabetes [20, 21]. Previous epidemiological studies have indicated that the prevalence of diabetes in normal-weight individuals is increasing, even in Western countries. In the United States, a study using Behavioral Risk Factor Surveillance System data reported that the rate of increase in diabetes prevalence was more pronounced among lean adults (BMI鈥�<鈥�25听kg/m2) than those who were overweight or obese (BMI鈥夆墺鈥�25听kg/m2) between 2015 and 2020 (+鈥�17.8% vs. +2.1%) [22]. However, the study used data collected through a telephone survey; hence, the BMI classification may not be as accurate as anthropometric measurements. A study using anthropometric measurements in the National Health and Nutrition Examination Survey indicated that the increase in diabetes prevalence was marginally higher in the overweight/obesity group (BMI 25.0鈥�34.9听kg/m2) than normal-weight group (BMI 18.5鈥�24.9听kg/m2) between 1999 and 2000 and 2017鈥�2018 (+鈥�1.7% vs. +1.8鈥�2.7%, respectively); however, the difference was not significant [23]. Overall, the increase in the prevalence of lean diabetes seems to be on par with that of overweight or obese diabetes.

In our subgroup analyses, both lean and overweight/obese groups showed similar upward patterns of diabetes trends across subgroups, except for gender. This gender difference is partially explained by a complex interplay of environmental and sociocultural factors. A study using middle-aged Korean adults reported that physical inactivity and unhealthy diets among women while alcohol consumption among men are significantly associated with an increased risk of metabolic syndrome [24]. Another study using Korean adults found that women with higher educational levels tended to overestimate their weight, while men were less sensitive to weight gain. This indicates that pressure related to weight can lead to abnormal weight management practices, such as irregular eating habits, which may negatively impact metabolic health [25]. Moreover, previous studies suggest that hormonal and metabolic factors contribute to the significant decline in HDL cholesterol with increasing glycaemia in women, while higher levels of visceral fat and related insulin resistance are more pronounced in men [26, 27]. These various genetic and environmental factors may have contributed to the prominent increase in lean diabetes among Korean women.

The main features of patients with lean type 2 diabetes are a greater insulin secretion defect and less insulin resistance than those with type 2 diabetes associated with obesity [28]. We also found that fasting insulin levels, HOMA-IR, and HOMA-尾 are lower in lean type 2 diabetes compared with overweight/obese type 2 diabetes. Meta-analyses of genome-wide association studies identified novel genetic variants in East Asian individuals [29]. These variants include genes encoding transcripts in the pancreas and non-coding RNAs that play roles in islet beta cell functions [29]. Moreover, several genetic variants expressed in human islet cells, such as glucokinase, were associated with progressive deterioration of glucose tolerance in the Korean population in a community-based prospective cohort study [30]. These genetic susceptibilities predispose individuals to reduced beta cell function and may help explain the pathophysiology underlying the development of type 2 diabetes in individuals with normal BMIs.

It has been also suggested that lean type 2 diabetes is associated with sarcopenia [31]. Sarcopenia, characterized by reduced muscle mass and function, is associated with impaired FPG levels and diabetes [32, 33]. Recent evidence has shown that sarcopenia is more prevalent in patients with type 2 diabetes, and low muscle mass is associated with poor glucose disposal, leading to the development of diabetes [34]. A decreased relative muscle mass is negatively associated with the development of type 2 diabetes even in younger individuals [35]. The ASMI and hand grip strength are important diagnostic tools for assessing sarcopenia according to the Asian Working Group on Sarcopenia [36]. In this study, the ASMI and hand grip strength were significantly lower in patients with lean type 2 diabetes after adjusting for age, suggesting a possible association between sarcopenia and lean type 2 diabetes among Korean adults.

