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Metabolic Risk Factors and Clinical Presentations of Metabolic Dysfunction-associated Steatotic Liver Disease Using Data from the All of Us Research Program

  • Ke-Qin Hu1,* ,
  • Seyedeh Neelufar Payrovnaziri2,
  • Argyrios Ziogas2,
  • Steven Hiek2,
  • Kuangda Shan1,
  • Tevan Luong1,
  • Jenny Fang2 and
  • Hoda Anton-Culver2
 Author information 

Abstract

Background and Aims

Metabolic dysfunction-associated steatotic liver disease (MASLD) affects approximately 32% of the US adult population. The present study aimed to utilize the All of Us electronic health record-linked large cohort to assess seven metabolic risk factors (MRFs) simultaneously, the impact by ethnicity and age, and clinical presentations of MASLD.

Methods

This study included a MASLD group (n = 15,060) and a frequency-matched control group (n = 75,300). Multivariable analyses were performed to compare the frequencies of MRFs and clinical outcomes between the two groups. Type 1 diabetes was not included in the multivariable analysis. Subgroup analyses were conducted according to race and ethnicity, as well as age.

Results

The overall frequency of MASLD was 6.0%. Compared with the control group, individuals with MASLD had significantly higher independent frequencies of obesity (66.1% vs. 41.3%), type 2 diabetes (39.5% vs. 16.9%), hypertension (64.3% vs. 38.6%), hyperlipidemia (59.8% vs. 37.3%), obstructive sleep apnea (28.9% vs. 13.4%), and hypothyroidism (21.2% vs. 13.4%). Obesity was identified as the strongest independent MRF among Asians, Whites, and Hispanics, particularly in individuals younger than 50 years, whereas hypertension was the strongest independent MRF in Blacks. MASLD was also associated with significantly higher frequencies of cardiac events, including coronary artery disease (17.1% vs. 9.4%) and myocardial infarction (7.1% vs. 4.2%); hepatic events, including cirrhosis (7.5% vs. 1.1%) and hepatocellular carcinoma (0.5% vs. 0.1%); and elevated liver enzymes, including alanine aminotransferase (27.7% vs. 10.1%), aspartate aminotransferase (18.0% vs. 6.4%), and alkaline phosphatase (19.8% vs. 13.1%), compared with the control group.

Conclusions

Our study demonstrated that obesity, hypertension, hyperlipidemia, type 2 diabetes, obstructive sleep apnea, and hypothyroidism were independent MRFs for MASLD overall, but the ranking of these MRFs by odds ratios could vary by ethnicity and age. MASLD presents with significantly higher rates of alanine aminotransferase, aspartate aminotransferase, and alkaline phosphatase elevation, as well as cardiac and hepatic events.

Graphical Abstract

Keywords

Metabolic dysfunction-associated steatotic liver disease, MASLD, Metabolic risk factor, MRF, All of Us program, Type 1 diabetes, Type 2 diabetes, Hypertension, Hyperlipidemia, Hypothyroidism, Obesity, Obstructive sleep apnea

Introduction

Metabolic dysfunction-associated steatotic liver disease (MASLD), previously termed non-alcoholic fatty liver disease, has emerged as a significant public health concern, as it is the most common etiology of chronic liver disease, with most current literature estimating the global prevalence to be approximately 32–38% in adult populations.1–7 MASLD can cause cirrhosis, is a rising etiology for hepatocellular carcinoma (HCC), and is now the most common indication for liver transplantation in those > 65 years old, particularly in women.8–11 This alarming trend parallels the global trends of obesity, insulin resistance, dyslipidemia, hypertension (HTN), and cardiovascular disease.12,13

Although most patients with MASLD are asymptomatic, 7–30% of them may develop metabolic dysfunction-associated steatohepatitis (MASH), previously termed nonalcoholic steatohepatitis.14,15 MASH, a more severe form of MASLD, is associated with varying ethnic disparities and carries a higher risk for developing cirrhosis, HCC, cardiac-related mortality, and all-cause mortality.14–19

Despite active clinical trials aimed at addressing this global epidemic, currently there are only two treatments approved by the U.S. Food and Drug Administration, i.e., resmetirom and semaglutide, for MASH.20–22 Early diagnosis and identifying and correcting the metabolic risk factors (MRFs) remain the mainstay in managing MASLD. While studies have explored the association of MRFs with the clinical presentations, natural course, and long-term outcomes of MASLD, many have been limited by study design, often single-center, retrospective, and involving small sample sizes. Although type 2 diabetes mellitus (T2DM), obesity, hyperlipidemia (HLD), and HTN are considered the most common MRFs for MASLD,9,14,15,23,24 the rank or importance of these MRFs in MASLD remains undetermined. Some studies indicate that ethnicity and age may also impact MASLD-related MRFs.25–27 Using the 2017–2018 National Health and Nutrition Examination Survey (NHANES) database, a recent cross-sectional study assessed 2,346 cases with MASLD and found that individuals aged 40–64 and ≥ 65 years, higher body mass index (BMI), diabetes, HTN, and hypertriglyceridemia were independently associated with a higher risk.28 These findings remain to be confirmed by larger cohort studies using different data sources. Additionally, understanding ethnicity-related differences in MRFs will help in developing individualized approaches for the early diagnosis of MASLD. The roles of other MRFs, such as obstructive sleep apnea (OSA),27–29 hypothyroidism (HT),28–30 and type 1 diabetes mellitus (T1DM),29–31 remain unknown or even controversial. To the best of our knowledge, no study has assessed all seven possible MRFs simultaneously in a large cohort. Therefore, additional studies utilizing large, multi-center designs are needed to address these issues.

