Abstract
We aim to evaluate the prevalence of steatotic liver disease (SLD) in United States (US) adolescents and explore whether metabolic dysfunction-associated steatotic liver disease (MASLD) can identify individuals with clinically significant fibrosis (CSF) in this study. The prevalence of SLD and its categories, including MASLD, metabolic dysfunction and alcohol associated liver disease (MetALD), alcohol related liver disease (ALD) and other SLD were determined. Weighted multivariable logistic regression analysis was conducted to evaluate the association between MASLD and CSF in adolescents with SLD. Among the total 1,446 US adolescents, SLD was present in 291 (20.1%) of individuals, including 260 (17.9%) for MASLD, 9 (0.6%) for MetALD and 5 (0.3%) for ALD. Only 58 (4%) had CSF. Patients with SLD showed a higher prevalence of CSF (9.6% vs. 2.6%, p < 0.001). Among patients with SLD, 89.3% met the MASLD criteria. The risk of CSF in patients with MASLD was not significantly different (odds ratio [OR] = 1.07, 95% confidence interval [CI] = 0.30–3.83, p = 0.9180) compared with those without MASLD. MASLD was met by most of the US adolescents with SLD. Moreover, MASLD was not associated with higher prevalence of CSF among adolescents with SLD.
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Introduction
Non-alcoholic fatty liver disease (NAFLD) has emerged as the predominant etiology of chronic liver disease in children and adolescents in the United States, primarily due to the rising prevalence of obesity in the pediatric population over the past two decades1,2. Prior research has indicated a prevalence of approximately 10% in the general paediatric population3and up to 29–38% in the obese subgroup4.
A redefinition of NAFLD as metabolic dysfunction-associated fatty liver disease (MAFLD) was proposed by an international expert consensus panel to underscore the primary pathogenetic influence of metabolic dysfunction in the onset and advancement of the disease, irrespective of the presence of other steatogenic factors5. This redefinition is applicable solely to the adult population and not to adolescents and children. Multiple studies have indicated that MAFLD may be more effective in identifying individuals with significant or advanced liver fibrosis compared to NAFLD in adults6,7. Eslam et al., representing an international panel, proposed a comprehensive framework and an age-specific MAFLD definition for paediatric individuals based on sex and age percentiles, due to the variations in etiology, natural history, and prognosis of fatty liver diseases in children compared to adults8. Ciardullo S et al. reported that MAFLD criteria were met by most United States (US) adolescents with steatosis, and the prevalence of MAFLD and clinically significant fibrosis (CSF) were alarmingly high in US adolescents. In contrast to the demonstrated efficacy of MAFLD in detecting liver fibrosis in adults, they indicated that MAFLD did not improve the ability to detect more CSF in US adolescents with steatosis9.
Despite the generally accepted superiority of MAFLD over NAFLD, concerns have been raised regarding the mixing of aetiologies, the potentially stigmatizing nature of the term ‘fatty’, and restricting the population to those with two metabolic risk factors10,11. A multi-society Delphi consensus expert panel recently proposed the term “steatotic liver disease (SLD)” as a comprehensive descriptor for liver steatosis and metabolic dysfunction-associated steatotic liver disease (MASLD) to replace the term NAFLD12. The panel recommended that the presence of hepatic steatosis, along with any cardiometabolic risk factor (CMRF), should warrant a diagnosis of MASLD12. Additionally, criteria for CMRFs in both adult and pediatric populations were concurrently suggested12.
The current study seeks to determine the prevalence of specific categories of SLD, such as MASLD, metabolic dysfunction and alcohol associated liver disease (MetALD), and alcohol related liver disease (ALD), other SLD including specific etiology SLD and cryptogenic SLD within US adolescents. Additionally, the study aim to investigate whether MASLD criteria can effectively distinguish between simple steatosis and progressive liver fibrosis in adolescents with SLD. We utilized data from adolescents who participated in the National Health and Nutrition Examination Survey (NHANES) from 2017 to March 2020, employing transient elastography (TE) for the assessment of steatosis and fibrosis.
