General characteristics of study participants
The general characteristics of the study subjects according to metabolically healthy and unhealthy phenotypes were shown in Table1. In total, 241 women aged 18–48 years, mean± SD age of 35.32±8.68 years, participated in our study. Among these, 78.99% were married and 1.26%, 10.50%, 38.66%, and 49.58%, respectively, were illiterate, under diploma education level, diploma education level, and bachelor and a higher academic degree. A significant difference was observed among the study participants in terms of their economic status (p=0.02). After controlling for potential confounders (age, physical activity (PA), energy intake, and BMI, this significance disappeared. The prevalence of sarcopenic obesity was 7.88%. The aforementioned demographic characteristics and prevalence of sarcopenic obesity were marginally different across the two groups (p=0.06). However, after adjusting for potential confounders, a significant difference was observed between the two groups (p=0.04). Subjects in the MUO group had a significantly higher body weight, BMI, WC, body fat mass (BFM), and visceral fat area (VFA) compared to subjects in the metabolically healthy (MHO) group (p <0.001). Similar findings were observed after adjusting for potential confounding variables. The FFM, fat mass index (FMI), and skeletal muscle mass (SMM) were significantly higher in the MUO group, p=0.004, p=0.001, and p=0.002 respectively. FBS was seen to be significantly higher in the MUO group after potential confounders were controlled for (p=0.03).TG, LDL, and total cholesterol were significantly higher (p<0.001) in the unhealthy group, while the levels of HDL were significantly higher (p<0.001) in the healthy group compared with the unhealthy group. After controlling for potential confounders, the results remained unchanged. A significant difference was also observed among the groups based on HOMA-IR (p<0.001) and insulin level (p=0.001), with the observed outcome remaining unchanged even after confounders were controlled for. While a non-significant difference was observed across the groups base on systolic blood pressure (SBP), a significantly higher diastolic blood pressure (DBP) was observed among the unhealthy group (p<0.001). (hs-CRP levels in the MUO group was significantly higher than in the MHO group (p<0.001). We, however, did not observe a statistically significant difference in physical activity among the two groups (p=0.33).
Table 1. General characteristics of study participants
variables
|
Metabolically Healthy
|
Metabolically Unhealthy
|
P-value*
|
P value‡**
|
(mean ± SD)
|
Demographic characteristic
|
Age (year) a
|
35.92 ±7.55
|
36.32 ±8.68
|
0.74
|
0.84
|
Marital status b
Single (%)
Married (%)
|
17 (34.0)
47 (25.0)
|
33 (66.0)
141 (75.0)
|
0.21
|
0.80
|
Education b
Illiterate (%)
Under diploma (%)
Diploma (%)
Bachelor and above (%)
|
1 (33.3)
4 (16.0)
24 (26.1)
35 (27.7)
|
2 (66.7)
21 (84.0)
68 (73.9)
83 (70.3)
|
0.57
|
0.73
|
Economic status b
Low class (%)
Middle class (%)
High class (%)
|
6 (19.4)
20 (48.8)
7 (29.2)
|
25 (80.6)
21 (51.2)
17 (70.8)
|
0.02
|
0.16
|
Sarcopenic obesity b
|
61 (27.5)
|
161 (72.5)
|
0.06
|
0.04
|
Non-sarcopenic obese (%)
|
Sarcopenic obese (%)
|
4 (21.1)
|
15 (78.9)
|
Anthropometry and Body Composition
|
Weight (kg) a
|
74.89 ±8.71
|
81.03 ±11.02
|
<0.001
|
<0.001
|