Likewise, some studies indicated that MASLD is clinically associated with increased cardiac events, such as coronary artery disease (CAD) and myocardial infarction (MI), and hepatic events, such as cirrhosis and HCC.8,10,13,14,23 However, high-quality studies using large cohorts with direct comparisons to control groups remain lacking. It is known that some MASLD patients present with elevated alanine aminotransferase (ALT) and/or aspartate aminotransferase (AST),16,32,33 but the exact rates of such elevations have not been assessed in large cohorts with appropriate comparisons. Additionally, the rates of alkaline phosphatase (ALP) elevation in MASLD patients remain to be determined.

The “All of Us (AoU) Research Program” is sponsored by the National Institute of Health to advance precision diagnosis, prevention, and treatment.34 AoU represents a unique opportunity, as it provides a large cohort of diverse participants34 to address the above issues for MASLD. The present study aimed to utilize the AoU electronic health record (EHR)-linked large cohort to assess MASLD comprehensively in a real-world setting. By comparing the MASLD group with a control group, we investigated crucial aspects of MASLD-related MRFs and the clinical presentation of MASLD that may impact the prevention, early diagnosis, and management of this disease.

Methods

Study population

This work was performed on data from the NIH AoU Research Program, a diverse nationwide cohort of over 800,000 participants. Data were accessed via the AoU Researcher Workbench, the program’s online data repository and research environment. We first created a research cohort consisting of participants whose EHR was linked to the rest of their AoU data. Then we identified participants (cases) with MASLD and from the available non-case participants we randomly selected controls in ratio of 1:5 frequency matched on age, sex, race and ethnicity. Since May 2018, AoU has enrolled participants aged 18 or older from various recruitment sites across the U.S., with a special focus on recruiting individuals from historically underrepresented communities in biomedical research. After a participant consented, their de-identified EHR data were submitted to AoU, and the data were made available to researchers through the program’s Researcher Workbench. In addition to EHR data, health questionnaires, physical measurements, the use of digital health technology, and the collection and analysis of biospecimens were also available. Data standardization in the AoU database was based on the Observational Medical Outcomes Partnership Common Data Model using the Systematized Nomenclature of Medicine Clinical Terms (SNOMED) vocabulary. More related information is available at https://allofus.nih.gov .

Case selection for MASLD and control groups

The initial cohort of AoU with available EHR data consisted of 287,012 participants (AoU Controlled Tier Dataset v7). As shown in Figure 1, 15,390 participants were excluded due to diagnoses of “alcohol abuse”, “nondependent alcohol abuse, continuous”, and “nondependent alcohol abuse in remission” (SNOMED codes: 15167005, 191882002, 191884001) in their EHR history. Among 271,622 eligible participants, MASLD was diagnosed in 15,462 by “steatosis of liver” (SNOMED code: 197321007), and the other 256,160 without a diagnosis of MASLD were considered eligible study controls. We further excluded 19,964 eligible controls whose EHR length was less than six months, resulting in 236,196 eligible controls. Among the 15,462 participants with a diagnosis of MASLD, we further excluded 290 who had an initial diagnosis more than 10 years before their latest available EHR data. We created the race and ethnicity characteristic based on the two separately recorded data columns in the AoU database, following this rule: if a participant reported their ethnicity as Hispanic or Latino, their race and ethnicity were considered Hispanic in our study; otherwise, it was their race (i.e., White, Black or African American [Black], Asian). We created a case-control study of participants with a diagnosis of MASLD (MASLD group) and those without a diagnosis of MASLD (control group). We chose the control group by frequency-matching with a ratio of 1:5 on age (for the MASLD group: age at diagnosis; for the control group: age at the latest available EHR date), assigned sex at birth, and race and ethnicity. Consequently, 112 cases were further excluded because they did not have an exact match on age, sex at birth, and self-reported race and ethnicity among the control group. As a result, our case-control study included 15,060 cases, which we refer to as MASLD group, and 75,300 cases as controls, i.e., the control group. Figure 1 illustrates the inclusion/exclusion criteria for this frequency-matched case-control study.

Overview of the study inclusion/exclusion criteria for the present frequency-matched case-control study.
Fig. 1  Overview of the study inclusion/exclusion criteria for the present frequency-matched case-control study.

EHR, electronic health record; MASLD, Metabolic dysfunction-associated steatotic liver disease.

Characteristics of interest

The characteristics of interest in this study were age (i.e., age at initial diagnosis of MASLD for cases and age at the latest EHR data available for the controls), assigned sex at birth (i.e., female, male, other/unknown), self-reported race and ethnicity (i.e., White, Black, Hispanic or Latino, Asian, and other/unknown), country of birth (i.e., USA vs. non-USA), MRFs (i.e., obesity by average BMI with a threshold of 25 for Asians and a threshold of 30 for non-Asians35–37), T2DM (SNOMED code: 44054006), HLD (SNOMED code: 55822004), HTN (SNOMED code: 38341003), OSA (SNOMED code: 78275009), HT (SNOMED code: 40930008), T1DM (SNOMED code: 46635009), cardiac events [i.e., CAD (SNOMED code: 53741008) and MI (SNOMED code: 22298006)], and hepatic events [i.e., cirrhosis (SNOMED code: 19943007) and HCC (SNOMED code: 109841003)]. Additionally, liver injury-related laboratory data, including ALT, AST, and ALP, were also available and collected in a small portion (as detailed in the RESULTS section) in both groups. All the above-mentioned variables were considered if their diagnosis occurred before, at the same time, or up to a maximum of three months after the diagnosis of MASLD. For BMI, due to data availability, we used the average value of data points in the participants’ EHR data.

