Clinical Differences and Non-Alcoholic Fatty Liver Disease-Related Factors of Lean and Non-Lean Patients with Metabolic Syndrome
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Ethics Approval
2.2. Patient Selection
- Waist circumference for Asian population ≥90 cm in men or ≥80 cm in women [18]
- Fasting blood sugar (FBS) ≥100 mg/dL or hypoglycemia agent usage
- High-density lipoprotein cholesterol (HDL-C) <40 mg/dL in men or <50 mg/dL in women
- Triglycerides (TG) ≥150 mg/dL or lipid-lowering drug usage
2.3. Definition of Outcomes and Assessment of NAFLD and Significant and Advanced Fibrosis
- imaging or histological evidence of hepatic steatosis (defined as a lipid concentration > 5–10% of the liver weight), and
2.4. Sample Size Calculation
2.5. Data Collection
2.6. Statistical Analysis
3. Results
3.1. Demographic Data
3.2. Clinical Outcomes and Prevalence of NAFLD and Liver Fibrosis
3.3. Performances of Scoring Systems for Predicting NAFLD and Liver Fibrosis
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
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Demographic Data | Lean (n = 131) | Non-Lean (n = 612) | ||||
---|---|---|---|---|---|---|
Non-NAFLD (n = 90, 68.7%) | NAFLD (n = 41, 31.3%) | p | Non-NAFLD (n = 229, 37.4%) | NAFLD (n = 383, 62.6%) | p | |
Age (year) | 73.5 ± 11.4 | 75.0 ± 10.7 | 0.461 | 68.8 ± 9.9 | 66.8 ± 11.9 | 0.033 |
Gender: male (n, %) | 31 (34.4) | 16 (39.0) | 0.695 | 90 (39.3) | 172 (44.9) | 0.178 |
BMI (kg/m2) | 20.9 ± 1.6 | 21.6 ± 1.5 | 0.019 | 26.7 ± 2.9 | 28.2 ± 4.1 | <0.001 |
Waist circumference (cm) | 79.4 ± 9.8 | 83.0 ± 7.5 | 0.056 | 91.7 ± 8.6 | 95.6 ± 9.5 | <0.001 |
Hip circumference (cm) | 89.2 ± 4.0 | 91.0 ± 4.7 | 0.101 | 100.3 ± 7.4 | 100.7 ± 7.1 | 0.667 |
Smoker/ex-smoker (n, %) | 9 (10.0) | 4 (9.8) | 1.000 | 124 (10.5) | 27 (7.1) | 0.173 |
DM (n, %) | 32 (35.6) | 25 (61.0) | 0.008 | 80 (34.9) | 206 (53.8) | <0.001 |
HT (n, %) | 70 (77.8) | 37 (90.2) | 0.096 | 200 (87.3) | 339 (88.5) | 0.700 |
DLP (n, %) | 87 (96.7) | 41 (100.0) | 0.552 | 223 (97.4) | 369 (96.3) | 0.640 |
AST median (IQR) (mg/dL) | 21.0 (17.0, 25.0) | 22.0 (18.0, 27.0) | 0.329 | 21.0 (18.0, 26.0) | 24.0 (20.0, 31.0) | <0.001 |
ALT median (IQR) (mg/dL) | 17.0 (13.0, 20.0) | 19.5 (15.0, 30.5) | 0.014 | 19.0 (15.0, 25.0) | 26.0 (19.0, 37.0) | <0.001 |
ALP median (IQR) (mg/dL) | 70.0 (53.0, 85.0) | 70.0 (62.0, 94.0) | 0.081 | 69.0 (59.0, 84.0) | 68.0 (58.0, 84.0) | 0.782 |
