DIABETICMedicine DOI: 10.1111/dme.12527
Research: Epidemiology Association between changes in body composition and risk of developing Type 2 diabetes in Koreans C.-H. Kim1, H.-K. Kim2, E.-H. Kim2, S.-J. Bae2 and J.-Y. Park3 1 Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University College of Medicine, Bucheon, 2Health Screening and Promotion Center, Asan Medical Center, Seoul and 3Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Ulsan College of Medicine, Seoul, Korea
Accepted 19 June 2014
Abstract Aims
To examine the effects of longitudinal changes in fat mass or lean body mass on risk of Type 2 diabetes in Korean
adults. Participants included 18 687 Korean adults (aged 20–79 years) who underwent routine medical check-ups in 2007–2008 and again in 2011–2012 with a mean (range) of 4.3 (3.0–5.7) years interval. Total fat, fat-free, and soft fat-free masses were determined using bioelectrical impedance.
Methods
A total of 692 subjects (3.7%) developed Type 2 diabetes during follow-up. Those who developed diabetes had a greater increase in percent body fat (2.9 3.0 vs 2.6 3.2 percentage points, P = 0.043), as well as greater decreases in percent fat-free mass ( 3.0 3.3 vs 2.7 3.3 percentage points, P = 0.008) and percent soft fat-free mass ( 2.8 3.1 vs 2.4 3.1 percentage points, P = 0.003) compared with those who did not develop diabetes. In multiple logistic regression analysis, an increase in total fat mass of > 10% was associated with an increased odds ratio for diabetes (1.29, 1.05–1.60), and a decreased total fat mass was associated with lower odds ratio (0.75, 0.58–0.96). A loss of total fat-free mass of > 5% (odds ratio 1.08, 0.90–1.30) or an increase in total fat-free mass (odds ratio 0.96, 0.71–1.28) was not significantly associated with the risk of diabetes after adjustments for baseline waist circumference and glucose levels.
Results
Conclusions These results show that changes in total body fat mass, but not lean body mass, are associated with development of Type 2 diabetes, independently of baseline measures of general or central obesity.
Diabet. Med. 31, 1393–1398 (2014)
Introduction Increased fat mass is a well-established independent risk factor for Type 2 diabetes, as shown in several cross-sectional and longitudinal studies [1,2]; however, low muscle mass may also be an important factor in insulin resistance and for the risk of Type 2 diabetes, as muscle is the primary tissue contributing to whole-body insulin-mediated glucose disposal [3]. Indeed, cross-sectional studies have shown that decreased muscle mass is associated with insulin resistance and dysglycaemia [3–5], but the association between longitudinal changes in fat mass or lean body mass and the risk of Type 2 diabetes remains unclear. Previous studies have reported that weight gain is associated with an increase, while weight loss is associated with a decrease in the risk of developing Type 2 diabetes [6,7]. BMI Correspondence to: Hong-Kyu Kim. E-mail: [email protected]
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
has been routinely used in clinical practice as a measure of obesity because it correlates well with body fat mass [8]; however, BMI cannot differentiate between fat and lean mass. It is unclear, therefore, whether increases in fat mass or decreases in lean body mass are primarily responsible for increasing the risk of Type 2 diabetes, as changes in body fat mass and lean body mass usually occur simultaneously in an individual. For instance, body composition changes with aging are characterized by loss of lean body mass and increased fat mass. Furthermore, decreased muscle mass accompanied by an increase in fat mass, termed sarcopenic obesity, is thought to increase the risk of cardiometabolic diseases synergistically [9,10], but it remains unknown whether small increases or decreases in fat mass or lean body mass within the normal range of BMI are associated with the risk of Type 2 diabetes. To date, there has been a paucity of data examining the effects of longitudinal changes in muscle or fat mass on the risk of Type 2 diabetes. In the present study, we assessed the
1393
DIABETICMedicine
What’s new? • This study examined the association between longitudinal changes in body composition and the risk of developing Type 2 diabetes in a large cohort of Korean adults. • An increase or decrease in total body fat mass is associated with the risk of Type 2 diabetes independently of baseline measures of general or central obesity. • An increase or decrease in lean body mass is not independently associated with risk of Type 2 diabetes. association between unintentional changes in body composition and the risk of developing Type 2 diabetes in Korean adults.
