1Division of Endocrinology and Metabolism, Department of Internal Medicine, Keimyung University School of Medicine, Daegu, Korea
2Division of Gastroenterology and Hepatology, Department of Internal Medicine, Keimyung University School of Medicine, Daegu, Korea
Copyright © 2021 Korean Diabetes Association
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.
AUTHOR CONTRIBUTIONS
Conception or design: E.H., H.S.K.
Acquisition, analysis, or interpretation of data: E.H., M.K.K., B.K.J., H.S.K.
Drafting the work or revising: E.H., M.K.K., H.S.K.
Final approval of the manuscript: H.S.K.
FUNDING
This study was supported by a grant (Eugene Han, 2017F-5) from the Korean Diabetes Association. The funders had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript.
Values are presented as mean±standard deviation, number (%), or median (interquartile range).
T2DM, type 2 diabetes mellitus; SBP, systolic blood pressure; DBP, diastolic blood pressure; FPG, fasting plasma glucose; HbA1c, glycosylated hemoglobin; PPPG, postprandial plasma glucose; BUN, blood urea nitrogen; eGFR, estimated glomerular filtration rate; HDL-C, high density lipoprotein cholesterol; LDL-C, low density lipoprotein cholesterol; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; HOMA-IR, homeostatic model assessment of insulin resistance; CAP, controlled attenuation parameter; ACR, albumin-to-creatinine ratio; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker.
Parameter | r | P value |
---|---|---|
Age, yr | –0.321 | 0.001 |
BMI, kg/m2 | 0.449 | <0.001 |
Waist circumference, cm | 0.339 | 0.001 |
Duration of T2DM, yr | –0.266 | 0.007 |
Presence of diabetic retinopathy | –0.081 | 0.421 |
ACE inhibitor/ARB use | 0.018 | 0.858 |
FPG, mg/dL | –0.101 | 0.316 |
HbA1c, % | –0.065 | 0.521 |
PPPG, mg/dL | –0.035 | 0.730 |
AST, IU/La | 0.192 | 0.056 |
ALT, IU/La | 0.319 | 0.001 |
γ-GT, IU/La | 0.281 | 0.005 |
Triglyceride, mg/dLa | 0.281 | 0.005 |
LDL-C, mg/dLa | 0.101 | 0.322 |
HOMA-IRa | 0.113 | 0.301 |
eGFR, mL/min/1.73 m2 | 0.166 | 0.099 |
Urinary ACR, mg/g creatininea | 0.331 | 0.001 |
CAP, controlled attenuation parameter; BMI, body mass index; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; FPG, fasting plasma glucose; HbA1c, glycosylated hemoglobin; PPPG, postprandial plasma glucose; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; LDL-C, low density lipoprotein cholesterol; HOMA-IR, homeostatic model assessment of insulin resistance; eGFR, estimated glomerular filtration rate; ACR, albumin-to-creatinine ratio.
a Log transformed.
Variable |
Model 1 |
Model 2 |
Model 3 |
Model 4 |
||||
---|---|---|---|---|---|---|---|---|
STD β | P value | STD β | P value | STD β | P value | STD β | P value | |
Duration of T2DM, yr | –0.160 | 0.135 | - | - | - | - | - | - |
Diabetic retinopathy | –0.414 | 0.680 | - | - | - | - | - | - |
ACE inhibitor/ARB use | 0.382 | 0.704 | - | - | - | - | - | - |
HbA1c, % | –0.177 | 0.083 | –0.157 | 0.131 | - | - | - | - |
ALT, IU/La | 0.153 | 0.119 | 0.195 | 0.081 | - | - | - | - |
γ-GT, IU/La | 0.096 | 0.344 | 0.060 | 0.574 | - | - | - | - |
Triglyceride, mg/dLa | 0.198 | 0.062 | 0.213 | 0.047 | - | - | - | - |
BMI, kg/m2 | 0.391 | 0.001 | 0.380 | <0.001 | 0.364 | <0.001 | - | - |
Waist circumference, cm | 0.287 | 0.003 | 0.284 | 0.006 | 0.300 | 0.003 | - | - |
Urinary ACR, mg/g creatininea | 0.305 | 0.001 | 0.321 | 0.001 | 0.299 | 0.004 | 0.321 | 0.001 |
Model 1: adjusted for age and sex; Model 2: adjusted for Model 1+duration of T2DM, diabetic retinopathy and ACE inhibitor/ARB use; Model 3: adjusted for Model 2+glycated hemoglobin, alanine aminotransferasea, gamma glutamyl transferasea and triglyceridea; Model 4: adjusted for Model 3+body mass index and waist circumference.