GGT median (IQR) (mg/dL) | 20.0 (15.0, 30.0) | 37.0 (23.0, 60.5) | <0.001 | 25.0 (21.0, 36.0) | 34.0 (23.0, 58.5) | <0.001 |
Albumin (g/dL) | 4.4 ± 0.3 | 4.4 ± 0.4 | 0.868 | 4.4 ± 0.3 | 4.4 ± 0.3 | 0.020 |
FBS (mg/dL) | 114.1 ± 35.4 | 130.7 ± 61.4 | 0.053 | 114.6 ± 39.8 | 119.7 ± 33.0 | 0.087 |
HbA1c (%) | 6.1 ± 0.9 | 6.8 ± 1.4 | <0.001 | 6.3 ± 1.1 | 6.4 ± 0.9 | 0.052 |
Total cholesterol (mg/dL) | 180.0 ± 37.9 | 171.7 ± 32.3 | 0.229 | 173.5 ± 38.7 | 175.6 ± 36.4 | 0.489 |
TG median (IQR) (mg/dL) | 89.0 (69.0, 125.0) | 115.0 (98.0, 167.0) | 0.003 | 105.0 (78.0, 147.0) | 131.0 (97.0, 173.0) | <0.001 |
HDL-C (mg/dL) | 62.4 ± 16.6 | 54.0 ± 16.1 | 0.008 | 55.2 ± 14.0 | 51.6 ± 12.4 | 0.001 |
LDL-C (mg/dL) | 98.1 ± 33.1 | 90.2 ± 31.4 | 0.204 | 95.7 ± 32.0 | 94.6 ± 31.9 | 0.671 |
Significant fibrosis (n, %) | 0 (0.0) | 10 (24.4) | - | 0 (0.0) | 84 (21.9) | - |
Advanced fibrosis (n, %) | 0 (0.0) | 10 (24.4) | - | 0 (0.0) | 66 (17.2) | - |
FLI | 10.9 (6.6, 20.3) | 24.8 (12.8, 39.7) | <0.001 | 42.1 (25.3, 58.1) | 59.0 (40.1, 78.8) | <0.001 |
FIB-4 | 1.469 (1.053, 2.098) | 1.470 (1.018, 2.480) | 0.779 | 1.337 (1.023, 1.797) | 1.204 (0.928, 1.702) | 0.100 |
NFS | −0.842 (−1.962, 0.091) | −0.913 (−2.266, −0.054) | 0.961 | −0.720 (−1.468, −0.025) | −0.872 (−1.702, −0.059) | 0.354 |
Demographic Data | Lean (n = 131) | Non-Lean (n = 612) | ||||
---|---|---|---|---|---|---|
Non-Advanced Fibrosis (n = 121, 92.4%) | Advanced Fibrosis (n = 10, 7.6%) | p | Non-Advanced Fibrosis (n = 546, 89.2%) | Advanced Fibrosis (n = 66, 10.8%) | p | |
Age (year) | 73.2 ± 10.8 | 83.4 ± 11.6 | 0.005 | 67.3 ± 10.9 | 69.7 ± 13.7 | 0.098 |
Gender: male (n, %) | 43 (35.5) | 4 (40.0) | 0.754 | 230 (42.1) | 32 (48.5) | 0.357 |
BMI (kg/m2) | 21.1 ± 1.5 | 21.0 ± 2.1 | 0.796 | 27.5 ± 3.6 | 28.8 ± 4.2 | 0.008 |
Waist circumference (cm) | 80.3 ± 9.1 | 85.0 ± 12.4 | 0.275 | 93.7 ± 9.2 | 98.6 ± 10.0 | <0.001 |
Hip circumference (cm) | 89.9 ± 4.4 | 93.5 ± 3.5 | 0.247 | 100.6 ± 7.2 | 101.0 ± 7.3 | 0.763 |
Smoker/ex-smoker (n, %) | 12 (9.9) | 1 (10.0) | 1 | 44 (8.1) | 7 (10.6) | 0.479 |
DM (n, %) | 50 (41.3) | 7 (70.0) | 0.102 | 235 (43.0) | 51 (77.2) | <0.001 |
HT (n, %) | 97 (80.2) | 10 (100.0) | 0.207 | 478 (87.6) | 61 (92.4) | 0.316 |
DLP (n, %) | 118 (97.5) | 10 (100.0) | 1 | 527 (96.5) | 65 (98.5) | 0.712 |
AST median (IQR) (mg/dL) | 21.0 (17.0, 25.0) | 64.0 (26.0, 89.0) | <0.001 | 22.0 (18.0, 27.0) | 35.0 (28.0, 44.0) | <0.001 |