Patients and methods We retrospectively assessed clinical and laboratory data obtained from 19 748 patients (aged 20–79 years) who visited the Health Promotion Center at Asan Medical Center (Seoul, Korea) for medical examinations in 2007–2008 and underwent follow-up examinations in 2011–2012. Patients with a history of physician-diagnosed diabetes mellitus, those who were taking anti-hyperglycaemic medications, and those with fasting blood glucose concentrations ≥7.0 mmol/l or HbA1c ≥48 mmol/mol (6.5%) at baseline were excluded. After the exclusion of an additional 1061 patients with a follow-up interval 10% was associated with a higher OR for diabetes (OR 1.29, 95% CI 1.05–1.60), and a decrease in total fat mass was associated with a lower OR (OR 0.75, 95% CI 0.58–0.96) after adjusting for age, sex, family history of diabetes, physical activity, waist circumference and fasting glucose level at baseline (Table 3). A loss of total fat-free mass of > 5% was associated with a higher OR for diabetes in minimally adjusted models (age-/sex-adjusted OR 1.39, 95% CI 1.17–1.65), but this association became insignificant after adjustment for family history of diabetes, physical activity, waist circumference and baseline glucose level (OR 1.08, 95% CI 0.90–1.30). An increase in total fat-free mass was not significantly protective against the risk of diabetes (OR 0.96, 95% CI
0.71–1.28). As our study population had a wide age range (20– 79 years) and the effects of body composition change could potentially be different by age, we analysed the data separately in subgroups of age < 50 years and > 50 years. The results were similar between the two age groups, although statistical significance was marginal in the subgroup of age > 50 years (Table 4). When we divided the participants into four groups according to increase/decrease of total fat mass/fat-free mass, participants with an increased total fat mass/decreased total fat-free mass had ~1.6-fold (OR 1.59, 95% CI 1.27–2.00) increased risk of diabetes compared with those with a decreased total fat mass/increased total fat-free mass group after adjusting for age, sex, and baseline waist circumference. The OR was also significantly higher in patients with increases in both total fat mass and total fat-free mass (OR 1.31, 95% CI 1.06–1.63), but was not significant for those with decreases in both total fat mass and total fat-free mass (OR 1.30, 95% CI 0.97–1.76). When we used soft fat-free mass (excluding bone mass) instead of total fat-free mass in the analysis, the results were basically the same (data not shown). To examine whether changes in central adiposity were associated with the risk of Type 2 diabetes, we analysed the risk of Type 2 diabetes according to changes in waist circumference. An increase in waist circumference >5% was associated with an increase in Type 2 diabetes risk (adjusted OR 1.91, 95% CI 1.55–2.34), while a decrease in waist circumference > 5% was associated with a decrease in risk (OR 0.64, 95% CI 0.46–0.87) after adjustment for age, sex, physical activity, family history of diabetes, baseline waist circumference and fasting glucose level.
Discussion In the present study, we found that an increase in total body fat mass was associated with the development of Type 2
Table 1 Baseline characteristics of participants who did and did not develop diabetes over 4.3 years
Age, years Sex: M/F, % BMI, kg/m2 Waist circumference, cm Systolic blood presssure, mmHg Diastolic blood pressure, mmHg Fasting glucose, mmol/l HbA1c, mmol/mol (%) Total cholesterol, mmol/l Triglycerides, mmol/l HDL cholesterol, mmol/l Fasting insulin, pmol/l Regular exercise: ≥ 3 times/week, % Alcohol consumption: ≥ 3 times/week, % Current smoker, % Data are summarized as mean
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
SD
No diabetes (n = 17 995)
Diabetes (n = 692)
P
48.5 61/39 23.7 81.6 116 73 5.3 34 4.72 1.38 1.47 48.1 43.4 12.6 21.3
51.7 76/24 25.6 87.7 121 76 6.0 41 4.79 1.85 1.32 62.5 40.2 19.3 37.1
Research: Epidemiology Association between changes in body composition and risk of developing Type 2 diabetes in Koreans C.-H. Kim1, H.-K. Kim2, E.-H. Kim2, S.-J. Bae2 and J.-Y. Park3 1 Division of Endocrinology and Metabolism, Department of Internal Medicine, Soonchunhyang University College of Medicine, Bucheon, 2Health Screening and Promotion Center, Asan Medical Center, Seoul and 3Division of Endocrinology and Metabolism, Department of Internal Medicine, University of Ulsan College of Medicine, Seoul, Korea
Accepted 19 June 2014
Abstract Aims
To examine the effects of longitudinal changes in fat mass or lean body mass on risk of Type 2 diabetes in Korean
adults. Participants included 18 687 Korean adults (aged 20–79 years) who underwent routine medical check-ups in 2007–2008 and again in 2011–2012 with a mean (range) of 4.3 (3.0–5.7) years interval. Total fat, fat-free, and soft fat-free masses were determined using bioelectrical impedance.
