The Additive Values of the Classification of Higher Serum Uric Acid Levels as a Diagnostic Criteria for Metabolic-Associated Fatty Liver Disease
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Population and Design
2.2. Clinical and Laboratory Parameters
2.3. Radiology Assessments
2.4. Statistical Analysis
3. Results
3.1. Baseline Characteristics of the Enrolled Subjects with NAFLD and MAFLD, or Those with MRI-PDFF
3.2. The Characteristics of NAFLD and MAFLD Patients Varied by the Quartiles of SUA Levels
3.3. Associations between SUA Levels and Steatosis Severity in NAFLD and MAFLD Patients
3.4. The Predictive Value of SUA Level to Steatosis Severity
3.5. The Different Levels of SUA between NAFLD and MAFLD Patients
3.6. Classifying Super Hyperuricemia into MAFLD versus Nonhyperuricemia-Involving Groups in Lean/Normal-Weight NAFLD–non-MAFLD with at Least One Criterion of Metabolic Dysfunction
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Characteristics | Non-NAFLD (n = 7216) | NAFLD (n = 3537) | Non-MAFLD (n = 203) | MAFLD Defined by MRI-PDFF (n = 1017) |
---|---|---|---|---|
Age, years | 45.2 ± 15.8 | 45.0 ± 16.4 | 45.7 ± 14.6 | 46.0 ± 15.3 |
Male, n(%) | 4339(60.1) | 2345(66.3) * | 140(69.0) | 767(75.4) ** |
BMI, kg/m2 | 22.7 ± 3.1 | 26.9 ± 3.8 * | 23.9 ± 2.9 | 27.0 ± 3.4 ** |
SBP, mmHg | 127 ± 23 | 131 ± 16 * | 127 ± 17 | 131 ± 16 ** |
DBP, mmHg | 76 ± 14 | 83 ± 11 * | 78 ± 11 | 84 ± 12 ** |
Hypertension, n(%) | 1230(17.0) | 1145(32.4) * | 37(18.2) | 352(34.6) ** |
T2DM, n(%) | 1190(16.5) | 994(28.1) * | 34(16.7) | 296(29.1) ** |
ALT, U/L | 22 ± 12 | 37 ± 20 * | 24 ± 14 | 38 ± 22 ** |
AST, U/L | 27 ± 22 | 29 ± 22 * | 26 ± 23 | 30 ± 24 ** |
GGT, U/L | 30 ± 38 | 60 ± 89 * | 47 ± 57 | 63 ± 73 ** |
ALP, U/L | 71 ± 19 | 79 ± 39 * | 74 ± 19 | 81 ± 41 ** |
Total cholesterol, mmol/L | 4.8 ± 1.2 | 5.2 ± 1.2 * | 5.0 ± 1.1 | 5.2 ± 1.1 ** |
Triglyceride, mmol/L | 1.3 ± 0.9 | 2.0 ± 1.5 * | 1.3 ± 0.6 | 1.9 ± 1.3 ** |
HDL-C, mmol/L | 1.3 ± 0.5 | 1.2 ± 0.3 * | 1.2 ± 0.3 | 1.1 ± 0.3 ** |