ALT median (IQR) (mg/dL) | 17.0 (13.0, 20.0) | 43.5 (21.0, 80.0) | 0.001 | 22.0 (16.0, 31.0) | 34.5 (25.0, 53.0) | <0.001 |
ALP median (IQR) (mg/dL) | 69.5 (55.0, 84.0) | 109.5 (75.0, 165.0) | 0.002 | 68.0 (58.0, 84.0) | 71.5 (62.0, 92.0) | 0.069 |
GGT median (IQR) (mg/dL) | 22.0 (17.0, 35.0) | 94.5 (43.5, 405) | <0.001 | 29.0 (21.0, 46.0) | 57.0 (35.0, 91.5) | <0.001 |
Albumin (g/dL) | 4.4 ± 0.3 | 4.1 ± 0.4 | 0.007 | 4.4 ± 0.3 | 4.4 ± 0.4 | 0.118 |
Platelet (×103/mm3) | 264.3 ± 80.3 | 197.4 ± 47.8 | 0.011 | 264.6 ± 64.8 | 221.9 ± 79.6 | <0.001 |
FBS (mg) | 118.9 ± 47.0 | 123.9 ± 25.1 | 0.742 | 116.5 ± 35.2 | 128.6 ± 38.6 | 0.010 |
HbA1c (%) | 6.3 ± 1.1 | 7.0 ± 1.5 | 0.061 | 6.3 ± 0.9 | 6.8 ± 1.3 | <0.001 |
Total cholesterol (mg/dL) | 179.1 ± 36.5 | 157.5 ± 29.6 | 0.071 | 175.6 ± 37.6 | 168.1 ± 34.3 | 0.119 |
TG median (IQR) (mg/dL) | 102.0 (73.0, 133.5) | 114.5 (101.0, 125.0) | 0.450 | 119.0 (86.0, 159.0) | 137.5 (112.0, 180.0) | 0.003 |
HDL-C (mg/dL) | 59.9 ± 16.4 | 58.7 ± 22.0 | 0.836 | 53.4 ± 13.2 | 49.2 ± 11.8 | 0.014 |
LDL-C (mg/dL) | 97.2 ± 32.2 | 75.8 ± 33.1 | 0.046 | 96.1 ± 32.0 | 85.6 ± 29.5 | 0.012 |
FIB-4 | 1.420 (1.038, 2.040) | 3.219 (2.789, 4.023) | <0.001 | 1.218 (0.945, 1.640) | 1.812 (1.341, 3.038) | <0.001 |
NFS | −1.043 (−2.094, −0.086) | 0.571 (−0.735, 0.726) | 0.004 | −0.879 (−1.696, −0.104) | −0.247 (−1.224, 1.131) | <0.001 |
NAFLD (n = 424) | Lean with NAFLD (n = 41, 9.7%) | Non-Lean with NAFLD (n = 383, 90.3%) | p |
---|---|---|---|
Age (year) | 75.0 ± 10.7 | 66.8 ± 11.9 | <0.001 |
Gender: male (n, %) | 16 (39.0) | 172 (44.9) | 0.512 |
BMI (kg/m2) | 21.6 ± 1.5 | 28.2 ± 4.1 | <0.001 |
Waist circumference (cm) | 83.0 ± 7.5 | 95.6 ± 9.5 | <0.001 |
Hip circumference (cm) | 91.0 ± 4.7 | 100.7 ± 7.1 | <0.001 |
Smoker/ex-smoker (n, %) | 4 (9.8) | 27 (7.1) | 0.525 |
DM (n, %) | 25 (61.0) | 206 (53.8) | 0.413 |
HT (n, %) | 37 (90.2) | 339 (88.5) | 1.000 |
DLP (n, %) | 41 (100.0) | 369 (96.3) | 0.379 |
AST median (IQR) (mg/dL) | 22.0 (18.0, 27.0) | 24.0 (20.0, 31.0) | 0.164 |
ALT median (IQR) (mg/dL) | 19.5 (15.0, 30.5) | 26.0 (19.0, 37.0) | 0.009 |
ALP median (IQR) (mg/dL) | 70.0 (62.0, 94.0) | 68.0 (58.0, 84.0) | 0.105 |
GGT median (IQR) (mg/dL) | 37.0 (23.0, 60.5) | 34.0 (23.0, 58.5) | 0.673 |
Albumin (g/dL) | 4.4 ± 0.4 | 4.4 ± 0.3 | 0.300 |
FBS | 130.7 ± 61.4 | 119.7 ± 33.0 | 0.069 |
HbA1c (%) | 6.8 ± 1.4 | 6.4 ± 0.9 | 0.013 |
