Article Search
검색
검색 팝업 닫기

Metrics

Help

  • 1. Aims and Scope

    Gut and Liver is an international journal of gastroenterology, focusing on the gastrointestinal tract, liver, biliary tree, pancreas, motility, and neurogastroenterology. Gut atnd Liver delivers up-to-date, authoritative papers on both clinical and research-based topics in gastroenterology. The Journal publishes original articles, case reports, brief communications, letters to the editor and invited review articles in the field of gastroenterology. The Journal is operated by internationally renowned editorial boards and designed to provide a global opportunity to promote academic developments in the field of gastroenterology and hepatology. +MORE

  • 2. Editorial Board

    Editor-in-Chief + MORE

    Editor-in-Chief
    Yong Chan Lee Professor of Medicine
    Director, Gastrointestinal Research Laboratory
    Veterans Affairs Medical Center, Univ. California San Francisco
    San Francisco, USA

    Deputy Editor

    Deputy Editor
    Jong Pil Im Seoul National University College of Medicine, Seoul, Korea
    Robert S. Bresalier University of Texas M. D. Anderson Cancer Center, Houston, USA
    Steven H. Itzkowitz Mount Sinai Medical Center, NY, USA
  • 3. Editorial Office
  • 4. Articles
  • 5. Instructions for Authors
  • 6. File Download (PDF version)
  • 7. Ethical Standards
  • 8. Peer Review

    All papers submitted to Gut and Liver are reviewed by the editorial team before being sent out for an external peer review to rule out papers that have low priority, insufficient originality, scientific flaws, or the absence of a message of importance to the readers of the Journal. A decision about these papers will usually be made within two or three weeks.
    The remaining articles are usually sent to two reviewers. It would be very helpful if you could suggest a selection of reviewers and include their contact details. We may not always use the reviewers you recommend, but suggesting reviewers will make our reviewer database much richer; in the end, everyone will benefit. We reserve the right to return manuscripts in which no reviewers are suggested.

    The final responsibility for the decision to accept or reject lies with the editors. In many cases, papers may be rejected despite favorable reviews because of editorial policy or a lack of space. The editor retains the right to determine publication priorities, the style of the paper, and to request, if necessary, that the material submitted be shortened for publication.

Search

Search

Year

to

Article Type

Original Article

Split Viewer

Association between Bioelectrical Impedance Parameters, Magnetic Resonance Imaging Muscle Parameters, and Fatty Liver Severity in Children and Adolescents

Kyungchul Song1 , Eun Gyung Seol2 , Eunju Lee3 , Hye Sun Lee3 , Hana Lee1 , Hyun Wook Chae1 , Hyun Joo Shin4

1Department of Pediatrics, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea; 2Department of Pediatrics, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea; 3Biostatistics Collaboration Unit, Yonsei University College of Medicine, Seoul, Korea; 4Department of Radiology, Research Institute of Radiological Science and Center for Clinical Imaging Data Science, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea

Correspondence to: Hyun Joo Shin
ORCID https://orcid.org/0000-0002-7462-2609
E-mail lamer-22@yuhs.ac

Received: July 29, 2024; Revised: August 19, 2024; Accepted: August 25, 2024

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.

Gut Liver 2025;19(1):108-115. https://doi.org/10.5009/gnl240342

Published online January 3, 2025, Published date January 15, 2025

Copyright © Gut and Liver.

Background/Aims: To evaluate the associations between pediatric fatty liver severity, bioelectrical impedance analysis (BIA), and magnetic resonance imaging parameters, including total psoas muscle surface area (tPMSA) and paraspinal muscle fat (PMF).
Methods: Children and adolescents who underwent BIA and liver magnetic resonance imaging between September 2022 and November 2023 were included. Linear regression analyses identified predictors of liver proton density fat fraction (PDFF) including BIA parameters, tPMSA, and PMF. Ordinal logistic regression analysis identified the association between these parameters and fatty liver grades. Pearson’s correlation coefficients were used to evaluate the relationships between tPMSA and muscle-related BIA parameters, and between PMF and fat-related BIA parameters.
Results: Overall, 74 participants aged 8 to 16 years were included in the study. In the linear regression analyses, the percentage of body fat was positively associated with PDFF in all participants, whereas muscle-related BIA parameters were negatively associated with PDFF in participants with obesity. PMF and the PMF index were positively associated with PDFF in normalweight and overweight participants. In the ordinal logistic regression, percentage of body fat was positively associated with fatty liver grade in normal-weight and overweight participants and those with obesity, whereas muscle-related BIA parameters were negatively associated with fatty liver grade in participants with obesity. The PMF index was positively associated with fatty liver grade in normal/overweight participants. In the Pearson correlation analysis, muscle-related BIA parameters were correlated with tPMSA, and the fat-related BIA parameters were correlated with PMF.
Conclusions: BIA parameters and PMF are potential screening tools for assessing fatty liver in children.

Keywords: Child, Fatty liver, Non-alcoholic fatty liver disease, Magnetic resonance imaging, Body composition

Nonalcoholic fatty liver disease (NAFLD) is a chronic liver disorder marked by the excess fat accumulation in the liver, ranging from simple steatosis to nonalcoholic steatohepatitis and hepatic fibrosis.1-3 The pathogenesis of pediatric NAFLD is closely linked to metabolic syndrome and cardiovascular disease, with key factors including central obesity and insulin resistance. These metabolic disturbances result in excessive fat accumulation in the liver, reflecting the hepatic manifestation of metabolic syndrome in children and adolescents with obesity.2,4 In addition, the risks of cardiovascular disease and liver fibrosis are correlated with fatty liver severity.5,6 NAFLD has high global prevalence, affecting 52.5% of children with obesity.7 In Korean children, its prevalence increased from 8.2% in 2009 to 16.8% in 2020.8,9 For screening pediatric NAFLD, alanine aminotransferase (ALT) and ultrasonography are suggested; however, their use is restricted due to limited sensitivity, need for blood sampling, and high costs.1,2,10

Based on the relationship between obesity and NAFLD, anthropometric measurements, including body mass index (BMI), are used for NAFLD assessment.2,11 A pediatric guideline suggests NAFLD screening administration for children with overweight and obesity.11 However, this assessment is limited because NAFLD is associated with muscle and fat contents as well as body weight.10,12 Considering this relationship, assessing body composition using bioelectrical impedance analysis (BIA) has been suggested as an alternative method for screening of obesity-related comorbidities, including NAFLD.10,13 However, investigations on the relationship between BIA parameters and fatty liver severity in children are limited.

Body composition assessment using imaging has been suggested in previous studies.14,15 El-Leithy and Kamal15 reported that the total psoas muscle surface area (tPMSA) is correlated with handgrip strength and disease severity in patients with hepatic cirrhosis. A Japanese study reported that muscle and fat mass assessed using computed tomography were related to the prognosis of patients who underwent liver transplantation.14 However, few studies have demonstrated the association of muscle and fat mass measured using magnetic resonance imaging (MRI) with other body composition measurement tools, including BIA, or their relationship with pediatric fatty liver disease.

This study aimed to explore the association of fatty liver grade with BIA and MRI muscle parameters, including tPMSA and paraspinal muscle fat (PMF), in children and adolescents. Additionally, we aimed to investigate the correlation between BIA parameters and tPMSA and PMF.

1. Study population

This study was performed in accordance with Strengthening the Reporting of Observational Studies in Epidemiology guidelines and regulations. The Institutional Review Board of Yongin Severance Hospital approved this retrospective study, and the need for informed consent was waived (IRB number: 9-2023-0068).

This retrospective, cross-sectional study included children and adolescents (aged <18 years) who visited the pediatric endocrinology outpatient clinic of our hospital for evaluation of obesity-related complications including fatty liver and/or abnormal liver enzymes from September 2022 to October 2023. Patients who underwent both BIA and liver fat quantification using MRI were enrolled in the study. We excluded participants with other causes of fatty liver, including alcohol consumption and hepatitis B or C viral infections.

2. Anthropometric measurements, laboratory tests, and BIA

Height was measured to the nearest 0.1 cm, and body weight was recorded using an electronic scale with an accuracy of 0.01 kg. BMI was then calculated by dividing the weight in kilograms by the height in meters squared (kg/m²). Height, weight, and BMI were expressed relative to the standard deviation scores (SDS) from the 2017 Korean national growth charts.16 We measured waist circumference (WC) by positioning a tape measure horizontally at the midpoint between the lowest rib and the iliac crest.10 Participants were categorized into three BMI groups: normal-weight (<85th percentile), overweight (85th to 95th percentile), or obese (≥95th percentile).16

Blood samples were collected from the antecubital vein following an 8-hour fast, then processed and promptly refrigerated. Serum aspartate transaminase and ALT levels were analyzed using an absorbance assay on a Roche Cobas 8000 c702 (Roche Diagnostics, Mannheim, Germany). The concentrations of hepatitis B surface antigen and anti-hepatitis C virus antibodies were also measured using the Roche Cobas 8000 c702 system.

For BIA parameters, skeletal muscle mass (SMM), fat-free mass (FFM), appendicular skeletal muscle mass (ASM), percentage of body fat (PBF), and visceral fat area (VFA) were measured using an InBody720 body composition analyzer (Biospace, Seoul, South Korea).

3. MRI acquisition and analysis of MRI parameters

Abbreviated liver fat quantification MRI was conducted on a 3-T system (Ingenia Elition X; Philips Medical Systems, Best, Netherlands) for patients who could cooperate without sedation, according to the clinical necessity in our institution. The sequences included axial single-shot fast spin-echo T2-weighted images and a three-dimensional volumetric multi-echo gradient sequence for proton density fat fraction (PDFF). The MRI settings for PDFF were as follows: repetition time, 5.7 milliseconds; echo time, 2.6 milliseconds; matrix, 160×160; slice thickness, 6 mm; flip angle, 3°; number of signal averages, 1; with six gradient echoes from 0.9 to 4.4 milliseconds. The total acquisition time was 15 seconds.17,18

To measure the liver PDFF value, an experienced board-certified pediatric radiologist drew four regions of interest (ROIs) in the liver parenchyma at different axial slices of the PDFF map on a picture archiving and communication system. By drawing ROIs, the fat signal percentages of the liver were automatically calculated, and the mean measurement (%) value was utilized as a representative value. Fatty liver grades by PDFF were defined as in a previous study: normal for PDFF ≤6%, mild for PDFF >6%, moderate for PDFF >17.5%, and severe for PDFF >23.3%.19 NAFLD was defined as a PDFF >6% in the MRI in the absence of other causes of fatty liver including alcohol consumption and hepatitis B or C viral infections.