Methods
Data source
NHANES (https://www.cdc.gov/nchs/nhanes/) is a comprehensive survey conducted by the National Center for Health Statistics in the US, encompassing individuals from the non-institutionalized general population aged ≥ 2 months. This ongoing, cross-sectional program employs a stratified, multistage, clustered probability sampling design to ensure the inclusion of participants that are nationally representative13. The NHANES program has evolved into the current continuous NHANES, a two-year cycle of data collection that has been ongoing since 1999. Vibration-controlled transient elastography (VCTE) examinations have been included in the NHANES protocol since the 2017–2018 cycle. Field operations of the NHANES were halted in March 2020 due to the COVID-19 pandemic. However, the data files from the most recent NHANES cycle (August 2021-August 2023) are currently not accessible online. This study examines data from the 2017-March 2020 cycle of the NHANES program, utilizing all available VCTE data. Hepatic steatosis in this study is determined by the median controlled attenuation parameter (CAP) measured through VCTE. Only participants 12 years and older in the NHANES 2017-March 2020 were eligible for VCTE. Therefore, adolescents aged 12–18 years in the NHANES 2017–2020 cycles and have completed VCTE exam were included.
The original survey received approval from National Center for Health Statistics Ethics Review Board. Written informed consents were obtained from the guardians of participants under the age of 18 years, as well as assents from those aged 12–17 years9. The present study was granted exemption by National Center for Health Statistics Ethics Review Board. due to the complete de-identification of the data set used in the analysis.
Study population
Out of the total 15,560 participants in NHANES 2017–2020, individuals over the age of 18 (N = 9459) and under the age of 12 (N = 4327) were excluded, leaving 1,774 adolescents in the study. Participants without available TE data (N = 142) and those with unreliable TE, such as ineligible (N = 42) and partial exams (N = 144), were subsequently excluded, resulting in a final study cohort of 1,446 individuals (Fig. 1). We have checked that all the involved 1,446 participants underwent a structured interview and examination at a mobile examination center (MEC), which included physical examinations and laboratory tests.
Clinical data and laboratory tests
Demographic characteristics were obtained from Questionnaire Data. Body mass index (BMI) was calculated by dividing kilograms by weight in meters square. The cutoff criteria for BMI categories were based on the Centers for Disease Control growth chart14. The laboratory methods used for the measurement of alanine aminotransferase (ALT), aspartate aminotransferase (AST), γ-glutamyl transpeptidase (GGT), platelet count, serum glucose, albumin, and lipid profiles, including high-density lipoprotein cholesterol (HDL-C) and low-density lipoprotein cholesterol (LDL-C), have been detailed in prior literature. Elevated ALT levels were defined as > 22 IU/L in women and > 26 IU/L in men, in accordance with guidelines from the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition (NASPGHAN)15.
Definition of SLD and CSF
Noninvasive markers and scores developed to predict steatosis were not accurate enough or sufficiently validated to be clinically useful to diagnose SLD in adolescents. Clinically available ultrasound was also not accurate for the diagnosis of hepatic steatosis because of its low sensitivity and specificity. That is why NASPGHAN NAFLD guidelines do not recommend the use of ultrasound alone to diagnose fatty liver or SLD in children and adolescents15. Moreover, ultrasound data, invasive hepatic histology, CT with radiation risk, highly accurate but expensive MRI and MRS were not available in NHANES 2017–2020. Therefore, we use CAP ≥ 263dB/m to diagnose SLD in US adolescents as referred to previous published researches9.
NHANES 2017–2018 utilized VCTE to assess liver fibrosis through the median liver stiffness measurement (LSM) and to quantify liver fat using the CAP. Detailed procedures can be found in the liver ultrasound transient elastography procedures manual. SLD was characterized by a median CAP ≥ 263dB/m with elastographic evidence of steatosis, while CSF was identified by a median LSM ≥ 8.0 kPa, as indicated by prior studies16,17.