LDL-C, mmol/L | 3.0 ± 1.3 | 3.2 ± 0.9 * | 3.1 ± 0.8 | 3.3 ± 0.8 ** |
FBG, mmol/L | 4.7 ± 1.0 | 5.1 ± 1.3 * | 4.8 ± 1.1 | 5.2 ± 1.2 ** |
HbA1c, % | 5.7 ± 0.9 | 6.2 ± 1.4 * | 5.9 ± 1.1 | 6.2 ± 1.5 ** |
Uric acid, μmol/L | 363 ± 135 | 403 ± 100 * | 362 ± 91 | 405 ± 98 ** |
HUA, n(%) | 2255(31.4) | 1663(47.3) * | 76(37.4) | 557(54.8) ** |
FIB-4 | 0.8 ± 0.6 | 0.9 ± 0.8 * | 0.8 ± 0.7 | 1.0 ± 0.8 ** |
FIB-4 > 1.30, n(%) | 978(13.6) | 612(17.3) * | 29(14.3) | 194(19.1) ** |
Moderate-to-severe steatosis, n(%) | - | 1222(34.5) | - | 319(31.4) |
Severe steatosis, n(%) | - | 298(8.4) | - | 174(17.1) |
Characteristics | Lean/Normal-Weight MAFLD | Lean/Normal-Weight MAFLD | Lean/Normal-Weight NAFLD–non-MAFLD | p | |||||
---|---|---|---|---|---|---|---|---|---|
SHUA(-) | SHUA(+) | SHUA(-) | SHUA(+) | LM(-) vs. LM(+) | LNM(-) vs. LNM(+) | LM vs. LNM(+) | LM(+) vs. LNM(+) | ||
n = 75 | n = 64(85.3%) | n = 11(14.7%) | n = 44(80.0%) | n = 11(20.0%) | |||||
Age, years | 45.4 ± 12.7 | 46.5 ± 12.9 | 39.4 ± 9.8 | 40.0 ± 12.2 | 38.4 ± 12.6 | 0.08 | 0.70 | 0.08 | 0.98 |
Male, n(%) | 42(56.0) | 35(54.7) | 7(63.6) | 29(65.9) | 8(72.7) | 0.82 | 0.94 | 0.88 | 0.15 |
BMI, kg/m2 | 21.8 ± 1.1 | 21.8 ± 1.0 | 21.6 ± 1.3 | 21.2 ± 1.5 | 22.0 ± 1.1 | 0.37 | 0.06 | 0.54 | 0.29 |
Waist circumference, cm | 79.3 ± 4.9 | 79.4 ± 5.2 | 78.8 ± 3.5 | 76.2 ± 5.4 | 79.5 ± 4.3 | 0.71 | 0.06 | 0.94 | 0.77 |
Abdominal obesity, n(%) | 13(17.3) | 10(15.6) | 3(27.3) | - | - | 0.61 | - | 0.71 | 0.21 |
WHR | 0.9 ± 0.05 | 0.9 ± 0.05 | 0.9 ± 0.03 | 0.8 ± 0.05 | 0.9 ± 0.04 | 0.75 | 0.13 | 0.84 | 0.96 |
SBP, mmHg | 130 ± 18 | 130 ± 17 | 131 ± 21 | 120 ± 15 | 119 ± 14 | 0.94 | 0.89 | 0.05 | 0.12 |
DBP, mmHg | 86 ± 11 | 86 ± 11 | 85 ± 12 | 79 ± 11 | 75 ± 11 | 0.54 | 0.31 | <0.01 | 0.06 |
Hypertension, n(%) | 30(40.0) | 26(42.2) | 4(36.4) | 8(18.2) | 2(18.2) | 0.37 | 0.98 | 0.29 | 0.63 |
ALT, U/L | 36 ± 29 | 38 ± 31 | 35 ± 20 | 32 ± 22 | 33 ± 22 | 0.30 | 0.90 | 0.77 | 0.65 |
AST, U/L | 38 ± 36 | 39 ± 29 | 32 ± 11 | 34 ± 24 | 35 ± 15 | 0.52 | 0.84 | 0.75 | 0.86 |