Statistical analysis

Comparisons of characteristics of interest between MASLD and control groups were performed using Fisher’s exact test or the contingency χ2 test. We performed multivariable logistic regression analysis with the dependent binary variable of presence or absence of MASLD diagnosis. All seven models were adjusted for the characteristics on which the MASLD and control groups were matched, including age, assigned sex at birth, race and ethnicity, and length of EHR. For each multivariable model, in addition to age, race and ethnicity, assigned sex at birth, and length of EHR, we included obesity, T2DM, HTN, HLD, OSA, and HT. Considering the variability observed in the results, we created additional multivariable logistic regression models on subgroups based on race and ethnicity (i.e., White, Black or African American, Hispanic or Latino, and Asian), age (< 50 vs. ≥ 50 years), and the combination of both. This study was implemented in the AoU Researcher Workbench Cloud environment using Python. All p-values associated with reported results in this analysis were considered statistically significant at p-value < 0.001 unless otherwise noted.

Results

Race- and ethnicity- and age-related distribution of MASLD in our study

As shown in Table 1, out of the 251,256 total eligible participants, 6.0% (n = 15,060) met the diagnostic criteria for MASLD. Within the MASLD group, the mean age was 54.3 ± 14.1 [median (IQR), 56 (44–65)], the male-to-female ratio was 1.95:1 (33.3% and 65.0%, respectively), and the race- and ethnicity distribution was 54.9%, 26.0%, 10.8%, and 2.5% for White, Hispanic, Black, and Asian participants, respectively. In addition, among the MASLD group, the distribution of age was as follows: age > 65 (26.3%), 50–59 (25.4%), 60–64 (13.4%), 40–49 (17.2%), and < 40 (17.7%) subgroups.

Table 1

Baseline demographics in MASLD and frequency-matched control groups

CharacteristicMASLD cases (n = 15,060)Frequency-matched controls (n = 75,300)
Age
  Mean (STDEV)54.3 (±14.1)54.3 (±14.1)
  Median (IQR)56 (44–65)56 (44–65)
Age categoriesn%n%
  <402,65917.7%13,29517.7%
  40–492,58517.2%12,92517.2%
  50–593,83225.4%19,16025.4%
  60–642,02013.4%10,10013.4%
  65+3,96426.3%19,82026.3%
Sex at birth
  Female9,78565.0%48,92565.0%
  Male5,01733.3%25,08533.3%
  Other/Unknown2581.7%1,2901.7%
Self-reported race-ethnicity
  White8,26554.9%41,32554.9%
  Hispanic or Latino3,91126.0%19,55526.0%
  Black or African American1,62310.8%8,11510.8%
  Asian3772.5%1,8852.5%
  Other/Unknown8845.9%4,4205.9%
Country born
  USA11,90979.1%59,21078.6%
  Not USA2,88319.1%14,74419.6%
  Unknown2681.8%1,3451.8%

Comparison of overall MRFs in MASLD vs. control group

As shown in Table 2 and Figure 2, we compared the differences in frequencies of the four most common or major MRFs (i.e., obesity, T2DM, HLD, and HTN) and three less-studied or minor MRFs (i.e., OSA, HT, and T1DM) in the MASLD vs. control group. Among the four major MRFs, obesity showed the highest frequency (66.1% vs. 41.3%) in the MASLD vs. control group. This included BMI ≥ 25 for Asians (71.1% vs. 43.2%) and BMI ≥ 30 for non-Asians (65.9% vs. 41.2%). The next most frequent major MRF was HTN (64.3% vs. 38.6%), followed by HLD (59.8% vs. 37.3%) and T2DM (39.5% vs. 16.9%) in the MASLD vs. control group. Among the three minor MRFs, OSA (28.9% vs. 13.4%) represented the highest frequency, followed by HT (21.2% vs. 13.4%) and T1DM (4.3% vs. 1.9%) in MASLD vs. control group. All p-values were < 0.0001.

Table 2

Comparison of metabolic risk factors, cardiac and hepatic events in MASLD and control groups

Types of variablesVariablesCases (n = 15,060)
Frequency-matched controls (n = 75,300)
p-value
n%n%
Metabolic risk factorsObesity9,94966.1%31,09141.3%<0.0001
  Asian26871.1%81543.2%<0.0001
  Non-Asian9,68165.9%30,27641.2%<0.0001
Type 2 diabetes5,95139.5%12,73216.9%<0.0001
Hyperlipidemia9,00759.8%28,10737.3%<0.0001
Hypertension9,68264.3%29,07438.6%<0.0001
Obstructive sleep apnea4,34628.9%10,05913.4%<0.0001
Hypothyroidism3,19321.2%10,10513.4%<0.0001
Type 1 diabetes6514.3%1,4061.9%<0.0001
Cardiac and hepatic eventsCoronary artery disease (CAD)2,57017.1%7,0669.4%<0.0001
Myocardial infarction1,0737.1%3,1384.2%<0.0001
Cirrhosis1,1267.5%7991.1%<0.0001
Hepatocellular Carcinoma810.5%900.1%<0.0001
Univariable analysis of overall frequencies of seven MRFs in cases vs. controls.
Fig. 2  Univariable analysis of overall frequencies of seven MRFs in cases vs. controls.

MRFs, metabolic risk factors; HTN, hypertension; HLD, hyperlipidemia; T2DM, type 2 diabetes mellitus; OSA, obstructive sleep apnea; HT, hypothyroidism; T1DM, type 1 diabetes mellitus.

We then further assessed whether these MRFs were independently associated with the diagnosis of MASLD. T1DM was excluded from the analysis because of its smaller sample size. As shown in Table 3 and Figure 3A, A, multivariable logistic regression analysis showed that obesity, T2DM, HTN, HLD, OSA, and HT were all independently and significantly associated with MASLD. For MASLD overall, the odds ratios (ORs) were as follows: obesity (OR = 2.2) was the strongest independent MRF, followed by T2DM (OR = 1.8), HTN (OR = 1.7), HLD (OR = 1.6), OSA (OR = 1.4), and HT (OR = 1.3). Table 3 summarizes ORs in different categories of analysis. All p-values were < 0.0001.