Definition of different SLD categories (MASLD, MetALD and ALD)
According to the newly proposed diagnostic criteria for MASLD in the pediatric population12, five CMRF groups have been delineated. Alcohol consumption was assessed following established protocols outlined in the existing literature18. MASLD was characterized as SLD with at least one CMRF and low alcohol consumption. MetALD was identified as SLD with at least one CMRF and moderate alcohol consumption. ALD was described as SLD without CMRFs and with excessive alcohol consumption. Specific etiology SLDs such as autoimmune hepatitis, Wilson’s disease, lysosomal storage diseases with liver involvement, and hepatitis C, et al. Cryptogenic SLD was defined as SLD with no CMRFs and other secific aetiology SLD.
Statistical analysis
Continuous variables were reported as weighted means ± standard deviations for normally distributed data, and as medians and interquartile range for non-normally distributed data, while categorical variables were presented as counts and percentages. Differences in means/medians or percentages were compared using linear regression for continuous variables and the design-adjusted chi-square test for categorical variables. Weighted multivariable logistic regression analysis was conducted to evaluate the impact of MASLD on the odds of CSF after adjusting the effect of confounding factors including age, sex and race/ethnicity. All statistical analyses were carried out using EmpowerStats (https://www.empowerstats.net/en/), which is based on R version 3.4.3 and incorporates the recommended weighting by NHANES. A two-sided p < 0.05 was considered as statistical significant.
Results
Clinical characteristics of participants with or without SLD
The clinical, laboratory, and metabolic characteristics of the 1,446 adolescents were analyzed according to whether they have SLD and are detailed in Table 1. The mean age was 15.0 years, with 47.0% being female, 17.3% classified as overweight, and 25.1% classified as obese. Only 52 individuals (4.2%) exhibited elevated ALT levels and 4 individuals (0.3%) met the condition of ALT ≥ 80IU/L. Among the five CMRFs for MASLD, overweight or obesity was the most prevalent, affecting 608 individuals (42.4%), followed by prediabetes or diabetes in 292 individuals (20.2%), elevated blood pressure in 96 individuals (6.6%), hypertriglyceridemia in 23 individuals (1.6%), and low HDL-C in 204 individuals (14.1%).
Among the total study participants, SLD was present in 291 (20.1%) of individuals, 260 (17.9%) for MASLD, 9 (0.6%) for MetALD, 5 (0.3%) for ALD (Fig. 2). Only 58 (4%) of the participants had CSF. The individuals with SLD were typically older (15.3 years vs. 14.9 years, p = 0.001) compared to those without SLD, although no significant differences were observed in terms of sex distribution and race-ethnicity origin. Laboratory parameters, including ALT, AST, GGT, and platelet count, were notably elevated in patients with SLD. Particularly, the mean ALT levels were significantly higher in patients with SLD (24.3 ± 19.0 vs. 14.2 ± 7.3, p < 0.001), but only 13.5% had elevated ALT levels and 1.6% had a value ≥ 80IU/L. Additionally, patients with SLD exhibit a distinct metabolic profile characterized by higher LDL-C (94.2 ± 26.1 vs. 85.4 ± 24.9, p < 0.001) and total cholesterol levels (160.5 ± 30.5 vs. 151.5 ± 28.9, p < 0.001). Patients with SLD were more likely to have overweight or obesity (85.9% vs. 31.4%, p < 0.001), prediabetes or diabetes (29.2% vs. 17.9%, p < 0.001), elevated BP (10.0% vs. 5.8%, p < 0.001), hypertriglyceridemia (5.2% vs. 0.7%, p < 0.001), and low HDL-C (26.8% vs. 10.9%, p < 0.001) compared with those without SLD. There was no statistically significant difference observed in alcohol consumption between participants with and without SLD. Additionally, among patients with SLD, 9 (3.1%) met the criteria for MetALD and 5 (1.7%) met the criteria for ALD. Patients with SLD exhibited a higher prevalence of CSF compared to those without SLD (9.6% vs. 2.6%, p < 0.001).