GGT, U/L | 65 ± 81 | 62 ± 79 | 77 ± 95 | 49 ± 77 | 35 ± 14 | 0.56 | 0.58 | 0.24 | 0.20 |
ALP, U/L | 79 ± 22 | 78 ± 23 | 85 ± 18 | 74 ± 19 | 79 ± 19 | 0.27 | 0.44 | 0.92 | 0.51 |
Total cholesterol, mmol/L | 5.1 ± 1.2 | 5.1 ± 1.2 | 4.7 ± 0.7 | 5.0 ± 1.1 | 4.8 ± 1.2 | 0.19 | 0.67 | 0.47 | 0.76 |
Triglyceride, mmol/L | 1.9 ± 1.0 | 1.9 ± 1.0 | 2.1 ± 1.2 | 1.3 ± 0.5 | 1.2 ± 0.4 | 0.59 | 0.86 | 0.02 | 0.03 |
HDL-C, mmol/L | 1.2 ± 0.4 | 1.2 ± 0.4 | 1.0 ± 0.2 | 1.3 ± 0.4 | 1.3 ± 0.3 | 0.18 | 0.62 | 0.41 | 0.53 |
LDL-C, mmol/L | 3.1 ± 0.9 | 3.2 ± 0.9 | 2.8 ± 0.7 | 3.1 ± 0.8 | 3.1 ± 0.9 | 0.17 | 0.97 | 0.79 | 0.48 |
FFA, µmol/L | 576 ± 152 | 579 ± 157 | 559 ± 129 | 545 ± 233 | 569 ± 171 | 0.99 | 0.68 | 0.90 | 0.93 |
FBG, mmol/L | 4.9 ± 0.6 | 5.0 ± 0.5 | 4.8 ± 0.6 | 4.6 ± 0.5 | 4.6 ± 1.1 | 0.42 | 0.89 | 0.05 | 0.33 |
HbA1c, % | 5.9 ± 1.7 | 6.0 ± 1.9 | 5.9 ± 2.4 | 5.9 ± 1.3 | 5.9 ± 1.9 | 0.57 | 0.77 | 0.79 | 0.86 |
FINS, μU/mL | 10.1 ± 4.4 | 10.2 ± 4.6 | 9.9 ± 3.2 | 7.0 ± 3.2 | 6.7 ± 2.7 | 0.87 | 0.86 | 0.01 | 0.08 |
HOMA-IR | 2.2 ± 1.0 | 2.3 ± 1.0 | 2.1 ± 0.7 | 1.5 ± 0.9 | 1.4 ± 0.7 | 0.60 | 0.81 | <0.01 | 0.08 |
HOMA-IR ≥ 2.5, n(%) | 28(37.3) | 25(39.1) | 3(27.3) | 3(6.8) | 0(0.00) | 0.68 | 0.98 | 0.01 | 0.21 |
Hs-CRP, mg/L | 3.4 ± 2.1 | 3.3 ± 2.5 | 3.4 ± 2.2 | 1.1 ± 0.9 | 1.5 ± 1.7 | 0.69 | 0.23 | 0.91 | 0.14 |
Uric acid, μmol/L | 370 ± 81 | 345 ± 56 | 510 ± 64 | 356 ± 63 | 524 ± 50 | <0.01 | <0.01 | <0.01 | 0.61 |
FIB-4 | 1.1 ± 0.7 | 1.1 ± 0.8 | 1.0 ± 0.6 | 1.1 ± 0.7 | 1.0 ± 0.6 | 0.43 | 0.39 | 0.72 | 0.47 |
FIB-4 > 1.30, n(%) | 22(29.3) | 17(26.6) | 5(45.5) | 7(15.9) | 1(9.1) | 0.20 | 0.92 | 0.29 | 0.15 |
SWE, kpa | 5.9 ± 3.3 | 5.9 ± 3.2 | 6.0 ± 3.5 | 6.0 ± 3.5 | 6.0 ± 3.5 | 0.71 | 0.89 | 0.64 | 0.92 |
SWE ≥ 6.1 kpa, n(%) | 30(40.0) | 23(35.9) | 7(63.6) | 19(43.2) | 6(54.5) | 0.16 | 0.50 | 0.36 | 0.67 |
Liver fat content, % | 12.4 ± 7.2 | 12.0 ± 6.9 | 15.4 ± 8.3 | 9.7 ± 5.7 | 16.0 ± 7.1 | 0.13 | <0.01 | 0.12 | 0.84 |
Moderate-to-severe steatosis, n(%) | 17(22.7) | 13(20.3) | 4(36.4) | 7(15.9) | 4(36.4) | 0.43 | 0.27 | 0.54 | 0.98 |