CAP, controlled attenuation parameter; STD, standardized coefficient; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; HbA1c, glycosylated hemoglobin; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; BMI, body mass index; ACR, albumin-to-creatinine ratio.
a Log transformed.
Parameter | Odds ratio (95% CI) | P value |
---|---|---|
Univariate logistic regression analysis | ||
Age, yr | 0.97 (0.94–0.99) | 0.030 |
Male sex | 1.05 (0.48–2.32) | 0.897 |
BMI, kg/m2 | 1.29 (1.13–1.48) | <0.001 |
Waist circumference, cm | 1.02 (1.02–1.11) | 0.008 |
Duration of T2DM, yr | 0.94 (0.89–0.99) | 0.034 |
ACE inhibitors or ARB use | 0.27 (0.28–1.44) | 0.273 |
HbA1c, % | 1.00 (0.83–1.21) | 0.986 |
HOMA-IRa | 1.32 (0.85–2.05) | 0.223 |
AST, IU/La | 1.22 (0.52–2.86) | 0.643 |
ALT, IU/La | 1.36 (0.74–2.51) | 0.328 |
γ-GT, IU/La | 1.33 (0.76–2.32) | 0.317 |
Triglyceride, mg/dLa | 2.43 (1.04–5.68) | 0.040 |
LDL-C, mg/dLa | 3.79 (1.36–10.55) | 0.011 |
Urinary ACR, mg/g creatininea | 1.54 (1.17–2.03) | 0.002 |
Multivariable logistic regression analysis | ||
Age, yr | 1.02 (0.98–1.06) | 0.443 |
BMI, kg/m2 | 1.34 (1.15–1.57) | <0.001 |
Duration of T2DM, yr | 0.97 (0.89–1.05) | 0.475 |
ACE inhibitors or ARB use | 0.38 (0.12–1.14) | 0.085 |
LDL-C, mg/dLa | 4.33 (1.20–15.63) | 0.025 |
Urinary ACR, mg/g creatininea | 1.88 (1.31–2.71) | 0.001 |
CI, confidence interval; BMI, body mass index; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; HbA1c, glycosylated hemoglobin; HOMA-IR, homeostatic model assessment of insulin resistance; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; LDL-C, low density lipoprotein cholesterol; ACR, albumin-to-creatinine ratio.
a Log transformed.
Characteristic | Total (n=100) | Patients without significant steatosis (n=44) | Patients with significant steatosis (n=56) | P value |
---|---|---|---|---|
Age, yr | 53.0±15.5 | 56.8±14.5 | 49.9±15.7 | 0.026 |
Male sex | 53 (53.0) | 23 (52.3) | 30 (53.6) | 0.897 |
Duration of T2DM, yr | 7.1±7.3 | 8.9±8.7 | 5.7±5.9 | 0.036 |
Body mass index, kg/m2 | 26.5±4.3 | 24.6±3.4 | 28.1±4.2 | <0.001 |
Obesity | 59 (59.0) | 16 (36.4) | 43 (76.8) | <0.001 |
Waist circumference, cm | 90.7±10.5 | 87.4±9.7 | 93.3±10.4 | 0.005 |
Central obesity | 60 (60.0) | 21 (47.7) | 39 (69.6) | 0.026 |
Current smoking | 23 (23.0) | 15 (34.1) | 8 (14.8) | 0.064 |
Regular exercise | 33 (33.0) | 14 (28.0) | 19 (38.0) | 0.288 |
SBP, mm Hg | 126.7±12.5 | 125.1±13.0 | 128.0±12.0 | 0.229 |
DBP, mm Hg | 72.8±11.7 | 70.1±14.0 | 74.9±9.0 | 0.056 |
FPG, mg/dL | 136.5±50.1 | 142.8±58.8 | 131.5±42.0 | 0.267 |
HbA1c, % | 7.9±2.0 | 8.0±2.2 | 7.9±2.0 | 0.986 |
PPPG, mg/dL | 186.2±65.2 | 184.0±61.5 | 188.0±68.6 | 0.757 |
BUN, mg/dL | 14.9±5.3 | 15.9±6.5 | 14.2±3.9 | 0.097 |
Creatinine, mg/dL | 0.8±0.2 | 0.8±0.2 | 0.8±0.2 | 0.371 |
eGFR, mL/min/1.73 m2 | 98.5±25.1 | 93.4±22.6 | 102.5±26.4 | 0.069 |
Albumin, mg/dL | 4.6±0.4 | 4.5±0.4 | 4.6±0.4 | 0.602 |
Total cholesterol, mg/dL | 150.0 (126.0–181.0) | 142.5 (119.5–170.3) | 159.0 (136.0–195.0) | 0.019 |
Triglyceride, mg/dL | 124.0 (101–177.7) | 117.2 (90.4–157.6) | 141.0 (111.0–185.0) | 0.034 |