Table 3

Odds ratios (ORs) for various MRFs in the full MASLD group, and age- and race-ethnicity subgroups

VariablesAll<50≥50WhiteHispanicBlackAsian<50-year-old
≥ 50-year-old
WhiteHispanicBlackAsianWhiteHispanicBlackAsian
Obesity2.2a3.2a1.9a2.4a2.1a1.6a2.8a4.0a2.7a2.1a5.3a2.1a1.7a1.5b1.8c
T2DM1.8a2.0a1.8a1.9a1.6a1.9a1.7a2.4a1.8a2.1a2.1c1.9a1.5b1.9a1.5c
HTN1.7a1.6a1.7a1.9a1.4b2.0a1.7a1.6a1.4b2.0a1.7c1.9a1.4b1.8a1.5c
HLD1.6a1.7a1.4b1.6a1.6a1.6a2.3a1.5a1.8a1.7a2.3a1.5b1.4b1.5b2.0a
OSA1.4b1.6a1.4b1.3b1.4b1.8a1.2d1.6a1.4b1.8a0.9d1.3b1.4b1.7a1.5d
HT1.3b1.4b1.2b1.2b1.5b1.3c0.9d1.3b1.8a1.7c1.3d1.2b1.3b1.1c0.6d
Multivariable analysis of overall and race- and ethnicity-related frequencies of MRFs.
Fig. 3  Multivariable analysis of overall and race- and ethnicity-related frequencies of MRFs.

Comparison of OR distribution for variable MRFs overall (A) and in various race- and ethnicity-related MASLD subgroups (B–E). (B and C). Multivariable analysis of age-related frequencies of MRFs in overall and various age-related MASLD subgroups. Comparison of OR distribution for variable MRFs in participants aged <50 years (A1–E1) vs. ≥50 years (A2–E2) overall (A1 vs. A2) and in various ethnicity-related MASLD subgroups (B1–E1 vs. B2–E2). MRFs, metabolic risk factors; HTN, hypertension; HLD, hyperlipidemia; T2DM, type 2 diabetes mellitus; OSA, obstructive sleep apnea; HT, hypothyroidism.

Comparison of self-reported race- and ethnicity- and age-related MRFs distribution in MASLD vs. control group

Self-reported race- and ethnicity-related MRFs

Table 3 and Figures 3A, B–E summarize the ORs and 95% confidence intervals (CIs) of these six MRFs in different self-reported race and ethnicity subgroups. Obesity showed the strongest association with MASLD in Asian, White, and Hispanic subgroups (ORs: 2.8, 2.4, 2.1), whereas HTN showed the strongest association with MASLD in the Black subgroup (OR: 2.0). Additionally, the rank of ORs for these MRFs varied across race and ethnicity subgroups, as shown in Table 3. For instance, OSA was the third MRF in the Black subgroup but was less common MRF in the other subgroups.

Age-related MRFs

Table 3 and Figure 3B, A1 and Figure 3C, A2 summarizes the ORs and 95% CIs of these six MRFs in participants younger than 50 years old (Figure 3B, A1) and in those aged 50 years or older (Figure 3C, A2), respectively. Although obesity and T2DM showed the strongest association with MASLD in both subgroups, the ORs were higher in the younger age subgroup (ORs in younger participants: 3.2 and 2.0; ORs in older participants: 1.9 and 1.8, respectively).

Age- and self-reported race- and ethnicity-related MRFs

Table 3 and Figures 3B, B1–E1 and Figures 3C, B2–E2 summarizes the ORs and 95% CIs of these six MRFs in participants younger than 50 years old (Figures 3B, B1–E1) and in those aged 50 years or older (Figures 3C, B2–E2), stratified by self-reported race and ethnicity. In younger participants, across all self-reported race and ethnicity subgroups, obesity showed the strongest association with MASLD (ORs: Asian 5.3, White 4.0, Hispanic 2.7, Black 2.1). However, in older participants, HLD (OR = 2.0) in the Asian subgroup and T2DM (OR = 1.9) in the Black subgroup showed the strongest association with MASLD.

MASLD clinical presentation

We then assessed MASLD clinical presentation by the frequencies of cardiac and hepatic events and liver enzyme elevations. As shown in Table 2 and Figure 4A, compared to the control group, the MASLD group had significantly higher frequencies of CAD (17.1% vs. 9.4%) and MI (7.1% vs. 4.2%). As shown in Figure 4B, the frequencies of both cirrhosis (7.5% vs. 1.1%) and HCC (0.5% vs. 0.1%) were significantly higher in the MASLD group than in the control group. All p-values were <0.001.

Clinical presentation of MASLD.
Fig. 4  Clinical presentation of MASLD.

Comparison of the frequencies for: (A) CAD and MI; (B) Cirrhosis and HCC; (C) ALT, AST, and ALP elevations in MASLD vs. control group. MASLD, Metabolic Dysfunction-Associated Steatotic Liver Disease; CAD, Coronary Artery Disease; M, Myocardial Infarction; HCC, Hepatocellular Carcinoma; ALT, Alanine Aminotransferase; AST, Aspartate Aminotransferase; ALP, Alkaline Phosphatase

In our data, 1,017 participants in the MASLD group and 989 participants in the control group also had laboratory data available. Using these data, we compared the frequencies of ALT (≥ 40 U/L), AST (≥ 40 U/L), and ALP (≥ 110 U/L) elevations in both groups. As shown in Figure 4C, the MASLD group had not only significantly higher rates of ALT (27.7% vs. 10.1%) but also AST (18.0% vs. 6.4%) and ALP (19.8% vs. 13.1%) elevations compared to the control group. All p-values were < 0.001.