Total cholesterol (mg/dL) | 171.7 ± 32.3 | 175.6 ± 36.4 | 0.511 |
TG median (IQR) (mg/dL) | 115.0 (98.0, 167.0) | 131.0 (97.0, 173.0) | 0.340 |
HDL-C (mg/dL) | 54.0 ± 16.1 | 51.6 ± 12.4 | 0.256 |
LDL-C (mg/dL) | 90.2 ± 31.4 | 94.6 ± 31.9 | 0.406 |
Significant fibrosis (n, %) | 10 (24.4) | 84 (21.9) | 0.695 |
Advanced fibrosis (n, %) | 10 (24.4) | 66 (17.2) | 0.283 |
Fatty Liver Index (FLI) | n | AUROC | Sensitivity (%) | Specificity (%) | PPV (%) | NPV (%) | LR+ | LR− |
---|---|---|---|---|---|---|---|---|
FLI ≥ 30 | ||||||||
All | 589 | 0.67 (0.63, 0.71) | 84.0 (79.7, 87.7) | 49.8 (43.3, 56.3) | 71.0 (66.4, 75.3) | 68.0 (60.5, 74.8) | 1.67 (1.46, 1.91) | 0.32 (0.24, 0.42) |
Lean | 101 | 0.67 (0.57, 0.77) | 46.9 (29.1, 65.3) | 87.0 (76.7, 93.9) | 62.5 (40.6, 81.2) | 77.9 (67.0, 86.6) | 3.59 (1.76, 7.33) | 0.61 (0.44, 0.86) |
Non-lean | 488 | 0.61 (0.57, 0.65) | 87.7 (83.6, 91.1) | 34.7 (27.6, 42.4) | 71.5 (66.8, 76.0) | 60.2 (49.8, 70.0) | 1.34 (1.20, 1.51) | 0.35 (0.25, 0.51) |
FLI > 60 | ||||||||
All | 589 | 0.65 (0.62, 0.69) | 45.4 (40.1, 50.8) | 85.4 (80.2, 89.6) | 82.0 (75.8, 87.1) | 51.6 (46.6, 56.7) | 3.10 (2.24, 4.30) | 0.64 (0.57, 0.71) |
Lean | 101 | 0.55 (0.50, 0.60) | 9.4 (2.0, 25.0) | 100 (94.8, 100.0) | 100 (29.2, 100.0) | 70.4 (60.3, 79.2) | NA | 0.91 (0.81, 1.01) |
Non-lean | 488 | 0.64 (0.60, 0.68) | 49.1 (43.4, 54.7) | 79.4 (72.5, 85.2) | 81.7 (75.4, 86.9) | 45.5 (39.7, 51.3) | 2.38 (1.74, 3.27) | 0.64 (0.56, 073) |
Scores | n | AUROC | Sensitivity (%) | Specificity (%) | PPV (%) | NPV (%) | LR+ | LR− |
---|---|---|---|---|---|---|---|---|
Fibrosis-4 (FIB-4) | ||||||||
FIB-4 ≥ 1.3 | ||||||||
All | 726 | 0.67 (0.62, 0.72) | 78.9 (68.1, 87.5) | 54.8 (50.9, 58.6) | 16.9 (13.2, 21.3) | 95.7 (93.1, 97.5) | 1.75 (1.51, 2.02) | 0.38 (0.25, 0.60) |
Lean | 127 | 0.71 (0.66, 0.75) | 100.0 (69.2, 100.0) | 41.9 (32.8, 51.4) | 12.8 (6.3, 22.3) | 100.0 (92.7, 100.0) | 1.72 (1.48, 2.01) | NA |
Non-lean | 599 | 0.67 (0.61, 0.72) | 75.8 (63.6, 85.5) | 57.6 (53.3, 61.8) | 18.1 (13.8, 23.2) | 95.0 (92.1, 97.1) | 1.79 (1.51, 2.11) | 0.42 (0.27, 0.65) |
FIB-4 ≥ 3.25 | ||||||||
All | 726 | 0.60 (0.56, 0.65) | 22.4 (13.6, 33.4) | 98.2 (96.8, 99.0) | 58.6 (38.9, 76.5) | 91.5 (89.2, 93.5) | 12.12 (6.02, 24.39) | 0.79 (0.70, 0.89) |
Lean | 127 | 0.73 (0.56, 0.89) | 50.0 (18.7, 81.3) | 95.7 (90.3, 98.6) | 50.0 (18.7, 81.3) | 95.7 (90.3, 98.6) | 11.70 (4.06, 33.71) | 0.52 (0.28, 0.97) |