HDL-C, mg/dL | 47.1 (36.4–53.4) | 48.5 (35.3–58.0) | 46.1 (40.1–52.1) | 0.726 |
LDL-C, mg/dL | 74.0 (54.5–94.0) | 61.5 (47.0–81.0) | 80.7 (63.3–100.1) | 0.006 |
AST, IU/L | 25.0 (19.0–37.0) | 25.0 (19.0–40.8) | 24.5 (20.0–36.3) | 0.622 |
ALT, IU/L | 29.0 (17.0–51.0) | 28.5 (16.3–51.8) | 29.5 (19.5–50.5) | 0.391 |
γ-GT, IU/L | 35.0 (21.0–55.0) | 35.0 (17.3–52.8) | 33.0 (23.0–61.0) | 0.428 |
HOMA-IR | 2.1 (1.2–4.0) | 1.8 (1.3–3.8) | 2.2 (1.4–4.3) | 0.242 |
CAP, dB/m | 302.3±47.2 | 260.3±29.9 | 335.3±28.2 | <0.001 |
Liver stiffness measurement, kPa | 6.1±2.6 | 5.7±2.7 | 6.4±2.5 | 0.194 |
Urinary ACR, mg/g creatinine | 5.0 (1.7–17.2) | 2.8 (1.1–8.0) | 8.8 (2.4–50.8) | 0.002 |
Albuminuria | 21 (21.0) | 3 (6.8) | 18 (32.1) | 0.002 |
Comorbidities | ||||
Hypertension | 36 (35.0) | 18 (40.9) | 18 (32.1) | 0.365 |
Cardiovascular disease | 10 (10.0) | 6 (13.6) | 4 (7.1) | 0.283 |
Diabetic retinopathy | 6 (6.0) | 4 (9.1) | 2 (3.0) | 0.249 |
Diabetic neuropathy | 16 (16.0) | 9 (20.5) | 7 (12.5) | 0.281 |
Medications | ||||
Metformin | 97 (97.0) | 43 (97.7) | 54 (96.4) | 0.706 |
Sulfonylurea | 30 (30.0) | 14 (31.8) | 16 (28.6) | 0.725 |
Thiazolidinedione | 7 (7.0) | 1 (2.3) | 6 (10.7) | 0.101 |
Insulin | 24 (24.0) | 9 (20.5) | 15 (26.8) | 0.462 |
Lipid lowering agents | 70 (70.0) | 29 (65.9) | 41 (73.2) | 0.429 |
ACE inhibitor/ARB | 35 (35.0) | 18 (40.9) | 17 (30.4) | 0.272 |
Parameter | r | P value |
---|---|---|
Age, yr | –0.321 | 0.001 |
BMI, kg/m2 | 0.449 | <0.001 |
Waist circumference, cm | 0.339 | 0.001 |
Duration of T2DM, yr | –0.266 | 0.007 |
Presence of diabetic retinopathy | –0.081 | 0.421 |
ACE inhibitor/ARB use | 0.018 | 0.858 |
FPG, mg/dL | –0.101 | 0.316 |
HbA1c, % | –0.065 | 0.521 |
PPPG, mg/dL | –0.035 | 0.730 |
AST, IU/L |
0.192 | 0.056 |
ALT, IU/L |
0.319 | 0.001 |
γ-GT, IU/L |
0.281 | 0.005 |
Triglyceride, mg/dL |
0.281 | 0.005 |
LDL-C, mg/dL |
0.101 | 0.322 |
HOMA-IR |
0.113 | 0.301 |
eGFR, mL/min/1.73 m2 | 0.166 | 0.099 |
Urinary ACR, mg/g creatinine |
0.331 | 0.001 |
Variable | Model 1 |
Model 2 |
Model 3 |
Model 4 |
||||
---|---|---|---|---|---|---|---|---|
STD β | P value | STD β | P value | STD β | P value | STD β | P value | |
Duration of T2DM, yr | –0.160 | 0.135 | - | - | - | - | - | - |
Diabetic retinopathy | –0.414 | 0.680 | - | - | - | - | - | - |
ACE inhibitor/ARB use | 0.382 | 0.704 | - | - | - | - | - | - |
HbA1c, % | –0.177 | 0.083 | –0.157 | 0.131 | - | - | - | - |
ALT, IU/L |
0.153 | 0.119 | 0.195 | 0.081 | - | - | - | - |
γ-GT, IU/L |
0.096 | 0.344 | 0.060 | 0.574 | - | - | - | - |
Triglyceride, mg/dL |
0.198 | 0.062 | 0.213 | 0.047 | - | - | - | - |
BMI, kg/m2 | 0.391 | 0.001 | 0.380 | <0.001 | 0.364 | <0.001 | - | - |
Waist circumference, cm | 0.287 | 0.003 | 0.284 | 0.006 | 0.300 | 0.003 | - | - |
Urinary ACR, mg/g creatinine |
0.305 | 0.001 | 0.321 | 0.001 | 0.299 | 0.004 | 0.321 | 0.001 |
Parameter | Odds ratio (95% CI) | P value |
---|---|---|
Univariate logistic regression analysis | ||
Age, yr | 0.97 (0.94–0.99) | 0.030 |
Male sex | 1.05 (0.48–2.32) | 0.897 |