Discussion

MASLD has emerged as a significant public health concern, with estimated global prevalence of approximately 32%–38% in adult populations.1–7 In the present study, we used the large cross-sectional AoU dataset, identified 15,060 participants with MASLD, and assessed its association with all seven reported MRFs simultaneously by comparing them with a matched control group containing 75,300 participants, creating a large and thorough case-control study. In a previous study that included a large primary care cohort of 17,669,973 subjects, the frequency of MASLD was 1.9%.38 In our cohort, the rate of MASLD was 6.0%, and the distribution by race and ethnicity showed that the frequency of MASLD was higher among Hispanics (7.8%), followed by Whites (5.8%), Asians (5.0%), and Blacks (3.1%). Such differences may be derived from participant selection. AoU data are collected from multicenter, nationwide, highly diversified sites and may be more representative of the general population. Previous studies indicated that prevalence could be age-related. For instance, Cheng et al. reported the highest prevalence at 34.6% in the 50–59 age group, followed by 33.1% in the 20–49 age group.26 Based on the AoU data, the highest frequency was in participants aged > 65 (26.3%) and 50–59 years (25.4%), followed by < 40 (17.7%), 40–49 (17.2%), and 60–64 (13.4%) subgroups. Our results reconfirmed the findings by Díaz et al., showing a higher frequency of MASLD in individuals aged ≥ 65 years using the NHANES database.28

Huang et al. reported that based on the third NHANES, the Hispanic population had a higher prevalence of MASLD at 37.0%, followed by Whites at 29.3%, whereas the non-Hispanic Black population had a lower prevalence at 24.7%.39 Using the same NHANES database, Díaz et al. also reported that the Hispanic group carried the highest prevalence of MASLD, i.e., 47.0%.28 In population-based studies performed in the U.S., the prevalence of MASLD was higher in Hispanics (22.9%), followed by Whites (14.4%) and Blacks (13.0%).40 In our cohort, the distribution of race and ethnicity among the MASLD group was 54.9%, 26.0%, 10.8%, and 2.5% for Whites, Hispanics, Blacks, and Asians, respectively, consistent with the previous reports.28,39,40

Previous studies have shown that the primary MRFs for MASLD include obesity, T2DM, HLD, and HTN, with obesity and T2DM found to be the most significant MRFs.9,14,15,22,23,28 Indeed, around 90% of individuals with MASLD have at least one MRF. Based on our large and diversified dataset, we reconfirmed that the frequencies of these four major MRFs were independently and significantly associated with MASLD in our MASLD group. Although the criteria may not be identical, our results confirmed Díaz et al.’s findings that overweight/obesity is the most common MRF for MASLD.28

Although OSA and HT have been reported as other MRFs for MASLD,29,30 such associations remain controversial. In the present study, we assessed OSA, HT, and T1DM in parallel with the four major MRFs, representing the first study to assess all seven MRFs simultaneously. Multivariable analysis confirmed that OSA and HT were independently and significantly associated with MASLD, although their ORs were lower than those of the four major MRFs. Thus, both OSA and HT should be considered as additional MRFs for MASLD. The frequency of T1DM in MASLD patients is almost unknown; one previous study with a very small sample size reported that 4.7% (6/128) of individuals with T1DM had MASLD.31 The present study demonstrated that the frequency of T1DM was low (4.3%) in the MASLD group, making it a relatively less common, but significant MRF for MASLD.

Studies have indicated different distributions of MRFs by ethnicity and age.25–27 However, no study had used a large and diversified dataset to address these issues. In this study, we stratified our data by self-reported race and ethnicity and found that the distribution of the six MRFs (excluding T1DM) varied among subgroups. For instance, obesity was the most common MRF in Asian, White, and Hispanic MASLD subgroups. Previous studies have reported a lower incidence of MASLD in Black populations, with cardiometabolic factors, such as HLD and HTN playing a more prominent role in hepatic steatosis.32 Consistent with this, our findings showed that the MRFs for MASLD in the Black subgroup differed significantly from those in other ethnic groups, with HTN being the strongest independent MRF. Consistent with prior reports,41,42 using the AoU dataset, we demonstrated that both OSA and HT were weaker or minor MRFs for MASLD in general and across all race and ethnicity subgroups, except that OSA was the third most common MRF for MASLD in the Black subgroup.

We further conducted age-stratified analyses of MRF distributions and found that among participants younger than 50 years, obesity was the strongest MRF for MASLD, followed by T2DM, HLD, OSA, HTN, and HT. However, in participants aged 50 years or older, the ORs for these MRFs were in the order of obesity, T2DM, HTN, HLD, OSA, and HT. Thus, compared with HLD, HTN had a stronger association with MASLD in older participants. Additionally, the strength of all these MRFs in association with MASLD, as measured by ORs, was generally weaker in the older age group compared with the younger group.

The variability in MRFs across race, ethnicity, and age subgroups may indicate the potential pathogenic roles of genetic susceptibility and other environmental factors. Prior studies have documented racial differences in key genetic polymorphisms associated with hepatic fat storage, such as PNPLA3, which occurs at higher frequency in Hispanics and Asians, especially those of Southeast Asian descent.43,44 Clinically, understanding these ethnicity- and age-related variations in MRF distribution for MASLD will help not only in age- and ethnicity-focused early diagnosis, but also in understanding MASLD-related pathogenesis and, likely, future individualized management.