The MRI muscle parameters, tPMSA and PMF, were evaluated. To measure tPMSA, the largest ROIs were separately drawn in the psoas muscles bilaterally on a single axial T2-weighted image at the mid L3 vertebra level, and the mean value (mm2) was used. To measure PMF, the largest ROIs were drawn in the paraspinal muscles bilaterally on a single axial PDFF map at the mid L2 vertebra level, and the mean value (%) was used, as in a previous study.20 The tPMSA index was calculated as tPMSA divided by height in meters squared (m2), and the PMF index was calculated as PMF divided by height in meters squared (m2).21

4. Statistical analysis

All continuous variables were presented as mean± standard deviation, whereas categorical variables were presented as numbers (percentages). Baseline characteristics were compared using the independent t-test for continuous variables and the chi-square test for categorical variables after dividing the participants into normal-weight, overweight, and obese groups. Linear regression analyses were conducted to identify predictors of liver PDFF, including variables such as BMI SDS, WC, tPMSA, PMF, SMM, FFM, PBF, and ALT. Ordinal logistic regression analyses were used to determine the association between independent variables and fatty liver grades using PDFF. Multivariable ordinal logistic regression analyses were performed after adjusting for age and sex. Odds ratios (ORs) with 95% confidence intervals and p-values were reported. Cutoff points for each parameter that maximize the sum of sensitivity and specificity were derived based on the Youden index. The Pearson correlation coefficients were calculated to assess the relationships between tPMSA and muscle-related BIA parameters (SMM, FFM, and ASM), and between PMF and fat-related BIA parameters (PBF and VFA). The results of the Pearson correlation are demonstrated in the forest plot. Statistical significance was set at p<0.05, and all analyses were performed using SAS (version 9.4; SAS Inc., Cary, NC, USA) and R, version 4.3.2 (The R Foundation for Statistical Computing; Vienna, Austria; http://www.R-project.org).

1. Baseline characteristics

During the study period, 727 patients visited our hospital for evaluation of obesity-related complications including fatty liver and/or abnormal liver enzymes, and 274 of these patients underwent BIA. Of the 274 participants, 74 were included because they underwent MRI. None of the participants were excluded from the study because they had no other causes of hepatic steatosis, including hepatitis viral infection or alcohol consumption. Table 1 shows the baseline characteristics of the participants. Mean age was 11.96±2.03 years, and among all participants, the participants with normal BMI, overweight, and obesity were 4, 13, and 57, respectively. The proportion of NAFLD among the participants in the normal-weight, overweight, and obesity groups were 83.78%, 76.47%, and 85.96%, respectively. Weight SDS, BMI SDS, WC, SMM, PBF, FFM, and ASM were higher in the participants with obesity than in normal-weight and overweight participants (p=0.022 for FMM, p=0.023 for ASM, p<0.001 for the others).

Table 1. Characteristics of the Participants According to BMI

CharacteristicTotalNormal and overweight (n=17)Obesity (n=57)p-value
Age, yr11.96±2.0311.80±2.0612.00±2.040.722
Male sex46 (62.16)9 (52.94)37 (64.91)0.372
Height SDS0.99±1.150.54±1.251.13±1.090.065
Weight SDS2.39±1.041.14±0.702.77±0.81<0.001
BMI SDS2.55±1.071.18±0.442.96±0.84<0.001
BMI class
Normal4 (5.41)4 (5.41)0
Overweight13 (17.57)13 (17.57)0
Obesity57 (77.03)057 (100.0)
WC, cm90.43±11.8778.56±6.5394.03±10.73<0.001
AST, IU/L34.26±29.2135.94±24.7533.75±30.600.789
ALT, IU/L40.24±39.3336.24±30.9641.44±41.670.635
PBF, %38.14±6.7232.02±5.2039.97± 6.03<0.001
VFA, cm2122.70±42.6777.90±25.66136.06±37.35<0.001
SMM, kg40.07±11.4234.52±10.1241.73±11.330.021
FFM, kg42.58±12.1636.70±10.7844.33±12.080.022
ASM, kg16.89±5.6614.18±5.1517.70±5.600.023
tPMSA, mm2714.68±510.00679.24±530.60725.25±508.060.747
tPMSA index286.20±184.34278.55±181.30288.48±186.760.847
PMF, %3.77±1.793.41±1.133.88±1.940.219
PMF index1.59±0.871.51±0.601.62±0.940.558
Liver PDFF, %19.99±12.9418.71±13.6120.37±12.840.646
NAFLD62 (83.78)13 (76.47)49 (85.96)0.454
Fatty liver grade by PDFF0.714
Normal (PDFF≤6%)12 (16.22)4 (23.53)8 (14.04)
Mild (6%24 (32.43)5 (29.41)19 (33.33)
Moderate (17.5%9 (12.16)1 (5.88)8 (14.04)
Severe (PDFF>23.3%)29 (39.19)7 (41.18)22 (38.60)

Data are presented as mean±SD or number (%).

BMI, body mass index; SDS, standard deviation score; WC, waist circumference; AST, aspartate aminotransferase; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat; PDFF, proton density fat fraction; NAFLD, nonalcoholic fatty liver disease.



2. Linear regression analyses for liver PDFF

Table 2 shows the results from the linear regression analyses for liver PDFF. In logistic regression analyses, ALT was positively associated with PDFF in the total group (β=0.17, p<0.001) and obese group (β=0.16, p<0.001). PBF was positively associated with PDFF in the total group (β=0.69, p=0.002), normal-weight and overweight (β=1.33, p=0.037), and obese groups (β=0.76, p=0.007). SMM, FFM, ASM were negatively associated with PDFF in the total group (SMM: β=–0.41, p=0.002; FFM: β=–0.38, p=0.002; ASM: β=–0.79, p=0.003) and obesity group (SMM: β=–0.42, p=0.004; FFM: β=–0.40, p=0.004; ASM: β=–0.82, p=0.006). PMF and the PMF index were positively associated with PDFF in the normal-weight and overweight groups (PMF: β=6.17, p=0.036; PMF index: β=11.50, p=0.039).

Table 2. Linear Regression Analyses for Liver PDFF

VariableTotalNormal and overweightObesity
β (95% CI)p-valueβ (95% CI)p-valueβ (95% CI)p-value
BMI SDS0.53 (–2.30 to 3.37)0.708–5.62 (–22.37 to 11.13)0.4850.60 (–3.54 to 4.74)0.773
WC–0.14 (–0.39 to 0.12)0.292–0.55 (–1.65 to 0.56)0.309–0.22 (–0.54 to 0.10)0.171
ALT0.17 (0.10 to 0.23)<0.0010.21 (–0.00 to 0.42)0.0540.16 (0.09 to 0.23)<0.001
PBF0.69 (0.27 to 1.12)0.0021.33 (0.09 to 2.57)0.0370.76 (0.22 to 1.29)0.007
VFA0.00 (–0.07 to 0.07)0.986–0.03 (–0.33 to 0.26)0.809–0.01 (–0.10 to 0.08)0.821
SMM–0.41 (–0.65 to –0.16)0.002–0.61 (–1.27 to 0.05)0.069–0.42 (–0.70 to –0.14)0.004
FFM–0.38 (–0.62 to –0.15)0.002–0.57 (–1.19 to 0.06)0.071–0.40 (–0.66 to –0.13)0.004
ASM–0.79 (–1.29 to –0.29)0.003–1.15 (–2.46 to 0.16)0.082–0.82 (–1.40 to –0.24)0.006
tPMSA–0.00 (–0.01 to 0.00)0.139–0.01 (–0.02 to 0.00)0.086–0.00 (–0.01 to 0.00)0.478
tPMSA index–0.01 (–0.02 to 0.01)0.485–0.03 (–0.07 to 0.01)0.1020.00 (–0.02 to 0.02)0.928
PMF0.58 (–1.11 to 2.28)0.4966.17 (0.45 to 11.88)0.0360.00 (–1.79 to 1.79)0.999
PMF index2.21 (–1.24 to 5.66)0.20511.50 (0.65 to 22.36)0.0391.10 (–2.57 to 4.78)0.549

PDFF, proton density fat fraction; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat.



3. Ordinal logistic regression analyses for fatty liver grade by PDFF

Table 3 shows the results from the ordinal logistic regression analyses for fatty liver grade by PDFF. In univariable logistic regression analyses, ALT was positively related with fatty liver grade in the total group (OR=1.11, p<0.001), and obese group (OR=1.15, p<0.001). PBF was positively associated with higher fatty liver grades in the total group (OR=1.11, p=0.002), normal-weight and overweight (OR=1.27, p=0.024), and obesity groups (OR=1.11, p=0.012). SMM, FFM, and ASM were negatively associated with fatty liver grade in the total group (SMM: OR=0.94, p=0.003; FFM: OR=0.95, p=0.003; ASM: OR=0.90, p=0.005) and obese group (SMM: OR=0.95, p=0.010; FFM: OR=0.95, p=0.009; ASM: OR=0.90, p=0.014). The PMF index was positively associated with fatty liver grade in the normal-weight and overweight groups (OR=7.65, p=0.047).