Severe steatosis, n(%) | 7(9.3) | 6(9.4) | 1(9.1) | 3(6.8) | 3(27.3) | 0.98 | 0.16 | 0.22 | 0.58 |
Characteristics | Lean/Normal-Weight MAFLD | Lean/Normal-Weight MAFLD | Lean/Normal-Weight NAFLD–non-MAFLD | p | |||||
---|---|---|---|---|---|---|---|---|---|
SHUA(-) | SHUA(+) | SHUA(-) | SHUA(+) | LM(-) vs. LM(+) | LNM (-) vs. LNM(+) | LM vs. LNM(+) | LM(+) vs. LNM(+) | ||
n = 185 | n = 160(86.5%) | n = 25(13.5%) | n = 267(83.2%) | n = 54(16.8%) | |||||
Age, years | 43.7 ± 12.3 | 44.1 ± 12.3 | 41.3 ± 12.4 | 40.9 ± 12.8 | 37.6 ± 11.4 | 0.30 | 0.08 | <0.01 | 0.22 |
Male, n(%) | 114(61.6) | 96(60.0) | 18(72.0) | 158(59.2) | 43(79.6) | 0.25 | <0.01 | 0.01 | 0.45 |
BMI, kg/m2 | 21.5 ± 1.6 | 21.5 ± 1.5 | 21.3 ± 1.9 | 21.2 ± 1.5 | 20.7 ± 2.4 | 0.42 | 0.03 | <0.01 | 0.12 |
SBP, mmHg | 133 ± 15 | 133 ± 15 | 133 ± 18 | 121 ± 15 | 124 ± 14 | 0.89 | 0.14 | <0.01 | 0.02 |
DBP, mmHg | 86 ± 9 | 87 ± 9 | 83 ± 6 | 78 ± 11 | 78 ± 12 | 0.15 | 0.65 | <0.01 | 0.04 |
Hypertension, n(%) | 113(61.1) | 99(61.9) | 14(56) | 71(26.6) | 15(27.8) | 0.86 | 0.86 | <0.01 | <0.01 |
ALT, U/L | 38 ± 33 | 38 ± 33 | 39 ± 36 | 36 ± 28 | 34 ± 19 | 0.91 | 0.76 | 0.42 | 0.54 |
AST, U/L | 28 ± 15 | 28 ± 16 | 27 ± 8 | 32 ± 31 | 29 ± 15 | 0.85 | 0.40 | 0.88 | 0.81 |
GGT, U/L | 64 ± 89 | 64 ± 91 | 65 ± 89 | 57 ± 96 | 64 ± 87 | 0.97 | 0.62 | 0.97 | 0.96 |
ALP, U/L | 80 ± 28 | 79 ± 29 | 89 ± 21 | 78 ± 28 | 88 ± 77 | 0.18 | 0.08 | 0.13 | 0.90 |
Total cholesterol, mmol/L | 5.2 ± 1.1 | 5.2 ± 1.2 | 4.9 ± 0.7 | 5.1 ± 1.2 | 5.1 ± 1.0 | 0.20 | 0.95 | 0.50 | 0.57 |
Triglyceride, mmol/L | 2.5 ± 1.5 | 2.5 ± 1.6 | 2.3 ± 1.2 | 1.4 ± 1.2 | 1.5 ± 0.8 | 0.61 | 0.84 | <0.01 | <0.01 |
HDL-C, mmol/L | 1.1 ± 0.3 | 1.1 ± 0.3 | 1.0 ± 0.3 | 1.3 ± 0.4 | 1.2 ± 0.3 | 0.21 | 0.08 | 0.21 | 0.08 |
LDL-C, mmol/L | 3.2 ± 0.9 | 3.2 ± 0.9 | 3.0 ± 0.6 | 3.2 ± 0.9 | 3.3 ± 0.8 | 0.24 | 0.35 | 0.30 | 0.12 |
FFA, µmol/L | 561 ± 162 | 564 ± 167 | 544 ± 139 | 558 ± 154 | 547 ± 151 | 0.87 | 0.64 | 0.92 | 0.89 |
FBG, mmol/L | 4.8 ± 0.6 | 4.8 ± 0.6 | 4.6 ± 0.5 | 4.8 ± 0.6 | 4.8 ± 0.8 | 0.24 | 0.91 | 0.96 | 0.33 |