Height (cm) a
|
161.09±5.18
|
161.51±5.83
|
0.06
|
0.92
|
BMI (kg/m2) a
|
28.75±2.86
|
31.11±3.64
|
<0.001
|
<0.001
|
WC (cm) a
|
93.38±7.01
|
99.64±9.27
|
<0.001
|
<0.001
|
Body fat mass (kg) a
|
29.76±5.96
|
34.03±7.34
|
<0.001
|
<0.001
|
Visceral fat area(cm2) a
|
14.04±2.89
|
15.72±3.25
|
<0.001
|
0.001
|
Fat-free mass (kg) a
|
44.84±4.68
|
47.10±5.57
|
0.004
|
0.01
|
Skeletal muscle mass (kg)a
|
24.42±2.69
|
25.89±3.32
|
0.002
|
0.008
|
Fat free mass index (kg) a
|
17.26±1.21
|
18.75±9.88
|
0.23
|
0.27
|
Fat mass index (kg) a
|
11.65±2.62
|
13.06±2.78
|
0.001
|
<0.001
|
Blood Parameters
|
FBG (mg/dL) a
|
4.68±0.40
|
4.86±0.49
|
0.05
|
0.03
|
TG (mg/dL) a
|
0.90±0.28
|
1.52±0.82
|
<0.001
|
<0.001
|
HDL (mg/dL) a
|
1.34±0.24
|
1.14±0.26
|
<0.001
|
<0.001
|
LDL (mg/dL) a
|
2.19±0.50
|
2.53±0.62
|
<0.001
|
0.001
|
Total cholesterol (mg/dL) a
|
4.37±0.74
|
4.89±0.93
|
<0.001
|
0.003
|
Insulin (mIU/l)
|
1.13±0.24
|
1.24±0.22
|
0.001
|
0.01
|
HOMA index a
|
2.47±0.85
|
3.66±1.24
|
<0.001
|
<0.001
|
Blood Pressure
|
SBP (mmHg) a
|
109.01±12.44
|
112.66±13.92
|
0.06
|
0.18
|
DBP (mmHg) a
|
73.74±8.29
|
79.39±10.05
|
<0.001
|
0.007
|
Inflammatory parameter and other variables
|
Hs-CRP (mg/L) a
|
1.33±1.18
|
5.37±4.91
|
<0.001
|
<0.001
|
Physical activity (MET min/week) a
|
989.33±1078.53
|
1304.14±2404.33
|
0.33
|
0.29
|
SD, standard deviation; BMI, body mass index; WC, waist circumference; FBG, fasting blood glucose; TG, triglyceride; HDL, high-density lipoprotein; LDL, low-density lipoprotein; hs-CRP, High sensitive c-reactive protein; SBP, systolic blood pressure; DBP, diastolic blood pressure.
Data are presented as mean ± standard deviation (SD) or percent.
‡Collinear variables did not enter into the model and this P-value obtained from ANCOVA analysis
*p-value obtained from independent T-test
** p-value obtained from ANCOVA test, variable adjust for age, physical activity, energy intake, and BMI
Chi-square and analysis of variance were used for qualitative and quantitative variables respectively, and the p-value was set to <0.05.
a Mean ± SD
b Sample size (%)
Dietary intake of study subjects according to metabolic statuses
As shown in Table 2, the food groups, mean dietary intakes, and the mean nutrient intakes of the study participants were not statistically significantly different between the MHO and MUO groups even after controlling for potential confounding variables (p>0.05).
Table 2. Dietary intake of study subjects according to metabolic statuses
Variables
|
Metabolic healthy
|
Metabolic unhealthy
|
P-value*
|
P-value**
|
Mean SD
|
Mean SD
|
Food groups
|
Fruits (g/d)
|
508.45
|
373.30
|
505.83
|
352.66
|
0.96
|
0.34
|
Vegetables(g/d)
|
379.99
|
227.11
|
387.94
|
248.29
|
0.82
|
0.12
|
Cereal(g/d)
|
422.18
|
195.27
|
427.86
|
226.56
|
0.86
|
0.61
|
Whole grains(g/d)
|
58.64
|
53.41
|
65.77
|
62.43
|
0.42
|
0. 31
|
Refined grains(g/d)
|
363.54
|
203.95
|
362.45
|
211.23
|
0.97
|
0.43
|
Nuts(g/d)
|
15.23
|
16.91
|
19.06
|
28.03
|
0.96
|
0.67
|
Legumes(g/d)
|
51.64
|
55.38
|
48.23
|
34.54
|
0.57
|
0.62
|
Red meat (g/d)
|
21.61
|
17.70
|
22.53
|
19.75
|
0.74
|
0.60
|
White meat(g/d)
|
38.34
|
32.02
|
47.34
|
42.68
|
0.12
|
0.54
|
Salt and salty snacks(g/d)
|
36.79
|
38.78
|
41.18
|
47.54
|
0.51
|
0.99
|
Dairy(g/d)
|
274.24
|
234.54
|
301.84
|
214.28
|
0.39
|
0.70
|
Tea(g/d)
|
637.96
|
463.59
|
793.25
|
912.36
|
0.19
|
0.19
|