Studies have reported increased cardiac and hepatic events in MASLD patients.8,10,13,14,23 Using the AoU dataset, we demonstrated that the frequencies of CAD and MI were significantly higher in the MASLD group than in the control group. Additionally, the frequencies of cirrhosis and HCC were also significantly higher in the MASLD group. These findings, derived from the large AoU dataset, reconfirmed previous studies showing the association of MASLD with the development of cardiac and hepatic comorbidities.8,10,14–16 Thus, assessing cardiac and hepatic comorbidities should be an essential part of MASLD management.

The most common abnormal laboratory test results in MASLD are elevated ALT and AST, although ALP may also be elevated.14,32,33 In our MASLD group with available data on ALT and AST, the frequencies of ALT and AST elevations were significantly higher than those in the control group. The relatively low frequencies of ALT/AST elevation in our MASLD group support the recommendation that the normal values of ALT/AST for MASLD should be lower than the current cutoff values of most laboratory references,45 and normal ALT/AST values by current laboratory references cannot rule out MASLD. Furthermore, in the MASLD group, the frequency of ALP elevation was slightly higher than that of AST elevation and was also significantly higher than in the control group. Thus, MASLD should be considered in individuals with ALP elevation after other possible causes are ruled out.

It should be noted that the present study has several limitations. First, the diagnosis of MASLD was based on EHR and ICD codes, which cannot fully rule out other coexisting liver diseases, such as viral hepatitis B and C, autoimmune hepatitis, and primary biliary cholangitis. Second, using alcohol-related codes alone may not exclude all patients with alcohol misuse. We also recognize that this study may have selection bias, as participants were selected based on the availability of existing records, which may not represent the general population. To mitigate potential recruitment variability in the AoU Research Program, we designed and performed a frequency-matched case-control study. Additionally, data accuracy depends on the quality of existing records entered by individual providers and ancillary medical staff into the EHR, so the data may be incomplete. We acknowledge that the reported results pertaining to ALT, AST, and ALP elevation are limited due to incomplete laboratory recordings in AoU.

Conclusions

The present study provides a unique opportunity to assess a large cohort of MASLD with diversified participants, and our results expand knowledge on the association of MASLD with the seven MRFs and the clinical presentation of MASLD.

Declarations

Acknowledgement

We gratefully acknowledge AoU participants for their contributions, without whom this research would not have been possible. We also thank the National Institutes of Health’s AoU Research Program for making the participant data examined in this study available. Part of this research effort was funded by the AoU Research Program Southern California Consortium 1OT2OD036428-01. Data analysis for the research reported in this publication was supported by the UC Irvine Genetic Epidemiology Research Institute. We also appreciate Mr. Yash Makarand Deole, Department of Statistics, Donald Bren School of Information and Computer Sciences, University of California, Irvine, for his great support in data analysis and interpretation.

Ethical statement

This study used data from the National Institutes of Health (NIH) All of Us Research Program, a nationwide research cohort designed to advance precision medicine. All participants in the All of Us Research Program provided written informed consent for participation and for the use of their data for research purposes. The data used in this study were accessed through the All of Us Researcher Workbench in accordance with program policies and data use agreements. This study involved analysis of de-identified data and did not involve direct contact with participants. In accordance with federal regulations and institutional policy, the study was determined to be exempt from human subjects research oversight or not human subjects research, as applicable, by the investigators’ Institutional Review Board (IRB). The study was conducted in accordance with the Declaration of Helsinki (as revised in 2024).

Data sharing statement

Individual-level data cannot be provided as per AoU’s data dissemination policy. The code used for analyses is available at the workbench environment of the All of Us research program.

Funding

The All of Us Research Program is supported by the National Institutes of Health, Office of the Director: Regional Medical Centers: 1 OT2 OD026549; 1 OT2 OD026554; 1 OT2 OD026557; 1 OT2 OD026556; 1 OT2 OD026550; 1 OT2 OD 026552; 1 OT2 OD026553; 1 OT2 OD026548; 1 OT2 OD026551; 1 OT2 OD026555; IAA #: AOD 16037; Federally Qualified Health Centers: HHSN 263201600085U; Data and Research Center: 5 U2C OD023196; Biobank: 1 U24 OD023121; The Participant Center: U24 OD023176; Participant Technology Systems Center: 1 U24 OD023163; Communications and Engagement: 3 OT2 OD023205; 3 OT2 OD023206; and Community Partners: 1 OT2 OD025277; 3 OT2 OD025315; 1 OT2 OD025337; 1 OT2 OD025276. In addition, the All of Us Research Program would not be possible without the partnership of its participants.

Conflict of interest

KQH is on the Madrigal Pharmaceuticals speaker bureau. The other authors have no conflict of interests related to this publication.

Authors’ contributions

Study initiation (KQH, HAC), study design (KQH), study coordination (KQH, SH, JF, HAC), data collection (KQH, SNP, AZ, SH, JF), data analysis (KQH, SNP, AZ), data interpretation (KQH, SNP, AZ, HAC), and manuscript preparation (KQH, SNP, AZ, KS, TL, HAC). All authors have approved the final version and publication of the manuscript.