HbA1c, % | 5.8 ± 1.6 | 5.9 ± 1.4 | 5.7 ± 1.9 | 5.8 ± 1.4 | 5.8 ± 1.7 | 0.24 | 0.79 | 0.86 | 0.61 |
Uric acid, μmol/L | 378 ± 81 | 357 ± 60 | 512 ± 66 | 354 ± 64 | 525 ± 66 | <0.01 | <0.01 | <0.01 | 0.42 |
FIB-4 | 0.9 ± 0.6 | 1.0 ± 0.6 | 0.9 ± 0.4 | 1.0 ± 1.0 | 0.9 ± 0.6 | 0.68 | 0.24 | 0.45 | 0.88 |
FIB-4 > 1.30, n(%) | 32(17.3) | 28(17.5) | 4(16.0) | 37(13.9) | 8(14.8) | 0.85 | 0.85 | 0.67 | 0.89 |
Moderate-to-severe steatosis, n(%) | 42(22.7) | 33(20.6) | 9(36) | 63(23.4) | 20(37.0) | 0.09 | 0.04 | 0.03 | 0.93 |
Severe steatosis, n(%) | 7(3.8) | 7(4.4) | 0(0) | 9(3.4) | 4(7.4) | 0.62 | 0.16 | 0.44 | 0.30 |
Characteristics | NAFLD–non-MAFLD + One Metabolic Dysregulation (Ultrasonography) | p | NAFLD–non-MAFLD + One Metabolic Dysregulation (MRI-PDFF) | p | ||
---|---|---|---|---|---|---|
SHUA(-) | SHUA(+) | SHUA(-) | SHUA(+) | |||
n = 188(82.8%) | n = 39(17.2%) | n = 30(78.9%) | n = 8(21.1%) | |||
Age, years | 41.6 ± 13.1 | 39.7 ± 11.2 | 0.39 | 39.4 ± 12.1 | 40.3 ± 8.6 | 0.85 |
Male, n(%) | 104(55.3) | 32(82.1) | <0.01 | 21(75.0) | 8(100) | 0.16 |
BMI, kg/m2 | 21.2 ± 1.4 | 20.6 ± 2.2 | 0.03 | 21.5 ± 1.2 | 22.1 ± 1.2 | 0.23 |
Waist circumference, cm | - | - | - | 76.7 ± 4.9 | 80.6 ± 5.2 | 0.06 |
Abdominal obesity, n(%) | - | - | - | 0(0) | 0(0) | - |
WHR | - | - | - | 0.8 ± 0.04 | 0.9 ± 0.04 | 0.06 |
SBP, mmHg | 123 ± 17 | 126 ± 14 | 0.25 | 122 ± 18 | 122 ± 15 | 0.99 |
DBP, mmHg | 81 ± 11 | 81 ± 11 | 0.26 | 80 ± 12 | 78 ± 9 | 0.62 |
Hypertension, n(%) | 71(37.8) | 15 (38.5) | 0.94 | 5(17.9) | 3(37.5) | 0.99 |
ALT, U/L | 33 ± 31 | 35 ± 20 | 0.37 | 32 ± 22 | 33 ± 23 | 0.68 |
AST, U/L | 36 ± 26 | 29 ± 14 | 0.23 | 35 ± 26 | 35 ± 14 | 0.79 |
GGT, U/L | 50 ± 95 | 73 ± 99 | 0.68 | 50 ± 80 | 40 ± 10 | 0.72 |
ALP, U/L | 77 ± 31 | 91 ± 48 | 0.09 | 79 ± 17 | 79 ± 18 | 0.49 |
Total cholesterol, mmol/L | 5.2 ± 1.2 | 5.1 ± 1.0 | 0.46 | 5.0 ± 1.3 | 4.9 ± 1.2 | 0.21 |
Triglyceride, mmol/L | 1.6 ± 1.2 | 1.7 ± 0.8 | 0.72 | 1.3 ± 0.6 | 1.5 ± 0.4 | 0.50 |