Dietary intake
|
Energy intake (kcal/d)
|
2505.26
|
727.89
|
2615.62
|
754.66
|
0.31
|
-
|
Carbohydrate (g/d)
|
362.65
|
126.42
|
370.55
|
117.74
|
0.65
|
0.20
|
Carbohydrate (% energy)
|
57.16
|
6.58
|
56.57
|
6.64
|
0.54
|
0.44
|
Protein (g/d)
|
83.30
|
26.04
|
89.26
|
28.26
|
0.14
|
0.58
|
Protein (% energy)
|
13.43
|
2.61
|
13.75
|
2.33
|
0.36
|
0.64
|
Fat (g/d)
|
88.66
|
27.49
|
94.91
|
33.61
|
0.18
|
0.33
|
Fat (% energy)
|
32.38
|
5.79
|
32.75
|
6.66
|
0.82
|
0.62
|
MUFA (g/d)
|
28.93
|
8.47
|
31.39
|
11.69
|
0.12
|
0.24
|
PUFA(g/d)
|
18.84
|
6.71
|
20.12
|
9.06
|
0.30
|
0.64
|
SFA (g/d)
|
25.99
|
9.76
|
28.43
|
11.60
|
0.13
|
0.14
|
Fiber (g/d)
|
45.18
|
20.05
|
44.30
|
17.86
|
0.74
|
0.15
|
Nutrients
|
Vitamin A (RAE)
|
729.58
|
351.47
|
795.26
|
428.82
|
0.27
|
0.84
|
Thiamine (mg/d)
|
2.01
|
0.65
|
2.05
|
0.63
|
0.63
|
0.39
|
Riboflavin (mg/d)
|
2.05
|
0.71
|
2.23
|
0.84
|
0.14
|
0.30
|
Niacin (mg/d)
|
23.59
|
7.09
|
25.25
|
9.30
|
0.19
|
0.74
|
Vitamin B6 (mg/d)
|
2.06
|
0.67
|
2.17
|
0.72
|
0.28
|
0.80
|
Folic acid (µg/d)
|
585.20
|
181.26
|
606.54
|
171.92
|
0.40
|
0.66
|
Vitamin B12 (µg/d)
|
3.99
|
2.00
|
4.47
|
2.36
|
0.15
|
0.29
|
Vitamin C (mg/d)
|
190.26
|
124.40
|
195.71
|
132.75
|
0.77
|
0.19
|
Vitamin E (mg/d)
|
15.91
|
6.73
|
17.32
|
9.28
|
0.26
|
0.37
|
Vitamin D (µg/d)
|
2.05
|
1.73
|
1.87
|
1.47
|
0.44
|
0.22
|
Iron (mg/d)
|
18.28
|
6.03
|
18.63
|
5.90
|
0.68
|
0.14
|
Selenium (µg/d)
|
114.81
|
36.86
|
119.67
|
42.80
|
0.42
|
0.95
|
Zinc (mg/d)
|
12.33
|
4.13
|
13.12
|
4.30
|
0.20
|
0.94
|
Magnesium (mg/d)
|
443.71
|
144.98
|
463.73
|
150.39
|
0.36
|
0.65
|
Calcium (mg/d)
|
1117.99
|
423.03
|
1158.55
|
410.52
|
0.50
|
0.82
|
Potassium (mg/d)
|
4208.43
|
1662.90
|
4345.83
|
1538.23
|
0.55
|
0.44
|
Caffeine (g/d)
|
147.13
|
105.55
|
157.53
|
178.52
|
0.66
|
0.72
|
|
|
|
|
|
|
|
|
MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid; SFA, Saturated fatty acid
Data are presented as mean ± standard deviation (SD).
a Calculated by analysis of variance and p-value<0.05 indicates a significant level.
*Obtained from Independent T-test
**Obtained from ANCOVA analysis
Food group adjusted by age, BMI, physical activity, and energy intake (Kcal)
Dietary intake (macronutrient and micronutrient) adjusted by energy intake (Kcal)
Correlation of main variables with sarcopenic obesity
Table 3 contains the correlation between sarcopenic obesity with the variables of interest in this study. A simple correlation revealed a significant inverse associations between FFM and FFMI with correlation coefficient (r=-0.30, p=<0.001) and (r=-0.12, p=0.01) respectively with sarcopenic obesity, while significant positive correlations were observed between BFM (r=0.27, p=<0.001) and FMI (r=0.33, p=<0.001) with sarcopenic obesity. A non-significant association was however observed between metabolic healthy obesity statuses with sarcopenic obesity.
Table 3. Spearman bivariate correlation of main variables with sarcopenic obesity
Variables
|
Spearman’s correlation coefficient (r)
|
P-value
|
Fat Free Mass
|
-0.30**
|
<0.001
|
Body Fat Mass
|
0.27**
|
<0.001
|
FFMI
|
-0.12*
|
0.01
|
FMI
|
0.33**
|
<0.001
|
Metabolic Healthy Obesity
|
0.04
|
0.45
|
Spearman Correlation Analysis
FFMI, fat-free mass index; FMI, fat mass index
**. Correlation is significant at the 0.01 level (2-tailed).
*. Correlation is significant at the 0.05 level (2-tailed).