Table 3. Ordinal Logistic Regression Analyses for Fatty Liver Grade by PDFF

VariableTotalNormal and overweightObesity
OR (95% CI)p-valueOR (95% CI)p-valueOR (95% CI)p-value
Univariable ordinal logistic regression analyses
BMI SDS1.03 (0.70–1.53)0.8640.44 (0.04–3.44)0.4421.02 (0.58–1.79)0.951
WC0.98 (0.94–1.01)0.1870.91 (0.77–1.05)0.1890.97 (0.92–1.01)0.114
ALT1.11 (1.06–1.16)<0.0011.04 (1.00–1.12)0.1281.15 (1.08–1.23)<0.001
PBF1.11 (1.04–1.19)0.0021.27 (1.05–1.60)0.0241.11 (1.03–1.21)0.012
VFA1.00 (0.99–1.01)0.7980.99 (0.95–1.03)0.6161.00 (0.98–1.01)0.639
SMM0.94 (0.91–0.98)0.0030.90 (0.79–1.00)0.0650.95 (0.90–0.99)0.010
FFM0.95 (0.91–0.98)0.0030.91 (0.80–1.00)0.0660.95 (0.91–0.99)0.009
ASM0.90 (0.83–0.97)0.0050.83 (0.65–1.01)0.0780.90 (0.82–0.98)0.014
tPMSA1.00 (1.00–1.00)0.4261.00 (1.00–1.00)0.1471.00 (1.00–1.00)0.923
tPMSA index1.00 (1.00–1.00)0.9691.00 (0.99–1.00)0.1461.00 (1.00–1.00)0.481
PMF1.12 (0.89–1.43)0.3502.96 (1.12–11.91)0.0551.04 (0.82–1.34)0.723
PMF index1.45 (0.90–2.50)0.1477.65 (1.19–75.58)0.0471.26 (0.78–2.15)0.355
Multivariable logistic regression analyses*
BMI SDS1.08 (0.73–1.59)0.7000.31 (0.02–3.01)0.3261.09 (0.61–1.98)0.767
WC1.00 (0.95–1.04)0.8150.95 (0.76–1.18)0.6510.98 (0.92–1.03)0.412
ALT1.10 (1.06–1.16)<0.0011.03 (0.98–1.11)0.3091.15 (1.08–1.23)<0.001
PBF1.10 (1.03–1.18)0.0071.23 (1.01–1.58)0.0591.11 (1.02–1.21)0.022
VFA1.00 (0.99–1.01)0.6971.00 (0.96–1.04)0.9351.00 (0.99–1.01)0.938
SMM0.93 (0.88–0.99)0.0270.91 (0.71–1.09)0.3370.91 (0.85–0.98)0.011
FFM0.94 (0.88–0.99)0.0260.92 (0.73–1.08)0.3490.92 (0.86–0.98)0.011
ASM0.88 (0.78–1.00)0.0470.87 (0.58–1.22)0.4410.85 (0.73–0.97)0.020
tPMSA1.00 (1.00–1.00)0.6241.00 (1.00–1.00)0.4371.00 (1.00–1.00)0.997
tPMSA index1.00 (1.00–1.00)0.9241.00 (0.99–1.00)0.3341.00 (1.00–1.00)0.573
PMF1.11 (0.87–1.42)0.4052.71 (0.97–10.66)0.0791.04 (0.81–1.33)0.767
PMF index1.30 (0.79–2.25)0.3135.58 (0.54–83.53)0.1581.19 (0.71–2.04)0.512

PDFF, proton density fat fraction; OR, odds ratio; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat.

*Adjusting for age and sex.



In multivariable logistic regression analyses after adjusting age and sex, ALT was positively related with fatty liver grade in the total group (OR=1.10, p<0.001), and obese group (OR=1.15, p<0.001). PBF was positively associated with higher fatty liver grades in the total group (OR=1.10, p=0.007) and obesity groups (OR=1.11, p=0.022). SMM, FFM, and ASM were negatively associated with fatty liver grade in the total group (SMM: OR=0.93, p=0.027; FFM: OR=0.94, p=0.026; ASM: OR=0.88, p=0.047) and obese group (SMM: OR=0.91, p=0.011; FFM: OR=0.92, p=0.011; ASM: OR=0.85, p=0.020).

4. Cutoff points for the parameters to predict NAFLD

Supplementary Table 1 shows the results of optimal cutoff points for the parameters which was significantly correlated with fatty liver grade in the multivariable ordinal logistic regression analyses. The cutoff points for PBF, SMM, FFM, and ASM were >34.90%, <42.15 kg, <44.85 kg, and <16.54 kg, respectively. The sensitivity for these values was 0.84, 0.69, 0.69, and 0.60, respectively, while the specificity was 0.67, 0.58, 0.58, and 0.67, respectively.

5. Correlation of MRI muscle parameters with BIA parameters

Fig. 1 shows the forest plot of the correlation of tPMSA with muscle-related BIA parameters and of PMF with fat-related BIA parameters for all the participants. tPMSA was positively correlated with SMM (r=0.40, p<0.001), FFM (r=0.40, p<0.001), and ASM (r=0.41, p<0.001) among the participants. PMF was positively correlated with PBF (r=0.47, p<0.001) and VFA (r=0.30, p=0.008) among the participants.

Figure 1.Forest plot of the Pearson correlation of bioelectrical impedance analysis parameters with total psoas muscle surface area (tPMSA) and paraspinal muscle fat (PMF). SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; PBF, percentage of body fat; VFA, visceral fat area; CI, confidence interval.

Our study demonstrated that PBF, PMF, and the PMF index were positively correlated with liver PDFF, whereas all muscle-related BIA parameters were negatively correlated with liver PDFF among children and adolescents. The univariable ordinal logistic regression analyses demonstrated that PBF and the PMF index were positively associated with fatty liver grade, whereas all muscle-related BIA parameters were negatively associated with fatty liver grade in children and adolescents. In addition, PBF and all muscle-related BIA parameters were significantly related with fatty liver grade even after adjusting age and sex. In the correlation analyses of the MRI muscle parameters, tPMSA was positively correlated with all muscle-related BIA parameters, whereas PMF was positively correlated with all fat-related BIA parameters.

The BIA parameters, PMF, and PMF index, were associated with fatty liver grade, whereas the BMI SDS and WC were not significantly related with fatty liver grade. Moreover, PBF, SMM, FFM, and ASM were significantly correlated with fatty liver grade even after adjusting age and sex. In pediatric fatty liver assessment, traditional measures, such as the BMI and WC, have limitations due to their inability to distinguish between muscle and fat mass, which can lead to misclassification of metabolic risk.10,12,13,22 To overcome these limitations, investigations on relationship between body composition and fatty liver were conducted.10,23,24 A meta-analysis reported that skeletal muscle index was negatively associated with NAFLD in adults.13 In a Chinese study, BIA outperformed anthropometric indices in predicting NAFLD among children.24 In a cross-sectional study, the predictability of waist-to-hip ratio for hepatic steatosis increased when combined with PBF or VFA.10

PBF and muscle-related BIA parameters were associated with fatty liver grade in the obesity group, not in the normal and overweight groups after adjusting age and sex. We divided the participants into normal and overweight group and obesity because differences in muscle and fat mass between normal and overweight, and obese children can impact obesity-related comorbidities including fatty liver.8,11,25 In the obesity group, larger amounts of adipose tissue can have more significant adverse effects on fatty liver.2,22,23 Consequently, the protective effects of muscle mass might become more apparent in this group. In a Korean study conducted in children who were overweight and obese, PBF was positively correlated with ALT elevation, whereas muscle-related BIA parameters, including SMM, FFM, and ASM, were negatively correlated with ALT elevation.10 The association between muscle parameters and fatty liver grade in obese children underscores the importance of a comprehensive approach to managing pediatric NAFLD that includes both fat and muscle assessments.

PMF and the PMF index were positively associated with liver PDFF. PMF was associated with fatty liver grade in children with normal BMI and overweight status, whereas tPMSA did not show a significant relationship with fatty liver grade. This difference can be attributed to the nature of the measurements, wherein tPMSA primarily reflects muscle mass, which may not directly indicate liver fat content or overall adiposity.20 In contrast, the PMF index measures fat infiltration in muscles, which is more closely associated with overall body fat and metabolic dysfunction, both of which are key factors in the development and severity of fatty liver disease.10,20,23 In a previous cohort study, fat mass was a more effective predictor for NAFLD among children than muscle mass was.23 In a Korean study, among children, tPMSA and PMF were positively associated with obesity but were not significantly associated with liver fat after adjusting for BMI.20 More studies are required to clarify the association of fatty liver with tPMSA and PMF.

Muscle-related BIA parameters, including SMM, FFM, and ASM, correlated with tPMSA, whereas fat-related BIA parameters, including PBF and VFA, correlated with PMF although coefficients of correlation were not high. In a Japanese study, SMM was positively associated with tPMSA.26 BIA devices are easily accessible outside medical facilities and provide a noninvasive body composition assessment method without radiation exposure.10,26 Given that BIA showed strong correlations with tPMSA and PMF measured by MRI as well as with the severity of fatty liver, we propose that BIA could serve as a practical method for body composition assessment in the management of NAFLD.

This study has some limitations. First, its retrospective design and the fact that the population was limited to Koreans restrict the generalizability of the findings. Second, genetic and environmental factors, such as nutrition and physical activity, were not considered. Third, our study focused on children and adolescents attending a real-world clinic for the evaluation of obesity-related comorbidities, resulting in a relatively higher proportion of fatty liver even among children with normal BMI and those who were overweight, compared to the general population. Additionally, participants with normal BMI and those who were overweight were combined due to the small sample sizes in these groups. This focus on a population predominantly affected by obesity led to a smaller number of normal-weight and overweight participants. Fourth, NAFLD was diagnosed using MRI rather than the gold standard of liver biopsy. However, MRI is the most accurate diagnostic tool for hepatic steatosis in imaging studies, as it provides the fatty liver grade using PDFF. Moreover, we assessed body composition using both BIA and MRI and provided insights into their relationship with NAFLD.

In conclusion, our study demonstrated an association between fatty liver grade and BIA parameters, including PBF and all muscle-related BIA parameters, as well as PMF and the PMF index, among children and adolescents. Moreover, PBF and all muscle-related BIA parameters were associated with fatty liver severity even after adjusting for age and sex, while anthropometric measurements were not. Fat-related BIA parameters correlated with PMF, and muscle-related BIA parameters correlated with tPMSA. Considering the noninvasive nature of BIA, its lack of radiation exposure, and its accessibility, these findings are particularly meaningful in the context of pediatric care and underscore the importance and practicality of considering body composition when assessing pediatric fatty liver. Additionally, our study provides a foundation for future research to explore the role of body composition assessments in the screening and management of NAFLD in children and adolescents.

The authors would like to thank InBody Corporation for providing the bioelectrical impedance analysis equipment.

Study concept and design: K.S., H.J.S. Data acquisition: K.S., E.G.S., H.L., H.J.S. Data analysis and interpretation: K.S., H.J.S. Drafting of the manuscript: K.S. Critical revision of the manuscript for important intellectual content: H.J.S. Statistical analysis: E.L. Administrative, technical, or material support; study supervision: H.S.L., H.W.C., H.J.S. Approval of final manuscript: all authors.