Clinical characteristics of participants with SLD based on whether they met MASLD criteria
The clinical, laboratory and metabolic features of patients with SLD based on whether they met MASLD criteria are provided in Table 2. There were no significant differences in mean age, sex distribution, or race/ethnicity between the two groups. Obese or overweight were present in the highest proportion (95.8%) of patients with MASLD. As respected BMI (33.4 ± 7.3 vs. 21.2 ± 2.5, p < 0.001) and waist circumference (104.5 ± 14.8 vs. 75.4 ± 7.7, p < 0.001) were much higher in patients with MASLD. Both the mean ALT level (25.1 ± 9.5 vs. 15.8 ± 7.5, p < 0.001) and the proportion of elevated ALT or ALT ≥ 80 IU/L in patients with MASLD were much higher than those without MASLD, but AST, platelet count, LDL-C, and total cholesterol did not differ significantly. According to the diagnostic criteria for MASLD, patients without MASLD did not exhibit overweight or obesity, prediabetes or diabetes, elevated SBP or DBP, higher triglycerides levels, and lower HDL-cholesterol levels were not found in any patient without MASLD. In contrast, among patients with MASLD, the majority (95.8%) was overweight or obese, 32.7% had prediabetes or diabetes, 30.0% had lower HDL-cholesterol levels, 11.2% had elevated SBP or DBP, and only 5.8% had hypertriglyceridemia. There was no significant difference in alcohol consumption between patients with or without MASLD.
Among patients with SLD, 260 (89.3%) met the MASLD criteria. Moreover, 9 (3.5%) met the MetALD and 4 (1.5%) met the ALD criteria in patients with MASLD. Among patients with SLD, the prevalence of CSF did not differ significantly according to whether they met MASLD criteria (9.6% VS. 9.7%, p = 0.991).
The association between MASLD and CSF evaluated by multivariable logistic regression analysis
Multivariable logistic regression analyses were preformed to detect the potential associations between MASLD and CSF among patients with SLD. The results were shown in Table 3. No significant difference in the weighted odds of CSF was observed in patients with MASLD when compared with patients having SLD but without MASLD (OR = 1.07, 95% CI = 0.30–3.83, p = 0.9180) after multivariable logistic regression analysis adjusting for age, sex and race/ethnicity.
Discussion
To our knowledge, this is the first study to estimate the prevalence of SLD, MASLD, MetALD, ALD, and CSF in adolescents in the general US population, as well as to explore whether MASLD was associated with higher prevalence of CSF in US adolescents with SLD. This study has some new finding as follows. First, the prevalence of SLD among the paediatric population in US is alarmingly high, affecting approximately one in five adolescents. Moreover, nearly one in twenty of adolescents in the general US population exhibited evidence of CSF. Second, the majority (89.3%) of adolescents with SLD as defined by transient elastography met the criteria for MASLD, with overweight or obesity being the most commonly met criterion among the five CMRFs at a rate of 95.8%. The application of the new SLD category definition provided a more comprehensive insight into the prevalence of SLD categories among US adolescents, with MASLD being the most prevalent (89.3%), followed by MetALD (3.1%), (ALD) (1.7%), and other SLDs. Third, only 12.7% of adolescents with MASLD had elevated ALT levels in accordance with the NASPGHAN guidelines. Fourth, the prevalence of CSF did not differ significantly between adolescents with MASLD and those who without. Furthermore, the risk of CSF in patients with MASLD did not show a significant difference when compared to patients without MASLD after controlling for age, sex, and race/ethnicity.
Due to limited data on the prevalence of the new proposed MASLD in adolescents, we compared our results with previously reported data on adolescents with MAFLD. A recent cross-sectional study by Ciardullo et al. examined 1,446 adolescents from the NHANES 2017–2020, the same study participants as in our current study, which found a prevalence of MAFLD of 22.7%9. Our study revealed a prevalence of MASLD of 17.9% in adolescents from the general population, did not differ significantly with the prevalence of MAFLD. A high degree of concordance was observed between MASLD and the previously proposed MAFLD definition in adolescents, with no significant impact on disease prevalence following the transition from MAFLD to MASLD diagnostic criteria.