Methods
A total of 692 subjects (3.7%) developed Type 2 diabetes during follow-up. Those who developed diabetes had a greater increase in percent body fat (2.9 3.0 vs 2.6 3.2 percentage points, P = 0.043), as well as greater decreases in percent fat-free mass ( 3.0 3.3 vs 2.7 3.3 percentage points, P = 0.008) and percent soft fat-free mass ( 2.8 3.1 vs 2.4 3.1 percentage points, P = 0.003) compared with those who did not develop diabetes. In multiple logistic regression analysis, an increase in total fat mass of > 10% was associated with an increased odds ratio for diabetes (1.29, 1.05–1.60), and a decreased total fat mass was associated with lower odds ratio (0.75, 0.58–0.96). A loss of total fat-free mass of > 5% (odds ratio 1.08, 0.90–1.30) or an increase in total fat-free mass (odds ratio 0.96, 0.71–1.28) was not significantly associated with the risk of diabetes after adjustments for baseline waist circumference and glucose levels.
Results
Conclusions These results show that changes in total body fat mass, but not lean body mass, are associated with development of Type 2 diabetes, independently of baseline measures of general or central obesity.
Diabet. Med. 31, 1393–1398 (2014)
Introduction Increased fat mass is a well-established independent risk factor for Type 2 diabetes, as shown in several cross-sectional and longitudinal studies [1,2]; however, low muscle mass may also be an important factor in insulin resistance and for the risk of Type 2 diabetes, as muscle is the primary tissue contributing to whole-body insulin-mediated glucose disposal [3]. Indeed, cross-sectional studies have shown that decreased muscle mass is associated with insulin resistance and dysglycaemia [3–5], but the association between longitudinal changes in fat mass or lean body mass and the risk of Type 2 diabetes remains unclear. Previous studies have reported that weight gain is associated with an increase, while weight loss is associated with a decrease in the risk of developing Type 2 diabetes [6,7]. BMI Correspondence to: Hong-Kyu Kim. E-mail: [email protected]
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
has been routinely used in clinical practice as a measure of obesity because it correlates well with body fat mass [8]; however, BMI cannot differentiate between fat and lean mass. It is unclear, therefore, whether increases in fat mass or decreases in lean body mass are primarily responsible for increasing the risk of Type 2 diabetes, as changes in body fat mass and lean body mass usually occur simultaneously in an individual. For instance, body composition changes with aging are characterized by loss of lean body mass and increased fat mass. Furthermore, decreased muscle mass accompanied by an increase in fat mass, termed sarcopenic obesity, is thought to increase the risk of cardiometabolic diseases synergistically [9,10], but it remains unknown whether small increases or decreases in fat mass or lean body mass within the normal range of BMI are associated with the risk of Type 2 diabetes. To date, there has been a paucity of data examining the effects of longitudinal changes in muscle or fat mass on the risk of Type 2 diabetes. In the present study, we assessed the
1393
DIABETICMedicine
What’s new? • This study examined the association between longitudinal changes in body composition and the risk of developing Type 2 diabetes in a large cohort of Korean adults. • An increase or decrease in total body fat mass is associated with the risk of Type 2 diabetes independently of baseline measures of general or central obesity. • An increase or decrease in lean body mass is not independently associated with risk of Type 2 diabetes. association between unintentional changes in body composition and the risk of developing Type 2 diabetes in Korean adults.