  1. Song K, Park G, Lee HS, et al. Comparison of the triglyceride glucose index and modified triglyceride glucose indices to predict nonalcoholic fatty liver disease in youths. J Pediatr 2022;242:79-85.
    Pubmed CrossRef
  2. Song K, Kim HS, Chae HW. Nonalcoholic fatty liver disease and insulin resistance in children. Clin Exp Pediatr 2023;66:512-519.
    Pubmed KoreaMed CrossRef
  3. Lee HW, Kim M, Youn J, Singh S, Ahn SH. Liver diseases in South Korea: a pulse check of the public's knowledge, awareness, and behaviors. Yonsei Med J 2022;63:1088-1098.
    Pubmed KoreaMed CrossRef
  4. Zhang L, El-Shabrawi M, Baur LA, et al. An international multidisciplinary consensus on pediatric metabolic dysfunction-associated fatty liver disease. Med 2024;5:797-815.
    Pubmed CrossRef
  5. Petta S, Maida M, Macaluso FS, et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology 2015;62:1101-1110.
    Pubmed CrossRef
  6. Sung KC, Ryan MC, Wilson AM. The severity of nonalcoholic fatty liver disease is associated with increased cardiovascular risk in a large cohort of non-obese Asian subjects. Atherosclerosis 2009;203:581-586.
    Pubmed CrossRef
  7. Li J, Ha A, Rui F, et al. Meta-analysis: global prevalence, trend and forecasting of non-alcoholic fatty liver disease in children and adolescents, 2000-2021. Aliment Pharmacol Ther 2022;56:396-406.
    Pubmed CrossRef
  8. Song K, Park G, Lee HS, et al. Trends in prediabetes and non-alcoholic fatty liver disease associated with abdominal obesity among Korean children and adolescents: based on the Korea National Health and Nutrition Examination Survey between 2009 and 2018. Biomedicines 2022;10:584.
    Pubmed KoreaMed CrossRef
  9. Song K, Yang J, Lee HS, et al. Changes in the prevalences of obesity, abdominal obesity, and non-alcoholic fatty liver disease among Korean children during the COVID-19 outbreak. Yonsei Med J 2023;64:269-277.
    Pubmed KoreaMed CrossRef
  10. Song K, Seol EG, Yang H, et al. Bioelectrical impedance parameters add incremental value to waist-to-hip ratio for prediction of metabolic dysfunction associated steatotic liver disease in youth with overweight and obesity. Front Endocrinol (Lausanne) 2024;15:1385002.
    Pubmed KoreaMed CrossRef
  11. Vos MB, Abrams SH, Barlow SE, et al. NASPGHAN clinical practice guideline for the diagnosis and treatment of nonalcoholic fatty liver disease in children: recommendations from the Expert Committee on NAFLD (ECON) and the North American Society of Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN). J Pediatr Gastroenterol Nutr 2017;64:319-334.
    Pubmed KoreaMed CrossRef
  12. Kim HY, Kim JH. Temporal trends in the prevalence of metabolically healthy overweight and obesity in Korean youth: data from the Korea National Health and Nutrition Examination Survey 2011-2019. Ann Pediatr Endocrinol Metab 2022;27:134-141.
    Pubmed KoreaMed CrossRef
  13. Cai C, Song X, Chen Y, Chen X, Yu C. Relationship between relative skeletal muscle mass and nonalcoholic fatty liver disease: a systematic review and meta-analysis. Hepatol Int 2020;14:115-126.
    Pubmed KoreaMed CrossRef
  14. Hamaguchi Y, Kaido T, Okumura S, et al. Impact of skeletal muscle mass index, intramuscular adipose tissue content, and visceral to subcutaneous adipose tissue area ratio on early mortality of living donor liver transplantation. Transplantation 2017;101:565-574.
    Pubmed CrossRef
  15. El-Leithy N, Kamal H. The value of CT imaging and psoas muscle index in grading the severity of sarcopenia in liver cirrhosis patients and its impact on morbidity and mortality. Med J Cairo Univ 2021;89:2157-2168.
    CrossRef
  16. Kim JH, Yun S, Hwang SS, et al. The 2017 Korean National Growth Charts for children and adolescents: development, improvement, and prospects. Korean J Pediatr 2018;61:135-149.
    Pubmed KoreaMed CrossRef
  17. Song K, Son NH, Chang DR, Chae HW, Shin HJ. Feasibility of ultrasound attenuation imaging for assessing pediatric hepatic steatosis. Biology (Basel) 2022;11:1087.
    Pubmed KoreaMed CrossRef
  18. Kim DK, Yoon H, Han K, et al. Effect of different driver power amplitudes on liver stiffness measurement in pediatric liver MR elastography. Abdom Radiol (NY) 2021;46:4729-4735.
    Pubmed CrossRef
  19. Shin J, Kim MJ, Shin HJ, et al. Quick assessment with controlled attenuation parameter for hepatic steatosis in children based on MRI-PDFF as the gold standard. BMC Pediatr 2019;19:112.
    Pubmed KoreaMed CrossRef
  20. Albakheet SS, Lee MJ, Yoon H, Shin HJ, Koh H. Psoas muscle area and paraspinal muscle fat in children and young adults with or without obesity and fatty liver. PLoS One 2021;16:e0259948.
    Pubmed KoreaMed CrossRef
  21. Yodoshi T, Orkin S, Arce Clachar AC, et al. Muscle mass is linked to liver disease severity in pediatric nonalcoholic fatty liver disease. J Pediatr 2020;223:93-99.
    Pubmed KoreaMed CrossRef
  22. Bonsembiante L, Targher G, Maffeis C. Non-alcoholic fatty liver disease in obese children and adolescents: a role for nutrition?. Eur J Clin Nutr 2022;76:28-39.
    Pubmed CrossRef
  23. Kim HY, Baik SJ, Lee HA, et al. Relative fat mass at baseline and its early change may be a predictor of incident nonalcoholic fatty liver disease. Sci Rep 2020;10:17491.
    Pubmed KoreaMed CrossRef
  24. Lee LW, Yen JB, Lu HK, Liao YS. Prediction of nonalcoholic fatty liver disease by anthropometric indices and bioelectrical impedance analysis in children. Child Obes 2021;17:551-558.
    Pubmed CrossRef
  25. Wells JC, Fewtrell MS, Williams JE, Haroun D, Lawson MS, Cole TJ. Body composition in normal weight, overweight and obese children: matched case-control analyses of total and regional tissue masses, and body composition trends in relation to relative weight. Int J Obes (Lond) 2006;30:1506-1513.
    Pubmed CrossRef
  26. Orkin S, Yodoshi T, Romantic E, et al. Body composition measured by bioelectrical impedance analysis is a viable alternative to magnetic resonance imaging in children with nonalcoholic fatty liver disease. JPEN J Parenter Enteral Nutr 2022;46:378-384.
    Pubmed KoreaMed CrossRef

Article

Original Article

Gut and Liver 2025; 19(1): 108-115

Published online January 15, 2025 https://doi.org/10.5009/gnl240342

Copyright © Gut and Liver.

Association between Bioelectrical Impedance Parameters, Magnetic Resonance Imaging Muscle Parameters, and Fatty Liver Severity in Children and Adolescents

Kyungchul Song1 , Eun Gyung Seol2 , Eunju Lee3 , Hye Sun Lee3 , Hana Lee1 , Hyun Wook Chae1 , Hyun Joo Shin4

1Department of Pediatrics, Gangnam Severance Hospital, Yonsei University College of Medicine, Seoul, Korea; 2Department of Pediatrics, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea; 3Biostatistics Collaboration Unit, Yonsei University College of Medicine, Seoul, Korea; 4Department of Radiology, Research Institute of Radiological Science and Center for Clinical Imaging Data Science, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea

Correspondence to:Hyun Joo Shin
ORCID https://orcid.org/0000-0002-7462-2609
E-mail lamer-22@yuhs.ac

Received: July 29, 2024; Revised: August 19, 2024; Accepted: August 25, 2024

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.

Abstract

Background/Aims: To evaluate the associations between pediatric fatty liver severity, bioelectrical impedance analysis (BIA), and magnetic resonance imaging parameters, including total psoas muscle surface area (tPMSA) and paraspinal muscle fat (PMF).
Methods: Children and adolescents who underwent BIA and liver magnetic resonance imaging between September 2022 and November 2023 were included. Linear regression analyses identified predictors of liver proton density fat fraction (PDFF) including BIA parameters, tPMSA, and PMF. Ordinal logistic regression analysis identified the association between these parameters and fatty liver grades. Pearson’s correlation coefficients were used to evaluate the relationships between tPMSA and muscle-related BIA parameters, and between PMF and fat-related BIA parameters.
Results: Overall, 74 participants aged 8 to 16 years were included in the study. In the linear regression analyses, the percentage of body fat was positively associated with PDFF in all participants, whereas muscle-related BIA parameters were negatively associated with PDFF in participants with obesity. PMF and the PMF index were positively associated with PDFF in normalweight and overweight participants. In the ordinal logistic regression, percentage of body fat was positively associated with fatty liver grade in normal-weight and overweight participants and those with obesity, whereas muscle-related BIA parameters were negatively associated with fatty liver grade in participants with obesity. The PMF index was positively associated with fatty liver grade in normal/overweight participants. In the Pearson correlation analysis, muscle-related BIA parameters were correlated with tPMSA, and the fat-related BIA parameters were correlated with PMF.
Conclusions: BIA parameters and PMF are potential screening tools for assessing fatty liver in children.

Keywords: Child, Fatty liver, Non-alcoholic fatty liver disease, Magnetic resonance imaging, Body composition

INTRODUCTION

Nonalcoholic fatty liver disease (NAFLD) is a chronic liver disorder marked by the excess fat accumulation in the liver, ranging from simple steatosis to nonalcoholic steatohepatitis and hepatic fibrosis.1-3 The pathogenesis of pediatric NAFLD is closely linked to metabolic syndrome and cardiovascular disease, with key factors including central obesity and insulin resistance. These metabolic disturbances result in excessive fat accumulation in the liver, reflecting the hepatic manifestation of metabolic syndrome in children and adolescents with obesity.2,4 In addition, the risks of cardiovascular disease and liver fibrosis are correlated with fatty liver severity.5,6 NAFLD has high global prevalence, affecting 52.5% of children with obesity.7 In Korean children, its prevalence increased from 8.2% in 2009 to 16.8% in 2020.8,9 For screening pediatric NAFLD, alanine aminotransferase (ALT) and ultrasonography are suggested; however, their use is restricted due to limited sensitivity, need for blood sampling, and high costs.1,2,10

Based on the relationship between obesity and NAFLD, anthropometric measurements, including body mass index (BMI), are used for NAFLD assessment.2,11 A pediatric guideline suggests NAFLD screening administration for children with overweight and obesity.11 However, this assessment is limited because NAFLD is associated with muscle and fat contents as well as body weight.10,12 Considering this relationship, assessing body composition using bioelectrical impedance analysis (BIA) has been suggested as an alternative method for screening of obesity-related comorbidities, including NAFLD.10,13 However, investigations on the relationship between BIA parameters and fatty liver severity in children are limited.