References

  1. Rinella ME, Lazarus JV, Ratziu V, Francque SM, Sanyal AJ, Kanwal F, et al. A multisociety Delphi consensus statement on new fatty liver disease nomenclature. Hepatology 2023;78(6):1966-1986 View Article PubMed/NCBI
  2. Hagström H, Vessby J, Ekstedt M, Shang Y. 99% of patients with NAFLD meet MASLD criteria and natural history is therefore identical. J Hepatol 2024;80(2):e76-e77 View Article PubMed/NCBI
  3. Wong VW, Ekstedt M, Wong GL, Hagström H. Changing epidemiology, global trends and implications for outcomes of NAFLD. J Hepatol 2023;79(3):842-852 View Article PubMed/NCBI
  4. Dong X, Li JM, Lu XL, Lin XY, Hong MZ, Weng S, et al. Global burden of adult non-alcoholic fatty liver disease (NAFLD) and non-alcoholic steatohepatitis (NASH) has been steadily increasing over the past decades and is expected to persist in the future. Transl Gastroenterol Hepatol 2024;9:33 View Article PubMed/NCBI
  5. Henry L, Paik J, Younossi ZM. Review article: the epidemiologic burden of non-alcoholic fatty liver disease across the world. Aliment Pharmacol Ther 2022;56(6):942-956 View Article PubMed/NCBI
  6. Teng ML, Ng CH, Huang DQ, Chan KE, Tan DJ, Lim WH, et al. Global incidence and prevalence of nonalcoholic fatty liver disease. Clin Mol Hepatol 2023;29(Suppl):S32-S42 View Article PubMed/NCBI
  7. Hsu CL, Loomba R. From NAFLD to MASLD: implications of the new nomenclature for preclinical and clinical research. Nat Metab 2024;6(4):600-602 View Article PubMed/NCBI
  8. Myers S, Neyroud-Caspar I, Spahr L, Gkouvatsos K, Fournier E, Giostra E, et al. NAFLD and MAFLD as emerging causes of HCC: A populational study. JHEP Rep 2021;3(2):100231 View Article PubMed/NCBI
  9. Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol 2015;62(1 Suppl):S47-S64 View Article PubMed/NCBI
  10. Targher G, Byrne CD, Tilg H. MASLD: a systemic metabolic disorder with cardiovascular and malignant complications. Gut 2024;73(4):691-702 View Article PubMed/NCBI
  11. Younossi ZM, Stepanova M, Ong J, Trimble G, AlQahtani S, Younossi I, et al. Nonalcoholic Steatohepatitis Is the Most Rapidly Increasing Indication for Liver Transplantation in the United States. Clin Gastroenterol Hepatol 2021;19(3):580-589.e5 View Article PubMed/NCBI
  12. Inoue Y, Qin B, Poti J, Sokol R, Gordon-Larsen P. Epidemiology of Obesity in Adults: Latest Trends. Curr Obes Rep 2018;7(4):276-288 View Article PubMed/NCBI
  13. Muzurović E, Peng CC, Belanger MJ, Sanoudou D, Mikhailidis DP, Mantzoros CS. Nonalcoholic Fatty Liver Disease and Cardiovascular Disease: a Review of Shared Cardiometabolic Risk Factors. Hypertension 2022;79(7):1319-1326 View Article PubMed/NCBI
  14. Rinella ME, Neuschwander-Tetri BA, Siddiqui MS, Abdelmalek MF, Caldwell S, Barb D, et al. AASLD Practice Guidance on the clinical assessment and management of nonalcoholic fatty liver disease. Hepatology 2023;77(5):1797-1835 View Article PubMed/NCBI
  15. Cotter TG, Rinella M. Nonalcoholic Fatty Liver Disease 2020: The State of the Disease. Gastroenterology 2020;158(7):1851-1864 View Article PubMed/NCBI
  16. Sharpton S, Shan K, Bettencourt R, Lee M, McCormick JB, Fisher-Hoch SP, et al. Prevalence and factors associated with liver fibrosis among first-degree relatives of Mexican Americans with hepatocellular carcinoma. Aliment Pharmacol Ther 2023;57(4):378-386 View Article PubMed/NCBI
  17. Deng Q, Zhang Y, Guan X, Wang C, Guo H. Association of healthy lifestyles with risk of all-cause and cause-specific mortality among individuals with metabolic dysfunction-associated steatotic liver disease: results from the DFTJ cohort. Ann Med 2024;56(1):2398724 View Article PubMed/NCBI
  18. Loomba R, Friedman SL, Shulman GI. Mechanisms and disease consequences of nonalcoholic fatty liver disease. Cell 2021;184(10):2537-2564 View Article PubMed/NCBI
  19. Duell PB, Welty FK, Miller M, Chait A, Hammond G, Ahmad Z, et al. Nonalcoholic Fatty Liver Disease and Cardiovascular Risk: A Scientific Statement From the American Heart Association. Arterioscler Thromb Vasc Biol 2022;42(6):e168-e185 View Article PubMed/NCBI
  20. Harrison SA, Bedossa P, Guy CD, Schattenberg JM, Loomba R, Taub R, et al. A Phase 3, Randomized, Controlled Trial of Resmetirom in NASH with Liver Fibrosis. N Engl J Med 2024;390(6):497-509 View Article PubMed/NCBI
  21. Kokkorakis M, Boutari C, Hill MA, Kotsis V, Loomba R, Sanyal AJ, et al. Resmetirom, the first approved drug for the management of metabolic dysfunction-associated steatohepatitis: Trials, opportunities, and challenges. Metabolism 2024;154:155835 View Article PubMed/NCBI
  22. Sanyal AJ, Newsome PN, Kliers I, Østergaard LH, Long MT, Kjær MS, et al. Phase 3 Trial of Semaglutide in Metabolic Dysfunction-Associated Steatohepatitis. N Engl J Med 2025;392(21):2089-2099 View Article PubMed/NCBI
  23. Streba LA, Vere CC, Rogoveanu I, Streba CT. Nonalcoholic fatty liver disease, metabolic risk factors, and hepatocellular carcinoma: an open question. World J Gastroenterol 2015;21(14):4103-4110 View Article PubMed/NCBI