In recent decades, the treatment guidelines for type 2 diabetes have predominantly focused on overweight or obese individuals. Weight loss effectiveness is one of the primary considerations in the selection of hypoglycemic agents. Weight loss strategies, including behavioral, pharmacological, and surgical interventions, are recommended for the prevention and treatment of type 2 diabetes in overweight and obese individuals [37]. However, there is little evidence regarding the impact of weight loss on the clinical course of type 2 diabetes in lean individuals. Considering the findings of this study, it may be beneficial to emphasize the importance of protein intake and resistance exercise in lifestyle interventions for individuals with lean diabetes. Type 2 diabetes is characterized by a heterogeneous phenotype that includes both insulin resistance and insulin deficiency, with lean type 2 diabetes specifically being more prominently associated with beta cell dysfunction. Although the mechanisms of beta cell dysfunction differ between type 1 diabetes and type 2 diabetes, this suggests the potential benefit of developing therapeutic strategies to delay beta cell dysfunction not only in type 1 diabetes but also in type 2 diabetes. Furthermore, in pharmacotherapy strategies, selecting a hypoglycemic agent aimed at weight loss may not be beneficial for individuals with lean diabetes. Additionally, Asian people with type 2 diabetes, characterized by a leaner body habitus, exhibit distinct response to hypoglycemic medications compared to populations in Western countries [38]. The findings of our study indicate that the prevalence of lean type 2 diabetes is continuously increasing with similar extents as obesity-related type 2 diabetes. Moreover, the divergent pathophysiology and clinical manifestations observed between lean and obese patients with type 2 diabetes necessitate the development of distinct therapeutic approaches.

This study has few limitations. First, we could not distinguish between type 1 diabetes mellitus, type 2 diabetes, and Maturity Onset Diabetes of the Young (MODY), because the KNHANES did not collect such information. However, we excluded possible patients with type 1 diabetes and those who were diagnosed with or injected insulin before 19 years of age. Furthermore, given the low prevalence of type 1 diabetes in Korea, which is less than 0.05% [39], and the prevalence of MODY, approximately 1.1% among non-type 1 diabetes cases [40], it is anticipated that its influence on the analysis may have been limited. Second, causal inferences regarding several clinical characteristics of type 2 diabetes according to BMI categories may be precluded because of the use of a series of cross-sectional studies. Despite the limited causal link, a comparison of multiple clinical profiles between lean type 2 diabetes and type 2 diabetes in overweight or obese individuals may provide an overview of the pathophysiology and clinical course of lean type 2 diabetes. Third, this study was conducted on Korean adults, which limits its applicability to other study settings. Future studies in other populations are needed to further investigate the characteristics of lean type 2 diabetes. Nevertheless, we identified the 20-year trends in the prevalence of lean type 2 diabetes in an Asian country, a highly prevalent area of lean type 2 diabetes, using nationally representative data collected using standardized protocols.

In conclusion, in a nationally representative sample of Korean adults, the prevalence of lean type 2 diabetes increased significantly between 2001 and 2019鈥�2021, with a rate of change comparable to that in type 2 diabetes in overweight or obese individuals. This upward trend in the prevalence of lean type 2 diabetes was more prominent in females, while the increase among those who were overweight or obese was more prominent in males than their counterparts. Participants with lean type 2 diabetes showed lower insulin levels, muscle mass, and strength. These findings underscore the necessity for an increased focus on lean type 2 diabetes and the development of specialized management strategies for this specific population.

Data availability

The datasets analyzed during the current study are available in the [KNHANES] repository, .

References

  1. Magliano D, Boyko E. IDF Diabetes Atlas 10th edition scientific committee. IDF DIABETES ATLAS [Internet]. Brussels: International Diabetes Federation; 2021.

    听

  2. George AM, Jacob AG, Fogelfeld L. Lean diabetes mellitus: an emerging entity in the era of obesity. World J diabetes. 2015;6(4):613.

    听 听 听 听

  3. Salvatore T, Galiero R, Caturano A, Rinaldi L, Criscuolo L, Di Martino A, Albanese G, Vetrano E, Catalini C, Sardu C et al. Current Knowledge on the Pathophysiology of Lean/Normal-Weight Type 2 Diabetes. Int J Mol Sci 2022, 24(1).

  4. Kibirige D, Sekitoleko I, Lumu W, Jones AG, Hattersley AT, Smeeth L, Nyirenda MJ. Understanding the pathogenesis of lean non-autoimmune diabetes in an African population with newly diagnosed diabetes. Diabetologia. 2022;65(4):675鈥�83.

    听 CAS听 听 听 听

  5. Hartmann B, Lanzinger S, Bramlage P, Gro脽 F, Danne T, Wagner S, Krakow D, Zimmermann A, Malcharzik C, Holl RW. Lean diabetes in middle-aged adults: a joint analysis of the German DIVE and DPV registries. PLoS ONE. 2017;12(8):e0183235.