Body composition assessment using imaging has been suggested in previous studies.14,15 El-Leithy and Kamal15 reported that the total psoas muscle surface area (tPMSA) is correlated with handgrip strength and disease severity in patients with hepatic cirrhosis. A Japanese study reported that muscle and fat mass assessed using computed tomography were related to the prognosis of patients who underwent liver transplantation.14 However, few studies have demonstrated the association of muscle and fat mass measured using magnetic resonance imaging (MRI) with other body composition measurement tools, including BIA, or their relationship with pediatric fatty liver disease.

This study aimed to explore the association of fatty liver grade with BIA and MRI muscle parameters, including tPMSA and paraspinal muscle fat (PMF), in children and adolescents. Additionally, we aimed to investigate the correlation between BIA parameters and tPMSA and PMF.

MATERIALS AND METHODS

1. Study population

This study was performed in accordance with Strengthening the Reporting of Observational Studies in Epidemiology guidelines and regulations. The Institutional Review Board of Yongin Severance Hospital approved this retrospective study, and the need for informed consent was waived (IRB number: 9-2023-0068).

This retrospective, cross-sectional study included children and adolescents (aged <18 years) who visited the pediatric endocrinology outpatient clinic of our hospital for evaluation of obesity-related complications including fatty liver and/or abnormal liver enzymes from September 2022 to October 2023. Patients who underwent both BIA and liver fat quantification using MRI were enrolled in the study. We excluded participants with other causes of fatty liver, including alcohol consumption and hepatitis B or C viral infections.

2. Anthropometric measurements, laboratory tests, and BIA

Height was measured to the nearest 0.1 cm, and body weight was recorded using an electronic scale with an accuracy of 0.01 kg. BMI was then calculated by dividing the weight in kilograms by the height in meters squared (kg/m²). Height, weight, and BMI were expressed relative to the standard deviation scores (SDS) from the 2017 Korean national growth charts.16 We measured waist circumference (WC) by positioning a tape measure horizontally at the midpoint between the lowest rib and the iliac crest.10 Participants were categorized into three BMI groups: normal-weight (<85th percentile), overweight (85th to 95th percentile), or obese (≥95th percentile).16

Blood samples were collected from the antecubital vein following an 8-hour fast, then processed and promptly refrigerated. Serum aspartate transaminase and ALT levels were analyzed using an absorbance assay on a Roche Cobas 8000 c702 (Roche Diagnostics, Mannheim, Germany). The concentrations of hepatitis B surface antigen and anti-hepatitis C virus antibodies were also measured using the Roche Cobas 8000 c702 system.

For BIA parameters, skeletal muscle mass (SMM), fat-free mass (FFM), appendicular skeletal muscle mass (ASM), percentage of body fat (PBF), and visceral fat area (VFA) were measured using an InBody720 body composition analyzer (Biospace, Seoul, South Korea).

3. MRI acquisition and analysis of MRI parameters

Abbreviated liver fat quantification MRI was conducted on a 3-T system (Ingenia Elition X; Philips Medical Systems, Best, Netherlands) for patients who could cooperate without sedation, according to the clinical necessity in our institution. The sequences included axial single-shot fast spin-echo T2-weighted images and a three-dimensional volumetric multi-echo gradient sequence for proton density fat fraction (PDFF). The MRI settings for PDFF were as follows: repetition time, 5.7 milliseconds; echo time, 2.6 milliseconds; matrix, 160×160; slice thickness, 6 mm; flip angle, 3°; number of signal averages, 1; with six gradient echoes from 0.9 to 4.4 milliseconds. The total acquisition time was 15 seconds.17,18

To measure the liver PDFF value, an experienced board-certified pediatric radiologist drew four regions of interest (ROIs) in the liver parenchyma at different axial slices of the PDFF map on a picture archiving and communication system. By drawing ROIs, the fat signal percentages of the liver were automatically calculated, and the mean measurement (%) value was utilized as a representative value. Fatty liver grades by PDFF were defined as in a previous study: normal for PDFF ≤6%, mild for PDFF >6%, moderate for PDFF >17.5%, and severe for PDFF >23.3%.19 NAFLD was defined as a PDFF >6% in the MRI in the absence of other causes of fatty liver including alcohol consumption and hepatitis B or C viral infections.

The MRI muscle parameters, tPMSA and PMF, were evaluated. To measure tPMSA, the largest ROIs were separately drawn in the psoas muscles bilaterally on a single axial T2-weighted image at the mid L3 vertebra level, and the mean value (mm2) was used. To measure PMF, the largest ROIs were drawn in the paraspinal muscles bilaterally on a single axial PDFF map at the mid L2 vertebra level, and the mean value (%) was used, as in a previous study.20 The tPMSA index was calculated as tPMSA divided by height in meters squared (m2), and the PMF index was calculated as PMF divided by height in meters squared (m2).21

4. Statistical analysis

All continuous variables were presented as mean± standard deviation, whereas categorical variables were presented as numbers (percentages). Baseline characteristics were compared using the independent t-test for continuous variables and the chi-square test for categorical variables after dividing the participants into normal-weight, overweight, and obese groups. Linear regression analyses were conducted to identify predictors of liver PDFF, including variables such as BMI SDS, WC, tPMSA, PMF, SMM, FFM, PBF, and ALT. Ordinal logistic regression analyses were used to determine the association between independent variables and fatty liver grades using PDFF. Multivariable ordinal logistic regression analyses were performed after adjusting for age and sex. Odds ratios (ORs) with 95% confidence intervals and p-values were reported. Cutoff points for each parameter that maximize the sum of sensitivity and specificity were derived based on the Youden index. The Pearson correlation coefficients were calculated to assess the relationships between tPMSA and muscle-related BIA parameters (SMM, FFM, and ASM), and between PMF and fat-related BIA parameters (PBF and VFA). The results of the Pearson correlation are demonstrated in the forest plot. Statistical significance was set at p<0.05, and all analyses were performed using SAS (version 9.4; SAS Inc., Cary, NC, USA) and R, version 4.3.2 (The R Foundation for Statistical Computing; Vienna, Austria; http://www.R-project.org).

RESULTS

1. Baseline characteristics

During the study period, 727 patients visited our hospital for evaluation of obesity-related complications including fatty liver and/or abnormal liver enzymes, and 274 of these patients underwent BIA. Of the 274 participants, 74 were included because they underwent MRI. None of the participants were excluded from the study because they had no other causes of hepatic steatosis, including hepatitis viral infection or alcohol consumption. Table 1 shows the baseline characteristics of the participants. Mean age was 11.96±2.03 years, and among all participants, the participants with normal BMI, overweight, and obesity were 4, 13, and 57, respectively. The proportion of NAFLD among the participants in the normal-weight, overweight, and obesity groups were 83.78%, 76.47%, and 85.96%, respectively. Weight SDS, BMI SDS, WC, SMM, PBF, FFM, and ASM were higher in the participants with obesity than in normal-weight and overweight participants (p=0.022 for FMM, p=0.023 for ASM, p<0.001 for the others).

Table 1 . Characteristics of the Participants According to BMI.

CharacteristicTotalNormal and overweight (n=17)Obesity (n=57)p-value
Age, yr11.96±2.0311.80±2.0612.00±2.040.722
Male sex46 (62.16)9 (52.94)37 (64.91)0.372
Height SDS0.99±1.150.54±1.251.13±1.090.065
Weight SDS2.39±1.041.14±0.702.77±0.81<0.001
BMI SDS2.55±1.071.18±0.442.96±0.84<0.001
BMI class
Normal4 (5.41)4 (5.41)0
Overweight13 (17.57)13 (17.57)0
Obesity57 (77.03)057 (100.0)
WC, cm90.43±11.8778.56±6.5394.03±10.73<0.001
AST, IU/L34.26±29.2135.94±24.7533.75±30.600.789
ALT, IU/L40.24±39.3336.24±30.9641.44±41.670.635
PBF, %38.14±6.7232.02±5.2039.97± 6.03<0.001
VFA, cm2122.70±42.6777.90±25.66136.06±37.35<0.001
SMM, kg40.07±11.4234.52±10.1241.73±11.330.021
FFM, kg42.58±12.1636.70±10.7844.33±12.080.022
ASM, kg16.89±5.6614.18±5.1517.70±5.600.023
tPMSA, mm2714.68±510.00679.24±530.60725.25±508.060.747
tPMSA index286.20±184.34278.55±181.30288.48±186.760.847
PMF, %3.77±1.793.41±1.133.88±1.940.219
PMF index1.59±0.871.51±0.601.62±0.940.558
Liver PDFF, %19.99±12.9418.71±13.6120.37±12.840.646
NAFLD62 (83.78)13 (76.47)49 (85.96)0.454
Fatty liver grade by PDFF0.714
Normal (PDFF≤6%)12 (16.22)4 (23.53)8 (14.04)
Mild (6%24 (32.43)5 (29.41)19 (33.33)
Moderate (17.5%9 (12.16)1 (5.88)8 (14.04)
Severe (PDFF>23.3%)29 (39.19)7 (41.18)22 (38.60)

Data are presented as mean±SD or number (%)..

BMI, body mass index; SDS, standard deviation score; WC, waist circumference; AST, aspartate aminotransferase; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat; PDFF, proton density fat fraction; NAFLD, nonalcoholic fatty liver disease..