Non-lean | 599 | 0.58 (0.54, 0.63) | 18.2 (9.8, 29.6) | 98.7 (97.3, 99.5) | 63.2 (38.4, 83.7) | 90.7 (88.0, 92.9) | 13.84 (5.65, 33.93) | 0.83 (0.74, 0.93) |
NAFLD fibrosis score (NFS) | ||||||||
NFS ≥ −1.455 | ||||||||
All | 655 | 0.59 (0.54, 0.63) | 84.2 (74.0, 91.6) | 32.8 (29.0, 36.8) | 14.1 (11.1, 17.7) | 94.1 (89.9, 96.9) | 1.25 (1.12, 1.40) | 0.48 (0.28, 0.82) |
Lean | 113 | 0.65 (0.54, 0.76) | 90.0 (55.5, 99.7) | 40.8 (31.2, 50.9) | 12.9 (6.1, 23.0) | 97.7 (87.7, 99.9) | 1.52 (1.17, 1.97) | 0.25 (0.04, 1.60) |
Non-lean | 542 | 0.57 (0.52, 0.62) | 83.3 (72.1, 91.4) | 31.1 (27.0, 35.5) | 14.4 (11.0, 18.3) | 93.1 (88.0, 96.5) | 1.21 (1.07, 1.37) | 0.54 (0.31, 0.93) |
NFS ≥ 0.676 | ||||||||
All | 655 | 0.63 (0.58, 0.69) | 34.2 (23.7, 46.0) | 92.4 (89.9, 94.4) | 37.1 (25.9, 49.5) | 91.5 (88.9, 93.6) | 4.50 (2.95, 6.86) | 0.71 (0.60, 0.84) |
Lean | 113 | 0.67 (0.51, 0.83) | 40.0 (12.2, 73.8) | 94.2 (87.8, 97.8) | 40.0 (12.2, 73.8) | 94.2 (87.8, 97.8) | 6.87 (2.32, 20.34) | 0.64 (0.38, 1.06) |
Non-lean | 542 | 0.63 (0.57, 0.69) | 33.3 (22.2, 46.0) | 92.0 (89.2, 94.3) | 36.7 (24.6, 50.1) | 90.9 (87.9, 93.3) | 4.18 (2.64, 6.60) | 0.72 (0.61, 0.86) |
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Boonchai, P.; Kositamongkol, C.; Jitrukthai, S.; Phothirat, S.; Mepramoon, E.; Nimitpunya, P.; Srivanichakorn, W.; Chaisathaphol, T.; Washirasaksiri, C.; Auesomwang, C.; et al. Clinical Differences and Non-Alcoholic Fatty Liver Disease-Related Factors of Lean and Non-Lean Patients with Metabolic Syndrome. J. Clin. Med. 2022, 11, 2445. https://doi.org/10.3390/jcm11092445
Boonchai P, Kositamongkol C, Jitrukthai S, Phothirat S, Mepramoon E, Nimitpunya P, Srivanichakorn W, Chaisathaphol T, Washirasaksiri C, Auesomwang C, et al. Clinical Differences and Non-Alcoholic Fatty Liver Disease-Related Factors of Lean and Non-Lean Patients with Metabolic Syndrome. Journal of Clinical Medicine. 2022; 11(9):2445. https://doi.org/10.3390/jcm11092445
Chicago/Turabian StyleBoonchai, Punyisa, Chayanis Kositamongkol, Suchanart Jitrukthai, Sukumal Phothirat, Euarat Mepramoon, Pongpol Nimitpunya, Weerachai Srivanichakorn, Thanet Chaisathaphol, Chaiwat Washirasaksiri, Chonticha Auesomwang, and et al. 2022. "Clinical Differences and Non-Alcoholic Fatty Liver Disease-Related Factors of Lean and Non-Lean Patients with Metabolic Syndrome" Journal of Clinical Medicine 11, no. 9: 2445. https://doi.org/10.3390/jcm11092445