    听 听 听 听

  6. Shavana S, Khan ZH, Anandan H. To Compare The Presenting Complications of the Lean With Normal Weight/Obese Type 2 Diabetes Patients. Annals Int Med Dent Res, 3(5):1.

  7. Coleman NJ, Miernik J, Philipson L, Fogelfeld L. Lean versus obese diabetes mellitus patients in the United States minority population. J Diabetes Complicat. 2014;28(4):500鈥�5.

    听 听

  8. Barma PD, Ranabir S, Prasad L, Singh TP. Clinical and biochemical profile of lean type 2 diabetes mellitus. Indian J Endocrinol Metabol. 2011;15(Suppl1):S40.

    听

  9. Teruya T, Sunagawa S, Mori A, Masuzaki H, Yanagida M. Markers for obese and non-obese Type 2 diabetes identified using whole blood metabolomics. Sci Rep. 2023;13(1):2460.

    听 CAS听 听 听 听

  10. Zhu Y, Sidell MA, Arterburn D, Daley MF, Desai J, Fitzpatrick SL, Horberg MA, Koebnick C, McCormick E, Oshiro C. Racial/ethnic disparities in the prevalence of diabetes and prediabetes by BMI: Patient Outcomes Research To Advance Learning (PORTAL) multisite cohort of adults in the US. Diabetes Care. 2019;42(12):2211鈥�9.

    听 听 听 听

  11. Gujral UP, Mohan V, Pradeepa R, Deepa M, Anjana RM, Narayan KM. Ethnic differences in the prevalence of diabetes in underweight and normal weight individuals: The CARRS and NHANES studies. Diabetes Res Clin Pract. 2018;146:34鈥�40.

    听 听 听 听

  12. Ong KL, Stafford LK, McLaughlin SA, Boyko EJ, Vollset SE, Smith AE, Dalton BE, Duprey J, Cruz JA, Hagins H. Global, regional, and national burden of diabetes from 1990 to 2021, with projections of prevalence to 2050: a systematic analysis for the Global Burden of Disease Study 2021. The Lancet 2023.

  13. Kweon S, Kim Y, Jang M-j, Kim Y, Kim K, Choi S, Chun C, Khang Y-H, Oh K. Data resource profile: the Korea national health and nutrition examination survey (KNHANES). Int J Epidemiol. 2014;43(1):69鈥�77.

    听 听 听 听

  14. Lee G, Chang J, Hwang S-s, Son JS, Park SM. Development and validation of prediction equations for the assessment of muscle or fat mass using anthropometric measurements, serum creatinine level, and lifestyle factors among Korean adults. Nutr Res Pract. 2020;15(1):95鈥�105.

    听 听 听 听

  15. Matthews DR, Hosker JP, Rudenski AS, Naylor B, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and 尾-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412鈥�9.

    听 CAS听 听 听

  16. Kim H-L, Lee EM, Ahn SY, Kim K-i, Kim HC, Kim JH, Lee H-Y, Lee JH, Park J-M, Cho EJ. The 2022 focused update of the 2018 Korean Hypertension Society Guidelines for the management of hypertension. Clin Hypertens. 2023;29(1):11.

    听 听 听 听

  17. Rhee EJ, Kim HC, Kim JH, Lee EY, Kim BJ, Kim EM, Song Y, Lim JH, Kim HJ, Choi S, et al. 2018 Guidelines for the management of dyslipidemia in Korea. Korean J Intern Med. 2019;34(5):1171.

    听 听 听 听

  18. Expert Panel on Detection E. Executive summary of the third report of the National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA. 2001;285(19):2486鈥�97.

    听 听

  19. Haam JH, Kim BT, Kim EM, Kwon H, Kang JH, Park JH, Kim KK, Rhee SY, Kim YH, Lee KY. Diagnosis of Obesity: 2022 Update of Clinical Practice Guidelines for Obesity by the Korean Society for the Study of Obesity. J Obes Metab Syndr 2023.

  20. Wang L, Peng W, Zhao Z, Zhang M, Shi Z, Song Z, Zhang X, Li C, Huang Z, Sun X, et al. Prevalence and Treatment of Diabetes in China, 2013鈥�2018. JAMA. 2021;326(24):2498鈥�506.