2. Linear regression analyses for liver PDFF

Table 2 shows the results from the linear regression analyses for liver PDFF. In logistic regression analyses, ALT was positively associated with PDFF in the total group (β=0.17, p<0.001) and obese group (β=0.16, p<0.001). PBF was positively associated with PDFF in the total group (β=0.69, p=0.002), normal-weight and overweight (β=1.33, p=0.037), and obese groups (β=0.76, p=0.007). SMM, FFM, ASM were negatively associated with PDFF in the total group (SMM: β=–0.41, p=0.002; FFM: β=–0.38, p=0.002; ASM: β=–0.79, p=0.003) and obesity group (SMM: β=–0.42, p=0.004; FFM: β=–0.40, p=0.004; ASM: β=–0.82, p=0.006). PMF and the PMF index were positively associated with PDFF in the normal-weight and overweight groups (PMF: β=6.17, p=0.036; PMF index: β=11.50, p=0.039).

Table 2 . Linear Regression Analyses for Liver PDFF.

VariableTotalNormal and overweightObesity
β (95% CI)p-valueβ (95% CI)p-valueβ (95% CI)p-value
BMI SDS0.53 (–2.30 to 3.37)0.708–5.62 (–22.37 to 11.13)0.4850.60 (–3.54 to 4.74)0.773
WC–0.14 (–0.39 to 0.12)0.292–0.55 (–1.65 to 0.56)0.309–0.22 (–0.54 to 0.10)0.171
ALT0.17 (0.10 to 0.23)<0.0010.21 (–0.00 to 0.42)0.0540.16 (0.09 to 0.23)<0.001
PBF0.69 (0.27 to 1.12)0.0021.33 (0.09 to 2.57)0.0370.76 (0.22 to 1.29)0.007
VFA0.00 (–0.07 to 0.07)0.986–0.03 (–0.33 to 0.26)0.809–0.01 (–0.10 to 0.08)0.821
SMM–0.41 (–0.65 to –0.16)0.002–0.61 (–1.27 to 0.05)0.069–0.42 (–0.70 to –0.14)0.004
FFM–0.38 (–0.62 to –0.15)0.002–0.57 (–1.19 to 0.06)0.071–0.40 (–0.66 to –0.13)0.004
ASM–0.79 (–1.29 to –0.29)0.003–1.15 (–2.46 to 0.16)0.082–0.82 (–1.40 to –0.24)0.006
tPMSA–0.00 (–0.01 to 0.00)0.139–0.01 (–0.02 to 0.00)0.086–0.00 (–0.01 to 0.00)0.478
tPMSA index–0.01 (–0.02 to 0.01)0.485–0.03 (–0.07 to 0.01)0.1020.00 (–0.02 to 0.02)0.928
PMF0.58 (–1.11 to 2.28)0.4966.17 (0.45 to 11.88)0.0360.00 (–1.79 to 1.79)0.999
PMF index2.21 (–1.24 to 5.66)0.20511.50 (0.65 to 22.36)0.0391.10 (–2.57 to 4.78)0.549

PDFF, proton density fat fraction; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat..



3. Ordinal logistic regression analyses for fatty liver grade by PDFF

Table 3 shows the results from the ordinal logistic regression analyses for fatty liver grade by PDFF. In univariable logistic regression analyses, ALT was positively related with fatty liver grade in the total group (OR=1.11, p<0.001), and obese group (OR=1.15, p<0.001). PBF was positively associated with higher fatty liver grades in the total group (OR=1.11, p=0.002), normal-weight and overweight (OR=1.27, p=0.024), and obesity groups (OR=1.11, p=0.012). SMM, FFM, and ASM were negatively associated with fatty liver grade in the total group (SMM: OR=0.94, p=0.003; FFM: OR=0.95, p=0.003; ASM: OR=0.90, p=0.005) and obese group (SMM: OR=0.95, p=0.010; FFM: OR=0.95, p=0.009; ASM: OR=0.90, p=0.014). The PMF index was positively associated with fatty liver grade in the normal-weight and overweight groups (OR=7.65, p=0.047).

Table 3 . Ordinal Logistic Regression Analyses for Fatty Liver Grade by PDFF.

VariableTotalNormal and overweightObesity
OR (95% CI)p-valueOR (95% CI)p-valueOR (95% CI)p-value
Univariable ordinal logistic regression analyses
BMI SDS1.03 (0.70–1.53)0.8640.44 (0.04–3.44)0.4421.02 (0.58–1.79)0.951
WC0.98 (0.94–1.01)0.1870.91 (0.77–1.05)0.1890.97 (0.92–1.01)0.114
ALT1.11 (1.06–1.16)<0.0011.04 (1.00–1.12)0.1281.15 (1.08–1.23)<0.001
PBF1.11 (1.04–1.19)0.0021.27 (1.05–1.60)0.0241.11 (1.03–1.21)0.012
VFA1.00 (0.99–1.01)0.7980.99 (0.95–1.03)0.6161.00 (0.98–1.01)0.639
SMM0.94 (0.91–0.98)0.0030.90 (0.79–1.00)0.0650.95 (0.90–0.99)0.010
FFM0.95 (0.91–0.98)0.0030.91 (0.80–1.00)0.0660.95 (0.91–0.99)0.009
ASM0.90 (0.83–0.97)0.0050.83 (0.65–1.01)0.0780.90 (0.82–0.98)0.014
tPMSA1.00 (1.00–1.00)0.4261.00 (1.00–1.00)0.1471.00 (1.00–1.00)0.923
tPMSA index1.00 (1.00–1.00)0.9691.00 (0.99–1.00)0.1461.00 (1.00–1.00)0.481
PMF1.12 (0.89–1.43)0.3502.96 (1.12–11.91)0.0551.04 (0.82–1.34)0.723
PMF index1.45 (0.90–2.50)0.1477.65 (1.19–75.58)0.0471.26 (0.78–2.15)0.355
Multivariable logistic regression analyses*
BMI SDS1.08 (0.73–1.59)0.7000.31 (0.02–3.01)0.3261.09 (0.61–1.98)0.767
WC1.00 (0.95–1.04)0.8150.95 (0.76–1.18)0.6510.98 (0.92–1.03)0.412
ALT1.10 (1.06–1.16)<0.0011.03 (0.98–1.11)0.3091.15 (1.08–1.23)<0.001
PBF1.10 (1.03–1.18)0.0071.23 (1.01–1.58)0.0591.11 (1.02–1.21)0.022
VFA1.00 (0.99–1.01)0.6971.00 (0.96–1.04)0.9351.00 (0.99–1.01)0.938
SMM0.93 (0.88–0.99)0.0270.91 (0.71–1.09)0.3370.91 (0.85–0.98)0.011
FFM0.94 (0.88–0.99)0.0260.92 (0.73–1.08)0.3490.92 (0.86–0.98)0.011
ASM0.88 (0.78–1.00)0.0470.87 (0.58–1.22)0.4410.85 (0.73–0.97)0.020
tPMSA1.00 (1.00–1.00)0.6241.00 (1.00–1.00)0.4371.00 (1.00–1.00)0.997
tPMSA index1.00 (1.00–1.00)0.9241.00 (0.99–1.00)0.3341.00 (1.00–1.00)0.573
PMF1.11 (0.87–1.42)0.4052.71 (0.97–10.66)0.0791.04 (0.81–1.33)0.767
PMF index1.30 (0.79–2.25)0.3135.58 (0.54–83.53)0.1581.19 (0.71–2.04)0.512

PDFF, proton density fat fraction; OR, odds ratio; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat..

*Adjusting for age and sex..



In multivariable logistic regression analyses after adjusting age and sex, ALT was positively related with fatty liver grade in the total group (OR=1.10, p<0.001), and obese group (OR=1.15, p<0.001). PBF was positively associated with higher fatty liver grades in the total group (OR=1.10, p=0.007) and obesity groups (OR=1.11, p=0.022). SMM, FFM, and ASM were negatively associated with fatty liver grade in the total group (SMM: OR=0.93, p=0.027; FFM: OR=0.94, p=0.026; ASM: OR=0.88, p=0.047) and obese group (SMM: OR=0.91, p=0.011; FFM: OR=0.92, p=0.011; ASM: OR=0.85, p=0.020).

4. Cutoff points for the parameters to predict NAFLD

Supplementary Table 1 shows the results of optimal cutoff points for the parameters which was significantly correlated with fatty liver grade in the multivariable ordinal logistic regression analyses. The cutoff points for PBF, SMM, FFM, and ASM were >34.90%, <42.15 kg, <44.85 kg, and <16.54 kg, respectively. The sensitivity for these values was 0.84, 0.69, 0.69, and 0.60, respectively, while the specificity was 0.67, 0.58, 0.58, and 0.67, respectively.

5. Correlation of MRI muscle parameters with BIA parameters

Fig. 1 shows the forest plot of the correlation of tPMSA with muscle-related BIA parameters and of PMF with fat-related BIA parameters for all the participants. tPMSA was positively correlated with SMM (r=0.40, p<0.001), FFM (r=0.40, p<0.001), and ASM (r=0.41, p<0.001) among the participants. PMF was positively correlated with PBF (r=0.47, p<0.001) and VFA (r=0.30, p=0.008) among the participants.

Figure 1. Forest plot of the Pearson correlation of bioelectrical impedance analysis parameters with total psoas muscle surface area (tPMSA) and paraspinal muscle fat (PMF). SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; PBF, percentage of body fat; VFA, visceral fat area; CI, confidence interval.

DISCUSSION

Our study demonstrated that PBF, PMF, and the PMF index were positively correlated with liver PDFF, whereas all muscle-related BIA parameters were negatively correlated with liver PDFF among children and adolescents. The univariable ordinal logistic regression analyses demonstrated that PBF and the PMF index were positively associated with fatty liver grade, whereas all muscle-related BIA parameters were negatively associated with fatty liver grade in children and adolescents. In addition, PBF and all muscle-related BIA parameters were significantly related with fatty liver grade even after adjusting age and sex. In the correlation analyses of the MRI muscle parameters, tPMSA was positively correlated with all muscle-related BIA parameters, whereas PMF was positively correlated with all fat-related BIA parameters.