This study presents the estimated prevalence of MetALD and ALD among US adolescents for the first time. MetALD accounted for 0.6% and ALD for 0.3% in the total 1,446 participants, while MetALD accounted for 3.1% and ALD for 1.7% of patients with SLD. In comparison, a recent cross-sectional study utilizing data from 3,173 adult participants in the 2017–2020 NHANES cycles reported that 7.7% of patients with SLD (CAP ≥ 274dB/m) were classified as MetALD, and 0.4% as ALD. Our findings indicate a lower prevalence of MetALD and a higher prevalence of ALD in adolescents when compared to the adult population in the aforementioned study. It is important to acknowledge that the limited number of participants enrolled in this study may have contributed to the lack of national representativeness, with only 291 patients diagnosed with SLD. This may partially account for the higher prevalence of ALD observed in our study. Another cross-sectional study conducted by Markos et al. utilized data from adult participants in the NHANES 2017–2020 and reported a prevalence of 3.61% (95% CI: 2.89 − 4.52%) for MetALD and 1.41% (95% CI: 0.93 − 2.14%) for ALD in the general US population when using CAP ≥ 263dB/m (consistent with the threshold in our study) for the diagnosis of SLD18. Our results indicated a significantly lower prevalence of MetALD and ALD in adolescents compared to the aforementioned adult counterparts. This aligns with previous research suggesting that alcohol consumption, especially excessive alcohol use, in not common among adolescents, as reported previously19.
Many blood-based non-invasive indicators have shown limited effectiveness in identifying CSF in adolescents, therefore we adopted VCTE data. The study found that 4% of the total participants, 9.6% of adolescents with SLD and 9.6% of adolescents with MASLD had the elastographic evidence of CSF defined by LSM ≥ 8.0 kPa. Our results are consistent with a recent cross-sectional study by ciardullo et al., which included 867 adolescents aged 12–18 years from NHANES 2017–2018 and reported that 4.4% (95% CI 2.51–6.33) had significant fibrosis, defined by LSM ≥ 7.4 kPa. A similar population study conducted by Abeysekera et al. in the United Kingdom, which included 3600 young adults with a mean age of 24 years, reported a prevalence of 2.7% in participants with CSF accessed by LSM ≥ 7.9 kPa20, consistent with our findings. It is important to note that subjects enrolled in the study were young adults, with a mean age difference of 9 years compared to the adolescents in our study with a mean age of 15 years. Additionally, there were notable differences in the distribution of race/ethnicity between the two studies. It is concerning that adolescents with CSF are at high risk of liver-related event in the future.
Whether adolescents with MASLD were at higher risk of progression towards more advanced stages, such as steatohepatitis and liver fibrosis, represents a significant research question. Screening for steatohepatitis in adolescents with SLD presents a challenging task, as there is currently no widely accepted noninvasive tool for its detection. Additionally, relying solely on elevated ALT levels is problematic, as a minority of adolescents with liver steatosis exhibit elevated ALT levels9,21. Our results are in accordance with these findings, showing that 13.5% of adolescents with SLD and 12.7% of adolescents with MASLD had elevated ALT levels. Research has consistently demonstrated that liver fibrosis, rather than steatohepatitis or elevated ALT levels, serves as the primary predictor of future liver-related adverse events and the long-term overall mortality in adult patients with NAFLD22,23. As such, one of the aims of this study is to assess MASLD was associated with higher prevalence of CSF in adolescents with SLD. Our analysis revealed that odds of CSF did not significantly differ based on whether adolescents met MASLD criteria. It is worth noting that a recent cross-sectional study by ciardullo et al. on the same study population with our current study revealed that the prevalence of CSF (LSM ≥ 7.4 kPa) did not show a statistically significant difference based on whether they met MAFLD criteria (9.7% vs. 15.2%, p= 0.276) with elastograhic evidence of steatosis (CAP ≥ 248dB/m). Furthermore, the odds of CSF did not differ significantly between the MAFLD (+) and MAFLD (-) group after adjusting for the confounding factors such as age, sex and race/ethnicity. Therefore, similar with the MAFLD study9, our study revealed that MASLD paediatric criteria did not improve the detective efficiency of CSF in adolescents with SLD. Future evidence from longitudinal studies is therefore urgently needed to demonstrate whether MASLD has the ability to predict long-term liver-related events.