Patients and methods We retrospectively assessed clinical and laboratory data obtained from 19 748 patients (aged 20–79 years) who visited the Health Promotion Center at Asan Medical Center (Seoul, Korea) for medical examinations in 2007–2008 and underwent follow-up examinations in 2011–2012. Patients with a history of physician-diagnosed diabetes mellitus, those who were taking anti-hyperglycaemic medications, and those with fasting blood glucose concentrations ≥7.0 mmol/l or HbA1c ≥48 mmol/mol (6.5%) at baseline were excluded. After the exclusion of an additional 1061 patients with a follow-up interval 10% was associated with a higher OR for diabetes (OR 1.29, 95% CI 1.05–1.60), and a decrease in total fat mass was associated with a lower OR (OR 0.75, 95% CI 0.58–0.96) after adjusting for age, sex, family history of diabetes, physical activity, waist circumference and fasting glucose level at baseline (Table 3). A loss of total fat-free mass of > 5% was associated with a higher OR for diabetes in minimally adjusted models (age-/sex-adjusted OR 1.39, 95% CI 1.17–1.65), but this association became insignificant after adjustment for family history of diabetes, physical activity, waist circumference and baseline glucose level (OR 1.08, 95% CI 0.90–1.30). An increase in total fat-free mass was not significantly protective against the risk of diabetes (OR 0.96, 95% CI
0.71–1.28). As our study population had a wide age range (20– 79 years) and the effects of body composition change could potentially be different by age, we analysed the data separately in subgroups of age < 50 years and > 50 years. The results were similar between the two age groups, although statistical significance was marginal in the subgroup of age > 50 years (Table 4). When we divided the participants into four groups according to increase/decrease of total fat mass/fat-free mass, participants with an increased total fat mass/decreased total fat-free mass had ~1.6-fold (OR 1.59, 95% CI 1.27–2.00) increased risk of diabetes compared with those with a decreased total fat mass/increased total fat-free mass group after adjusting for age, sex, and baseline waist circumference. The OR was also significantly higher in patients with increases in both total fat mass and total fat-free mass (OR 1.31, 95% CI 1.06–1.63), but was not significant for those with decreases in both total fat mass and total fat-free mass (OR 1.30, 95% CI 0.97–1.76). When we used soft fat-free mass (excluding bone mass) instead of total fat-free mass in the analysis, the results were basically the same (data not shown). To examine whether changes in central adiposity were associated with the risk of Type 2 diabetes, we analysed the risk of Type 2 diabetes according to changes in waist circumference. An increase in waist circumference >5% was associated with an increase in Type 2 diabetes risk (adjusted OR 1.91, 95% CI 1.55–2.34), while a decrease in waist circumference > 5% was associated with a decrease in risk (OR 0.64, 95% CI 0.46–0.87) after adjustment for age, sex, physical activity, family history of diabetes, baseline waist circumference and fasting glucose level.
Discussion In the present study, we found that an increase in total body fat mass was associated with the development of Type 2
Table 1 Baseline characteristics of participants who did and did not develop diabetes over 4.3 years
Age, years Sex: M/F, % BMI, kg/m2 Waist circumference, cm Systolic blood presssure, mmHg Diastolic blood pressure, mmHg Fasting glucose, mmol/l HbA1c, mmol/mol (%) Total cholesterol, mmol/l Triglycerides, mmol/l HDL cholesterol, mmol/l Fasting insulin, pmol/l Regular exercise: ≥ 3 times/week, % Alcohol consumption: ≥ 3 times/week, % Current smoker, % Data are summarized as mean
ª 2014 The Authors. Diabetic Medicine ª 2014 Diabetes UK
SD
No diabetes (n = 17 995)
Diabetes (n = 692)
P
48.5 61/39 23.7 81.6 116 73 5.3 34 4.72 1.38 1.47 48.1 43.4 12.6 21.3
51.7 76/24 25.6 87.7 121 76 6.0 41 4.79 1.85 1.32 62.5 40.2 19.3 37.1