The BIA parameters, PMF, and PMF index, were associated with fatty liver grade, whereas the BMI SDS and WC were not significantly related with fatty liver grade. Moreover, PBF, SMM, FFM, and ASM were significantly correlated with fatty liver grade even after adjusting age and sex. In pediatric fatty liver assessment, traditional measures, such as the BMI and WC, have limitations due to their inability to distinguish between muscle and fat mass, which can lead to misclassification of metabolic risk.10,12,13,22 To overcome these limitations, investigations on relationship between body composition and fatty liver were conducted.10,23,24 A meta-analysis reported that skeletal muscle index was negatively associated with NAFLD in adults.13 In a Chinese study, BIA outperformed anthropometric indices in predicting NAFLD among children.24 In a cross-sectional study, the predictability of waist-to-hip ratio for hepatic steatosis increased when combined with PBF or VFA.10

PBF and muscle-related BIA parameters were associated with fatty liver grade in the obesity group, not in the normal and overweight groups after adjusting age and sex. We divided the participants into normal and overweight group and obesity because differences in muscle and fat mass between normal and overweight, and obese children can impact obesity-related comorbidities including fatty liver.8,11,25 In the obesity group, larger amounts of adipose tissue can have more significant adverse effects on fatty liver.2,22,23 Consequently, the protective effects of muscle mass might become more apparent in this group. In a Korean study conducted in children who were overweight and obese, PBF was positively correlated with ALT elevation, whereas muscle-related BIA parameters, including SMM, FFM, and ASM, were negatively correlated with ALT elevation.10 The association between muscle parameters and fatty liver grade in obese children underscores the importance of a comprehensive approach to managing pediatric NAFLD that includes both fat and muscle assessments.

PMF and the PMF index were positively associated with liver PDFF. PMF was associated with fatty liver grade in children with normal BMI and overweight status, whereas tPMSA did not show a significant relationship with fatty liver grade. This difference can be attributed to the nature of the measurements, wherein tPMSA primarily reflects muscle mass, which may not directly indicate liver fat content or overall adiposity.20 In contrast, the PMF index measures fat infiltration in muscles, which is more closely associated with overall body fat and metabolic dysfunction, both of which are key factors in the development and severity of fatty liver disease.10,20,23 In a previous cohort study, fat mass was a more effective predictor for NAFLD among children than muscle mass was.23 In a Korean study, among children, tPMSA and PMF were positively associated with obesity but were not significantly associated with liver fat after adjusting for BMI.20 More studies are required to clarify the association of fatty liver with tPMSA and PMF.

Muscle-related BIA parameters, including SMM, FFM, and ASM, correlated with tPMSA, whereas fat-related BIA parameters, including PBF and VFA, correlated with PMF although coefficients of correlation were not high. In a Japanese study, SMM was positively associated with tPMSA.26 BIA devices are easily accessible outside medical facilities and provide a noninvasive body composition assessment method without radiation exposure.10,26 Given that BIA showed strong correlations with tPMSA and PMF measured by MRI as well as with the severity of fatty liver, we propose that BIA could serve as a practical method for body composition assessment in the management of NAFLD.

This study has some limitations. First, its retrospective design and the fact that the population was limited to Koreans restrict the generalizability of the findings. Second, genetic and environmental factors, such as nutrition and physical activity, were not considered. Third, our study focused on children and adolescents attending a real-world clinic for the evaluation of obesity-related comorbidities, resulting in a relatively higher proportion of fatty liver even among children with normal BMI and those who were overweight, compared to the general population. Additionally, participants with normal BMI and those who were overweight were combined due to the small sample sizes in these groups. This focus on a population predominantly affected by obesity led to a smaller number of normal-weight and overweight participants. Fourth, NAFLD was diagnosed using MRI rather than the gold standard of liver biopsy. However, MRI is the most accurate diagnostic tool for hepatic steatosis in imaging studies, as it provides the fatty liver grade using PDFF. Moreover, we assessed body composition using both BIA and MRI and provided insights into their relationship with NAFLD.

In conclusion, our study demonstrated an association between fatty liver grade and BIA parameters, including PBF and all muscle-related BIA parameters, as well as PMF and the PMF index, among children and adolescents. Moreover, PBF and all muscle-related BIA parameters were associated with fatty liver severity even after adjusting for age and sex, while anthropometric measurements were not. Fat-related BIA parameters correlated with PMF, and muscle-related BIA parameters correlated with tPMSA. Considering the noninvasive nature of BIA, its lack of radiation exposure, and its accessibility, these findings are particularly meaningful in the context of pediatric care and underscore the importance and practicality of considering body composition when assessing pediatric fatty liver. Additionally, our study provides a foundation for future research to explore the role of body composition assessments in the screening and management of NAFLD in children and adolescents.

ACKNOWLEDGEMENTS

The authors would like to thank InBody Corporation for providing the bioelectrical impedance analysis equipment.

CONFLICTS OF INTEREST

No potential conflict of interest relevant to this article was reported.

AUTHOR CONTRIBUTIONS

Study concept and design: K.S., H.J.S. Data acquisition: K.S., E.G.S., H.L., H.J.S. Data analysis and interpretation: K.S., H.J.S. Drafting of the manuscript: K.S. Critical revision of the manuscript for important intellectual content: H.J.S. Statistical analysis: E.L. Administrative, technical, or material support; study supervision: H.S.L., H.W.C., H.J.S. Approval of final manuscript: all authors.

SUPPLEMENTARY MATERIALS

Supplementary materials can be accessed at https://doi.org/10.5009/gnl240342.

Fig 1.

Figure 1.Forest plot of the Pearson correlation of bioelectrical impedance analysis parameters with total psoas muscle surface area (tPMSA) and paraspinal muscle fat (PMF). SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; PBF, percentage of body fat; VFA, visceral fat area; CI, confidence interval.
Gut and Liver 2025; 19: 108-115https://doi.org/10.5009/gnl240342

Table 1 Characteristics of the Participants According to BMI

CharacteristicTotalNormal and overweight (n=17)Obesity (n=57)p-value
Age, yr11.96±2.0311.80±2.0612.00±2.040.722
Male sex46 (62.16)9 (52.94)37 (64.91)0.372
Height SDS0.99±1.150.54±1.251.13±1.090.065
Weight SDS2.39±1.041.14±0.702.77±0.81<0.001
BMI SDS2.55±1.071.18±0.442.96±0.84<0.001
BMI class
Normal4 (5.41)4 (5.41)0
Overweight13 (17.57)13 (17.57)0
Obesity57 (77.03)057 (100.0)
WC, cm90.43±11.8778.56±6.5394.03±10.73<0.001
AST, IU/L34.26±29.2135.94±24.7533.75±30.600.789
ALT, IU/L40.24±39.3336.24±30.9641.44±41.670.635
PBF, %38.14±6.7232.02±5.2039.97± 6.03<0.001
VFA, cm2122.70±42.6777.90±25.66136.06±37.35<0.001
SMM, kg40.07±11.4234.52±10.1241.73±11.330.021
FFM, kg42.58±12.1636.70±10.7844.33±12.080.022
ASM, kg16.89±5.6614.18±5.1517.70±5.600.023
tPMSA, mm2714.68±510.00679.24±530.60725.25±508.060.747
tPMSA index286.20±184.34278.55±181.30288.48±186.760.847
PMF, %3.77±1.793.41±1.133.88±1.940.219
PMF index1.59±0.871.51±0.601.62±0.940.558
Liver PDFF, %19.99±12.9418.71±13.6120.37±12.840.646
NAFLD62 (83.78)13 (76.47)49 (85.96)0.454
Fatty liver grade by PDFF0.714
Normal (PDFF≤6%)12 (16.22)4 (23.53)8 (14.04)
Mild (6%24 (32.43)5 (29.41)19 (33.33)
Moderate (17.5%9 (12.16)1 (5.88)8 (14.04)
Severe (PDFF>23.3%)29 (39.19)7 (41.18)22 (38.60)

Data are presented as mean±SD or number (%).

BMI, body mass index; SDS, standard deviation score; WC, waist circumference; AST, aspartate aminotransferase; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat; PDFF, proton density fat fraction; NAFLD, nonalcoholic fatty liver disease.


Table 2 Linear Regression Analyses for Liver PDFF

VariableTotalNormal and overweightObesity
β (95% CI)p-valueβ (95% CI)p-valueβ (95% CI)p-value
BMI SDS0.53 (–2.30 to 3.37)0.708–5.62 (–22.37 to 11.13)0.4850.60 (–3.54 to 4.74)0.773
WC–0.14 (–0.39 to 0.12)0.292–0.55 (–1.65 to 0.56)0.309–0.22 (–0.54 to 0.10)0.171
ALT0.17 (0.10 to 0.23)<0.0010.21 (–0.00 to 0.42)0.0540.16 (0.09 to 0.23)<0.001
PBF0.69 (0.27 to 1.12)0.0021.33 (0.09 to 2.57)0.0370.76 (0.22 to 1.29)0.007
VFA0.00 (–0.07 to 0.07)0.986–0.03 (–0.33 to 0.26)0.809–0.01 (–0.10 to 0.08)0.821
SMM–0.41 (–0.65 to –0.16)0.002–0.61 (–1.27 to 0.05)0.069–0.42 (–0.70 to –0.14)0.004
FFM–0.38 (–0.62 to –0.15)0.002–0.57 (–1.19 to 0.06)0.071–0.40 (–0.66 to –0.13)0.004
ASM–0.79 (–1.29 to –0.29)0.003–1.15 (–2.46 to 0.16)0.082–0.82 (–1.40 to –0.24)0.006
tPMSA–0.00 (–0.01 to 0.00)0.139–0.01 (–0.02 to 0.00)0.086–0.00 (–0.01 to 0.00)0.478
tPMSA index–0.01 (–0.02 to 0.01)0.485–0.03 (–0.07 to 0.01)0.1020.00 (–0.02 to 0.02)0.928
PMF0.58 (–1.11 to 2.28)0.4966.17 (0.45 to 11.88)0.0360.00 (–1.79 to 1.79)0.999
PMF index2.21 (–1.24 to 5.66)0.20511.50 (0.65 to 22.36)0.0391.10 (–2.57 to 4.78)0.549

PDFF, proton density fat fraction; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat.