Association between obesity statuses with measures of body composition
With the binary logistic regression analysis, beta (β), odds ratio (OR), and confidence interval (CI) for the association of sarcopenic obesity with measures of body composition in crude and adjusted models are presented in Table 4. In the crude model, participants with MUO had greater odds of increasing FFM (β= 0.76, OR=0.27, 95% CI=0.13-0.56, p=0.001) than the MHO subjects. However, after controlling for age, total energy intake, and physical activity level, the MUO groups had 0.29 folds decreased odds of FFM (β=-0.89, OR=0.29, 95% CI=0.13-0.62, p=0.008) compared to the MHO group. After additionally controlling for weight and economic status, the observed association disappeared (β=-0.55, OR=0.26, 95% CI=0.11-0.59, p=0.07). In the crude model, participants with MUO were observed to be positively associated with greater odds of increasing BFM (β=1.31, OR: 3.73, 95% CI=1.27-10.91, p=0.01) than those with MHO. Also, after controlling for age, total energy intake, and physical activity level, subjects with MUO phenotype had 4.44 greater odds for BFM, compared to those with MHO phenotype (β=1.49, OR=4.44, 95% CI=1.31-15.00, p=0.01). Even after additional control for weight and economic status, the positive association of the MUO score with higher odds for the BFM remained significant (β=0.95, OR=2.60, 95% CI=1.39-17.20, p=0.02). Subjects with MUO phenotype in the crude model were observed to have a 0.87 kg lower SMM compared with the MHO subjects (β=-0.87, OR=0.50, 95% CI=0.27-0.90, p=0.006). After age, total energy intake, and physical activity had been controlled for, the MUO participants had a 0.83 lower SMM compared with the MHO subjects (β=-0.83, OR=0.46, 95% CI=0.22-0.84, p=0.01). Furthermore, after additional adjustment for weight and economic status, the association remained significant (β=-0.73, OR=0.47, 95% CI=0.24-0.94, p=0.03). In the crude model, a non-significant association was seen between metabolic healthy statuses with sarcopenic obesity scores (β=0.35, OR=1.42, 95% CI=0.45-4.45, p=0.54). However, after controlling for age, total energy intake, physical activity level, weight, and economic status, we observed MUO subjects to have 4.21 fold greater odds for sarcopenic obesity compared to the MHO subjects (β=1.43, OR=4.21, 95% CI=1.28-62.26, p=0.02).
Table 4. Association between metabolic healthy statuses with measures of body composition and sarcopenic obesity
Variables
|
|
β
|
OR (95% CI)
|
P-value
|
Fat-Free Mass
|
|
|
|
|
Crude
|
MUO
|
0.76
|
0.27 (0.13,0.56)
|
0.001
|
|
MHO
|
Ref
|
Ref
|
|
Model 1
|
MUO
|
-0.89
|
0.29 (0.13,0.62)
|
0.008
|
|
MHO
|
Ref
|
Ref
|
|
Model 2
|
MUO
|
-0.55
|
0.26 (0.11,0.59)
|
0. 07
|
|
MHO
|
Ref
|
Ref
|
|
Body Fat Mass
|
|
|
|
|
Crude
|
MUO
|
1.31
|
3.73 (1.27, 10.91)
|
0.01
|
|
MHO
|
Ref
|
Ref
|
|
Model 1
|
MUO
|
1.49
|
4.44 (1.31, 15.00)
|
0.01
|
|
MHO
|
Ref
|
Ref
|
|
Model 2
|
MUO
|
0.95
|
2.60 (1.39, 17.20)
|
0.02
|
|
MHO
|
Ref
|
Ref
|
|
Skeletal Muscle Mass
|
|
|
|
|
Crude
|
MUO
|
-0.87
|
0.50 (0.27, 0.90)
|
0.006
|
|
MHO
|
Ref
|
Ref
|
|
Model 1
|
MUO
|
-0.83
|
0.46 (0.22, 0.84)
|
0.01
|
|
MHO
|
Ref
|
Ref
|
|
Model 2
|
MUO
|
-0.73
|
0.47 (0.24, 0.94)
|
0.03
|
|
MHO
|
Ref
|
Ref
|
|
Sarcopenic obesity
|
|
|
|
|
Crude
|
MUO
|
0.35
|
1.42 (0.45, 4.45)
|
0.54
|
|
MHO
|
Ref
|
Ref
|
|
Model 1
|
MUO
|
0.42
|
1.52 (0.40, 5.70)
|
0.53
|
|
MHO
|
Ref
|
Ref
|
|
Model 2
|
MUO
|
1.43
|
4.21 (1.28, 62.26)
|
0.02
|
|
MHO
|
Ref
|
Ref
|
|
MUO; metabolic unhealthy obese, MH; metabolic obese
P-values are reported base on the Binary logistic regression test and are considered significant at ˂0.05
Healthy obese is a reference group
Model 1: Adjusted for age, kcal, and physical activity
Model 2: Model 1 confounders with further adjustment with weight and economic status