BMI, kg/m2 | 1.29 (1.13–1.48) | <0.001 |
Waist circumference, cm | 1.02 (1.02–1.11) | 0.008 |
Duration of T2DM, yr | 0.94 (0.89–0.99) | 0.034 |
ACE inhibitors or ARB use | 0.27 (0.28–1.44) | 0.273 |
HbA1c, % | 1.00 (0.83–1.21) | 0.986 |
HOMA-IR |
1.32 (0.85–2.05) | 0.223 |
AST, IU/L |
1.22 (0.52–2.86) | 0.643 |
ALT, IU/L |
1.36 (0.74–2.51) | 0.328 |
γ-GT, IU/L |
1.33 (0.76–2.32) | 0.317 |
Triglyceride, mg/dL |
2.43 (1.04–5.68) | 0.040 |
LDL-C, mg/dL |
3.79 (1.36–10.55) | 0.011 |
Urinary ACR, mg/g creatinine |
1.54 (1.17–2.03) | 0.002 |
Multivariable logistic regression analysis | ||
Age, yr | 1.02 (0.98–1.06) | 0.443 |
BMI, kg/m2 | 1.34 (1.15–1.57) | <0.001 |
Duration of T2DM, yr | 0.97 (0.89–1.05) | 0.475 |
ACE inhibitors or ARB use | 0.38 (0.12–1.14) | 0.085 |
LDL-C, mg/dL |
4.33 (1.20–15.63) | 0.025 |
Urinary ACR, mg/g creatinine |
1.88 (1.31–2.71) | 0.001 |
Values are presented as mean±standard deviation, number (%), or median (interquartile range). T2DM, type 2 diabetes mellitus; SBP, systolic blood pressure; DBP, diastolic blood pressure; FPG, fasting plasma glucose; HbA1c, glycosylated hemoglobin; PPPG, postprandial plasma glucose; BUN, blood urea nitrogen; eGFR, estimated glomerular filtration rate; HDL-C, high density lipoprotein cholesterol; LDL-C, low density lipoprotein cholesterol; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; HOMA-IR, homeostatic model assessment of insulin resistance; CAP, controlled attenuation parameter; ACR, albumin-to-creatinine ratio; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker.
CAP, controlled attenuation parameter; BMI, body mass index; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; FPG, fasting plasma glucose; HbA1c, glycosylated hemoglobin; PPPG, postprandial plasma glucose; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; LDL-C, low density lipoprotein cholesterol; HOMA-IR, homeostatic model assessment of insulin resistance; eGFR, estimated glomerular filtration rate; ACR, albumin-to-creatinine ratio. Log transformed.
Model 1: adjusted for age and sex; Model 2: adjusted for Model 1+duration of T2DM, diabetic retinopathy and ACE inhibitor/ARB use; Model 3: adjusted for Model 2+glycated hemoglobin, alanine aminotransferasea, gamma glutamyl transferasea and triglyceridea; Model 4: adjusted for Model 3+body mass index and waist circumference. CAP, controlled attenuation parameter; STD, standardized coefficient; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; HbA1c, glycosylated hemoglobin; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; BMI, body mass index; ACR, albumin-to-creatinine ratio. Log transformed.
CI, confidence interval; BMI, body mass index; T2DM, type 2 diabetes mellitus; ACE, angiotensin-converting enzyme; ARB, angiotensin II receptor blocker; HbA1c, glycosylated hemoglobin; HOMA-IR, homeostatic model assessment of insulin resistance; AST, aspartate transaminase; ALT, alanine transferase; γ-GT, gamma glutamyltransferase; LDL-C, low density lipoprotein cholesterol; ACR, albumin-to-creatinine ratio. Log transformed.