Table 3 Ordinal Logistic Regression Analyses for Fatty Liver Grade by PDFF

VariableTotalNormal and overweightObesity
OR (95% CI)p-valueOR (95% CI)p-valueOR (95% CI)p-value
Univariable ordinal logistic regression analyses
BMI SDS1.03 (0.70–1.53)0.8640.44 (0.04–3.44)0.4421.02 (0.58–1.79)0.951
WC0.98 (0.94–1.01)0.1870.91 (0.77–1.05)0.1890.97 (0.92–1.01)0.114
ALT1.11 (1.06–1.16)<0.0011.04 (1.00–1.12)0.1281.15 (1.08–1.23)<0.001
PBF1.11 (1.04–1.19)0.0021.27 (1.05–1.60)0.0241.11 (1.03–1.21)0.012
VFA1.00 (0.99–1.01)0.7980.99 (0.95–1.03)0.6161.00 (0.98–1.01)0.639
SMM0.94 (0.91–0.98)0.0030.90 (0.79–1.00)0.0650.95 (0.90–0.99)0.010
FFM0.95 (0.91–0.98)0.0030.91 (0.80–1.00)0.0660.95 (0.91–0.99)0.009
ASM0.90 (0.83–0.97)0.0050.83 (0.65–1.01)0.0780.90 (0.82–0.98)0.014
tPMSA1.00 (1.00–1.00)0.4261.00 (1.00–1.00)0.1471.00 (1.00–1.00)0.923
tPMSA index1.00 (1.00–1.00)0.9691.00 (0.99–1.00)0.1461.00 (1.00–1.00)0.481
PMF1.12 (0.89–1.43)0.3502.96 (1.12–11.91)0.0551.04 (0.82–1.34)0.723
PMF index1.45 (0.90–2.50)0.1477.65 (1.19–75.58)0.0471.26 (0.78–2.15)0.355
Multivariable logistic regression analyses*
BMI SDS1.08 (0.73–1.59)0.7000.31 (0.02–3.01)0.3261.09 (0.61–1.98)0.767
WC1.00 (0.95–1.04)0.8150.95 (0.76–1.18)0.6510.98 (0.92–1.03)0.412
ALT1.10 (1.06–1.16)<0.0011.03 (0.98–1.11)0.3091.15 (1.08–1.23)<0.001
PBF1.10 (1.03–1.18)0.0071.23 (1.01–1.58)0.0591.11 (1.02–1.21)0.022
VFA1.00 (0.99–1.01)0.6971.00 (0.96–1.04)0.9351.00 (0.99–1.01)0.938
SMM0.93 (0.88–0.99)0.0270.91 (0.71–1.09)0.3370.91 (0.85–0.98)0.011
FFM0.94 (0.88–0.99)0.0260.92 (0.73–1.08)0.3490.92 (0.86–0.98)0.011
ASM0.88 (0.78–1.00)0.0470.87 (0.58–1.22)0.4410.85 (0.73–0.97)0.020
tPMSA1.00 (1.00–1.00)0.6241.00 (1.00–1.00)0.4371.00 (1.00–1.00)0.997
tPMSA index1.00 (1.00–1.00)0.9241.00 (0.99–1.00)0.3341.00 (1.00–1.00)0.573
PMF1.11 (0.87–1.42)0.4052.71 (0.97–10.66)0.0791.04 (0.81–1.33)0.767
PMF index1.30 (0.79–2.25)0.3135.58 (0.54–83.53)0.1581.19 (0.71–2.04)0.512

PDFF, proton density fat fraction; OR, odds ratio; CI, confidence interval; BMI, body mass index; SDS, standard deviation score; WC, waist circumference; ALT, alanine aminotransferase; PBF, percentage of body fat; VFA, visceral fat area; SMM, skeletal muscle mass; FFM, fat-free mass; ASM, appendicular skeletal muscle mass; tPMSA, total psoas muscle surface area; PMF, paraspinal muscle fat.

*Adjusting for age and sex.


References

  1. Song K, Park G, Lee HS, et al. Comparison of the triglyceride glucose index and modified triglyceride glucose indices to predict nonalcoholic fatty liver disease in youths. J Pediatr 2022;242:79-85.
    Pubmed CrossRef
  2. Song K, Kim HS, Chae HW. Nonalcoholic fatty liver disease and insulin resistance in children. Clin Exp Pediatr 2023;66:512-519.
    Pubmed KoreaMed CrossRef
  3. Lee HW, Kim M, Youn J, Singh S, Ahn SH. Liver diseases in South Korea: a pulse check of the public's knowledge, awareness, and behaviors. Yonsei Med J 2022;63:1088-1098.
    Pubmed KoreaMed CrossRef
  4. Zhang L, El-Shabrawi M, Baur LA, et al. An international multidisciplinary consensus on pediatric metabolic dysfunction-associated fatty liver disease. Med 2024;5:797-815.
    Pubmed CrossRef
  5. Petta S, Maida M, Macaluso FS, et al. The severity of steatosis influences liver stiffness measurement in patients with nonalcoholic fatty liver disease. Hepatology 2015;62:1101-1110.
    Pubmed CrossRef
  6. Sung KC, Ryan MC, Wilson AM. The severity of nonalcoholic fatty liver disease is associated with increased cardiovascular risk in a large cohort of non-obese Asian subjects. Atherosclerosis 2009;203:581-586.
    Pubmed CrossRef
  7. Li J, Ha A, Rui F, et al. Meta-analysis: global prevalence, trend and forecasting of non-alcoholic fatty liver disease in children and adolescents, 2000-2021. Aliment Pharmacol Ther 2022;56:396-406.
    Pubmed CrossRef
  8. Song K, Park G, Lee HS, et al. Trends in prediabetes and non-alcoholic fatty liver disease associated with abdominal obesity among Korean children and adolescents: based on the Korea National Health and Nutrition Examination Survey between 2009 and 2018. Biomedicines 2022;10:584.
    Pubmed KoreaMed CrossRef
  9. Song K, Yang J, Lee HS, et al. Changes in the prevalences of obesity, abdominal obesity, and non-alcoholic fatty liver disease among Korean children during the COVID-19 outbreak. Yonsei Med J 2023;64:269-277.
    Pubmed KoreaMed CrossRef
  10. Song K, Seol EG, Yang H, et al. Bioelectrical impedance parameters add incremental value to waist-to-hip ratio for prediction of metabolic dysfunction associated steatotic liver disease in youth with overweight and obesity. Front Endocrinol (Lausanne) 2024;15:1385002.
    Pubmed KoreaMed CrossRef
  11. Vos MB, Abrams SH, Barlow SE, et al. NASPGHAN clinical practice guideline for the diagnosis and treatment of nonalcoholic fatty liver disease in children: recommendations from the Expert Committee on NAFLD (ECON) and the North American Society of Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN). J Pediatr Gastroenterol Nutr 2017;64:319-334.
    Pubmed KoreaMed CrossRef
  12. Kim HY, Kim JH. Temporal trends in the prevalence of metabolically healthy overweight and obesity in Korean youth: data from the Korea National Health and Nutrition Examination Survey 2011-2019. Ann Pediatr Endocrinol Metab 2022;27:134-141.
    Pubmed KoreaMed CrossRef
  13. Cai C, Song X, Chen Y, Chen X, Yu C. Relationship between relative skeletal muscle mass and nonalcoholic fatty liver disease: a systematic review and meta-analysis. Hepatol Int 2020;14:115-126.
    Pubmed KoreaMed CrossRef
  14. Hamaguchi Y, Kaido T, Okumura S, et al. Impact of skeletal muscle mass index, intramuscular adipose tissue content, and visceral to subcutaneous adipose tissue area ratio on early mortality of living donor liver transplantation. Transplantation 2017;101:565-574.
    Pubmed CrossRef
  15. El-Leithy N, Kamal H. The value of CT imaging and psoas muscle index in grading the severity of sarcopenia in liver cirrhosis patients and its impact on morbidity and mortality. Med J Cairo Univ 2021;89:2157-2168.
    CrossRef
  16. Kim JH, Yun S, Hwang SS, et al. The 2017 Korean National Growth Charts for children and adolescents: development, improvement, and prospects. Korean J Pediatr 2018;61:135-149.
    Pubmed KoreaMed CrossRef
  17. Song K, Son NH, Chang DR, Chae HW, Shin HJ. Feasibility of ultrasound attenuation imaging for assessing pediatric hepatic steatosis. Biology (Basel) 2022;11:1087.
    Pubmed KoreaMed CrossRef
  18. Kim DK, Yoon H, Han K, et al. Effect of different driver power amplitudes on liver stiffness measurement in pediatric liver MR elastography. Abdom Radiol (NY) 2021;46:4729-4735.
    Pubmed CrossRef
  19. Shin J, Kim MJ, Shin HJ, et al. Quick assessment with controlled attenuation parameter for hepatic steatosis in children based on MRI-PDFF as the gold standard. BMC Pediatr 2019;19:112.
    Pubmed KoreaMed CrossRef
  20. Albakheet SS, Lee MJ, Yoon H, Shin HJ, Koh H. Psoas muscle area and paraspinal muscle fat in children and young adults with or without obesity and fatty liver. PLoS One 2021;16:e0259948.
    Pubmed KoreaMed CrossRef
  21. Yodoshi T, Orkin S, Arce Clachar AC, et al. Muscle mass is linked to liver disease severity in pediatric nonalcoholic fatty liver disease. J Pediatr 2020;223:93-99.
    Pubmed KoreaMed CrossRef
  22. Bonsembiante L, Targher G, Maffeis C. Non-alcoholic fatty liver disease in obese children and adolescents: a role for nutrition?. Eur J Clin Nutr 2022;76:28-39.
    Pubmed CrossRef
  23. Kim HY, Baik SJ, Lee HA, et al. Relative fat mass at baseline and its early change may be a predictor of incident nonalcoholic fatty liver disease. Sci Rep 2020;10:17491.
    Pubmed KoreaMed CrossRef
  24. Lee LW, Yen JB, Lu HK, Liao YS. Prediction of nonalcoholic fatty liver disease by anthropometric indices and bioelectrical impedance analysis in children. Child Obes 2021;17:551-558.
    Pubmed CrossRef
  25. Wells JC, Fewtrell MS, Williams JE, Haroun D, Lawson MS, Cole TJ. Body composition in normal weight, overweight and obese children: matched case-control analyses of total and regional tissue masses, and body composition trends in relation to relative weight. Int J Obes (Lond) 2006;30:1506-1513.
    Pubmed CrossRef
  26. Orkin S, Yodoshi T, Romantic E, et al. Body composition measured by bioelectrical impedance analysis is a viable alternative to magnetic resonance imaging in children with nonalcoholic fatty liver disease. JPEN J Parenter Enteral Nutr 2022;46:378-384.
    Pubmed KoreaMed CrossRef
Gut and Liver

Vol.19 No.1
January, 2025

pISSN 1976-2283
eISSN 2005-1212

qrcode
qrcode

Supplementary

Share this article on :

  • line

Popular Keywords

Gut and LiverQR code Download
qr-code

Editorial Office