HDL-C, mmol/L | 1.3 ± 0.4 | 1.2 ± 0.2 | 0.04 | 1.3 ± 0.5 | 1.3 ± 0.3 | 0.98 |
LDL-C, mmol/L | 3.3 ± 0.9 | 3.3 ± 0.7 | 0.87 | 3.1 ± 0.8 | 3.7 ± 0.3 | 0.07 |
FFA, µmol/L | 546 ± 197 | 536 ± 176 | 0.41 | 556 ± 255 | 539 ± 184 | 0.66 |
FBG, mmol/L | 4.8 ± 0.7 | 4.9 ± 0.9 | 0.67 | 4.6 ± 0.6 | 4.7 ± 1.3 | 0.55 |
HbA1c, % | 5.7 ± 1.6 | 5.8 ± 1.9 | 0.29 | 5.9 ± 1.7 | 5.9 ± 1.8 | 0.18 |
FINS, μU/mL | - | - | - | 6.7 ± 10.3 | 6.9 ± 3.4 | 0.63 |
HOMA-IR | - | - | - | 1.5 ± 0.9 | 1.4 ± 1.0 | 0.55 |
HOMA-IR ≥ 2.5, n(%) | - | - | - | 7(25.0) | 1(12.5) | 0.52 |
Hs-CRP, mg/L | - | - | - | 1.3 ± 1.2 | 1.6 ± 1.5 | 0.46 |
Uric acid, μmol/L | 354 ± 63 | 529 ± 72 | <0.01 | 355 ± 56 | 523 ± 44 | <0.01 |
FIB-4 | 1.1 ± 1.2 | 0.9 ± 0.6 | 0.27 | 1.1 ± 0.6 | 1.0 ± 0.6 | 0.73 |
FIB-4 ≥ 1.3, n(%) | 29(15.4) | 6(15.4) | 0.99 | 6(20.0) | 1(12.5) | 0.39 |
SWE, kpa | - | - | - | 5.4 ± 1.3 | 5.3 ± 1.6 | 0.60 |
SWE ≥ 6.1 kpa, n(%) | - | - | - | 5(17.9) | 4(50.0) | 0.07 |
Liver fat content, % | - | - | - | 10.2 ± 5.7 | 18.1 ± 7.8 | <0.01 |
Moderate-to-severe steatosis, n(%) | 47(25.0) | 14(35.9) | 0.16 | 10(35.7) | 7(87.5) | 0.02 |
Severe steatosis, n(%) | 7(3.7) | 2(5.1) | 0.99 | 1(3.6) | 2(25.0) | 0.11 |
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He, J.; Ye, J.; Sun, Y.; Feng, S.; Chen, Y.; Zhong, B. The Additive Values of the Classification of Higher Serum Uric Acid Levels as a Diagnostic Criteria for Metabolic-Associated Fatty Liver Disease. Nutrients 2022, 14, 3587. https://doi.org/10.3390/nu14173587
He J, Ye J, Sun Y, Feng S, Chen Y, Zhong B. The Additive Values of the Classification of Higher Serum Uric Acid Levels as a Diagnostic Criteria for Metabolic-Associated Fatty Liver Disease. Nutrients. 2022; 14(17):3587. https://doi.org/10.3390/nu14173587
Chicago/Turabian StyleHe, Jie, Junzhao Ye, Yanhong Sun, Shiting Feng, Youpeng Chen, and Bihui Zhong. 2022. "The Additive Values of the Classification of Higher Serum Uric Acid Levels as a Diagnostic Criteria for Metabolic-Associated Fatty Liver Disease" Nutrients 14, no. 17: 3587. https://doi.org/10.3390/nu14173587