    听 听 听 听

  21. Bae JH, Han KD, Ko SH, Yang YS, Choi JH, Choi KM, Kwon HS, Won KC. Diabetes Fact Sheet in Korea 2021. Diabetes Metab J. 2022;46(3):417鈥�26.

    听 听 听 听

  22. Adesoba TP, Brown CC. Trends in the Prevalence of Lean Diabetes Among US Adults, 2015鈥�2020. Diabetes Care. 2023;46(4):885鈥�9.

    听 听 听

  23. Wang L, Li X, Wang Z, Bancks MP, Carnethon MR, Greenland P, Feng Y-Q, Wang H, Zhong VW. Trends in prevalence of diabetes and control of risk factors in diabetes among US adults, 1999鈥�2018. JAMA. 2021;326(8):704鈥�16.

    听 听

  24. Yoon J, Kim J, Son H. Gender differences of health behaviors in the risk of metabolic syndrome for middle-aged adults: a national cross-sectional study in South Korea. Int J Environ Res Public Health. 2021;18(7):3699.

    听 听 听 听

  25. Lee Y. Slender women and overweight men: gender differences in the educational gradient in body weight in South Korea. Int J Equity Health. 2017;16:1鈥�18.

    听 听

  26. Zheng J, Gao Y, Jing Y, Zhou X, Shi Y, Li Y, Wang L, Wang R, Li M, Xiao C. Gender differences in the relationship between plasma lipids and fasting plasma glucose in non-diabetic urban Chinese population: a cross-section study. Front Med. 2014;8:477鈥�83.

    听 听 听

  27. Washirasaksiri C, Srivanichakorn W, Godsland IF, Kositamongkol C, Chariyalertsak S, Kessomboon P, Assanangkornchai S, Taneepanichskul S, Neelapaichit N, Phisalprapa P. Increasing glycaemia is associated with a significant decline in HDL cholesterol in women with prediabetes in two national populations. Sci Rep. 2021;11(1):12194.

    听 CAS听 听 听 听

  28. Gudipaty L, Rosenfeld NK, Fuller CS, Cuchel M, Rickels MR. Different 尾-cell secretory phenotype in non鈥恛bese compared to obese early type 2 diabetes. Diab/Metab Res Rev. 2020;36(5):e3295.

    听 CAS听 听

  29. Spracklen CN, Horikoshi M, Kim YJ, Lin K, Bragg F, Moon S, Suzuki K, Tam CH, Tabara Y, Kwak S-H. Identification of type 2 diabetes loci in 433,540 East Asian individuals. Nature. 2020;582(7811):240鈥�5.

    听 CAS听 听 听 听

  30. Ohn JH, Kwak SH, Cho YM, Lim S, Jang HC, Park KS, Cho NH. 10-year trajectory of beta-cell function and insulin sensitivity in the development of type 2 diabetes: a community-based prospective cohort study. Lancet Diabetes Endocrinol. 2016;4(1):27鈥�34.

    听 CAS听 听 听

  31. Sugimoto K, Tabara Y, Ikegami H, Takata Y, Kamide K, Ikezoe T, Kiyoshige E, Makutani Y, Onuma H, Gondo Y, et al. Hyperglycemia in non-obese patients with type 2 diabetes is associated with low muscle mass: The Multicenter Study for Clarifying Evidence for Sarcopenia in Patients with Diabetes Mellitus. J Diabetes Investig. 2019;10(6):1471鈥�9.

    听 CAS听 听 听 听

  32. Chen H, Huang X, Dong M, Wen S, Zhou L, Yuan X. The Association Between Sarcopenia and Diabetes: From Pathophysiology Mechanism to Therapeutic Strategy. Diabetes Metabolic Syndrome Obes 2023:1541鈥�54.

  33. Mesinovic J, Zengin A, De Courten B, Ebeling PR, Scott D. Sarcopenia and type 2 diabetes mellitus: a bidirectional relationship. Diabetes metabolic syndrome obesity: targets therapy 2019:1057鈥�72.

  34. Marcotte-Ch茅nard A, Oliveira B, Little JP, Candow DG. Sarcopenia and type 2 diabetes: Pathophysiology and potential therapeutic lifestyle interventions. Diabetes Metabolic Syndrome: Clin Res Reviews 2023:102835.

  35. Hong S, Chang Y, Jung HS, Yun KE, Shin H, Ryu S. Relative muscle mass and the risk of incident type 2 diabetes: A cohort study. PLoS ONE. 2017;12(11):e0188650.