This study has several limitations. First, a few studies have ever evaluated the accuracy of VCTE to identify steatosis and fibrosis in adolescents, as liver biopsies are not feasible in this population. A recent literature from 2023 in US compared the severity of NAFLD by liver histology, CAP, VCTE, MRI-PDFF, and MR elastography24. The findings concluded that neither VCTE liver stiffness nor CAP correlated well with established imaging modalities and biopsy measures of liver fat or stiffness. This may cause skepticism among pediatricians researching MASLD in the US regarding the reliability of diagnosing SLD using CAP24. This represents a significant limitation. Furthermore, the thresholds for CAP in diagnosing steatosis and LSM in diagnosing CSF are derived from a large landmark study performed in adults25. The results in this study should be interpreted with caution. Second, due to the lack of clear guidelines on alcohol consumption in adolescents, standards were adapted from recommendations for adults. Third, the multivariable logistical regression analyses in this study were adjusted for only three confounding variables due to the limited number of patients with CSF, thus potentially limiting the persuasiveness of the results. Forth, although we have checked and confirmed that none of the 1446 participants has specific etiology SLDs such as autoimmune hepatitis, Wilson’s disease, lysosomal storage diseases with liver involvement, and hepatitis C, we cannot exclude all the possible specific etiologies for SLD with data from NHANES. The study defines SLD as a median CAP ≥ 263 dB/m with elastographic evidence of steatosis, but specific etiology SLD patients may not have undergone CAP assessment. This could result in an overestimation of the proportion of MASLD within the defined SLD. However, we consider that it does not affect the reliability of our results. Future studies with larger sample sizes are necessary to determine if there is a notable disparity in the prevalence of CSF among adolescents with and without MASLD, as well as to assess the effectiveness of MASLD criteria in improving the diagnostic accuracy of CSF in adolescents with SLD.
In conclusion, the prevalence of MASLD and CSF in US adolescents is alarmingly high while the prevalence of MetALD and ALD are relatively low. MASLD was met by most of the US adolescents with SLD. Moreover, MASLD could not differentiate simple steatosis from progressive forms among adolescents with SLD.
Data availability
The data are publicly available at https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx? Cycle=2017-2020.
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Acknowledgements
The authors thank the staff and the participants of the NHANES study for their valuable contributions.
Funding
This study was supported by Zhejiang University and Ningbo First Hospital docking discipline general medicine (zd2020018); the Medical Health Science and Technology Project of Zhejiang Provincial Health Commission (Grant No. 2024KY1530, 2021KY989, & 2019KY579) and the First Batch of Young Technical Backbone Talents Project of Ningbo Municipal Health Commission (Nai-Bin Yang).
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G.Q.Q. and Y.S.Q. designed the study. G.X.S. and N.B.Y. wrote the manuscript. J.G.C., C.M.J. and Z.Z.L. researched and analyzed data. X.Y. reviewed and edited the manuscript. Y.W.X. and S.S.J. participated in data analysis. All authors approved the final version of the manuscript to be published. N.B.Y. is the guarantor of this work.
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Shi, GX., Qian, YS., Jiang, CM. et al. Prevalence of steatotic liver disease (MASLD, MetALD, ALD) and clinically significant fibrosis in US adolescents. Sci Rep 14, 25724 (2024). https://doi.org/10.1038/s41598-024-76922-9
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DOI: https://doi.org/10.1038/s41598-024-76922-9