    听 听 听 听

  36. Chen L-K, Woo J, Assantachai P, Auyeung T-W, Chou M-Y, Iijima K, Jang HC, Kang L, Kim M, Kim S. Asian Working Group for Sarcopenia: 2019 consensus update on sarcopenia diagnosis and treatment. J Am Med Dir Assoc. 2020;21(3):300鈥�7. e302.

    听 听 听

  37. American Diabetes Association Professional Practice C. 8. Obesity and Weight Management for the Prevention and Treatment of Type 2 Diabetes: Standards of Care in Diabetes-2024. Diabetes Care. 2024;47(Suppl 1):S145鈥�57.

    听 听

  38. Ke C, Narayan KMV, Chan JCN, Jha P, Shah BR. Pathophysiology, phenotypes and management of type 2 diabetes mellitus in Indian and Chinese populations. Nat Rev Endocrinol. 2022;18(7):413鈥�32.

    听 CAS听 听 听 听

  39. Lee Y-B, Han K, Kim B, Jin S-M, Lee S-E, Jun JE, Ahn J, Kim G, Kim JH. High proportion of adult cases and prevalence of metabolic syndrome in type 1 diabetes mellitus population in Korea: a nationwide study. Diabetes Metabolism J. 2019;43(1):76鈥�89.

    听 听

  40. Park SS, Jang SS, Ahn CH, Kim JH, Jung HS, Cho YM, Lee YA, Shin CH, Chae JH, Kim JH. Identifying pathogenic variants of monogenic diabetes using targeted panel sequencing in an East Asian population. J Clin Endocrinol Metabolism. 2019;104(9):4188鈥�98.

    听 听

Acknowledgements

We would like to thank the Academic Clinical Research Operating and Supporting System of the Chungnam National University Hospital Biomedical Research Institute for their collaboration on this research.

Funding

J.H.L was supported by Chungnam National University Hospital Research Fund, 2019. The funders had no role in the study design, data collection and analysis, decision to publish, or manuscript preparation.

Author information

Authors and Affiliations

  1. Department of Internal Medicine, Chungnam National University Sejong Hospital, Sejong, South Korea

    Ji Min Kim听&听Kyoung Hye Joung

  2. Department of Internal Medicine, Chungnam National University Hospital, 266 Munhwa-ro, Jung-gu, Daejeon, 35015, South Korea

    Hyun Jin Kim,听Bon Jeong Ku听&听Ju Hee Lee

  3. Department of Health Care Policy Research, Korea Institute for Health and Social Affairs, 370 Sicheong-daero, Sejong, 30147, South Korea

    Sukyoung Jung

Authors
  1. Ji Min Kim

    You can also search for this author in 听

  2. Kyoung Hye Joung

    You can also search for this author in 听

  3. Hyun Jin Kim

    You can also search for this author in 听

  4. Bon Jeong Ku

    You can also search for this author in 听

  5. Sukyoung Jung

    You can also search for this author in 听

  6. Ju Hee Lee

    You can also search for this author in 听

Contributions

Conceptualization: J.M.K., J.H.L.听Methodology: S.J.听Formal analysis: S.J.听Data curation: S.J.听Writing 鈥� original draft: J.M.K., S.J., J.H.L.听Writing 鈥� reviewing and editing: J.M.K., K.H.J., H.J.K, B.J.K, S.J., J.H.L.听Visualization: J.M.K., S.J.听Supervision: S.J., J.H.L.听S.J. is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding authors

Correspondence to Sukyoung Jung or Ju Hee Lee.

Ethics declarations

Ethics approval and consent to participate

This study was reviewed and deemed exempt by the Institutional Review Board (IRB) of the Chungnam National University Sejong Hospital (IRB number: 2023-09-005) because only publicly available and anonymized data were used.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher鈥檚 note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article鈥檚 Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article鈥檚 Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit .

About this article

Cite this article

Kim, J.M., Joung, K.H., Kim, H.J. et al. Lean diabetes: 20-year trends in its prevalence and clinical features among Korean adults. 樱花视频 24, 3554 (2024). https://doi.org/10.1186/s12889-024-21034-2

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12889-024-21034-2

Keywords

樱花视频

ISSN: 1471-2458

Contact us