  24. Akter S. Non-alcoholic Fatty Liver Disease and Steatohepatitis: Risk Factors and Pathophysiology. Middle East J Dig Dis 2022;14(2):167-181 View Article PubMed/NCBI
  25. Bertolotti M, Lonardo A, Mussi C, Baldelli E, Pellegrini E, Ballestri S, et al. Nonalcoholic fatty liver disease and aging: epidemiology to management. World J Gastroenterol 2014;20(39):14185-14204 View Article PubMed/NCBI
  26. Cheng HY, Wang HY, Chang WH. Nonalcoholic fatty liver disease: prevalence, influence on age and sex, and relationship with metabolic syndrome and insulin resistance. Int J Gerontolo 2013;4:194-198 View Article
  27. Riazi K, Swain MG, Congly SE, Kaplan GG, Shaheen AA. Race and Ethnicity in Non-Alcoholic Fatty Liver Disease (NAFLD): A Narrative Review. Nutrients 2022;14(21):4556 View Article PubMed/NCBI
  28. Díaz LA, Lazarus JV, Fuentes-López E, Idalsoaga F, Ayares G, Desaleng H, et al. Disparities in steatosis prevalence in the United States by Race or Ethnicity according to the 2023 criteria. Commun Med (Lond) 2024;4(1):219 View Article PubMed/NCBI
  29. Mesarwi OA, Loomba R, Malhotra A. Obstructive Sleep Apnea, Hypoxia, and Nonalcoholic Fatty Liver Disease. Am J Respir Crit Care Med 2019;199(7):830-841 View Article PubMed/NCBI
  30. Bikeyeva V, Abdullah A, Radivojevic A, Abu Jad AA, Ravanavena A, Ravindra C, et al. Nonalcoholic Fatty Liver Disease and Hypothyroidism: What You Need to Know. Cureus 2022;14(8):e28052 View Article PubMed/NCBI
  31. Memaj P, Jornayvaz FR. Non-alcoholic fatty liver disease in type 1 diabetes: Prevalence and pathophysiology. Front Endocrinol (Lausanne) 2022;13:1031633 View Article PubMed/NCBI
  32. Sanyal AJ, American Gastroenterological Association. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology 2002;123(5):1705-1725 View Article PubMed/NCBI
  33. Ekstedt M, Franzén LE, Mathiesen UL, Thorelius L, Holmqvist M, Bodemar G, et al. Long-term follow-up of patients with NAFLD and elevated liver enzymes. Hepatology 2006;44(4):865-873 View Article PubMed/NCBI
  34. Denny JC, Rutter JL, Goldstein DB, Philippakis A, Smoller JW, Jenkins G, et al. The “All of Us” Research Program. N Engl J Med 2019;381(7):668-676 View Article PubMed/NCBI
  35. Long MT, Noureddin M, Lim JK. AGA Clinical Practice Update: Diagnosis and Management of Nonalcoholic Fatty Liver Disease in Lean Individuals: Expert Review. Gastroenterology 2022;163(3):764-774.e1 View Article PubMed/NCBI
  36. Examination Committee of Criteria for ‘Obesity Disease’ in Japan, Japan Society for the Study of Obesity. New criteria for ‘obesity disease’ in Japan. Circ J 2002;66(11):987-992 View Article PubMed/NCBI
  37. Haam JH, Kim BT, Kim EM, Kwon H, Kang JH, Park JH, et al. Diagnosis of Obesity: 2022 Update of Clinical Practice Guidelines for Obesity by the Korean Society for the Study of Obesity. J Obes Metab Syndr 2023;32(2):121-129 View Article PubMed/NCBI
  38. Alexander M, Loomis AK, Fairburn-Beech J, van der Lei J, Duarte-Salles T, Prieto-Alhambra D, et al. Real-world data reveal a diagnostic gap in non-alcoholic fatty liver disease. BMC Med 2018;16(1):130 View Article PubMed/NCBI
  39. Huang Q, Zou X, Wen X, Zhou X, Ji L. NAFLD or MAFLD: Which Has Closer Association With All-Cause and Cause-Specific Mortality?-Results From NHANES III. Front Med (Lausanne) 2021;8:693507 View Article PubMed/NCBI
  40. Rich NE, Oji S, Mufti AR, Browning JD, Parikh ND, Odewole M, et al. Racial and Ethnic Disparities in Nonalcoholic Fatty Liver Disease Prevalence, Severity, and Outcomes in the United States: A Systematic Review and Meta-analysis. Clin Gastroenterol Hepatol 2018;16(2):198-210.e2 View Article PubMed/NCBI
  41. He W, An X, Li L, Shao X, Li Q, Yao Q, et al. Relationship between Hypothyroidism and Non-Alcoholic Fatty Liver Disease: A Systematic Review and Meta-analysis. Front Endocrinol (Lausanne) 2017;8:335 View Article PubMed/NCBI
  42. Aron-Wisnewsky J, Clement K, Pépin JL. Nonalcoholic fatty liver disease and obstructive sleep apnea. Metabolism 2016;65(8):1124-1135 View Article PubMed/NCBI
  43. Meroni M, Longo M, Tria G, Dongiovanni P. Genetics Is of the Essence to Face NAFLD. Biomedicines 2021;9(10):1359 View Article PubMed/NCBI
  44. Wagenknecht LE, Palmer ND, Bowden DW, Rotter JI, Norris JM, Ziegler J, et al. Association of PNPLA3 with non-alcoholic fatty liver disease in a minority cohort: the Insulin Resistance Atherosclerosis Family Study. Liver Int 2011;31(3):412-416 View Article PubMed/NCBI
  45. Kwo PY, Cohen SM, Lim JK. ACG Clinical Guideline: Evaluation of Abnormal Liver Chemistries. Am J Gastroenterol 2017;112(1):18-35 View Article PubMed/NCBI

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Cite this article
Hu KQ, Payrovnaziri SN, Ziogas A, Hiek S, Shan K, Luong T, et al. Metabolic Risk Factors and Clinical Presentations of Metabolic Dysfunction-associated Steatotic Liver Disease Using Data from the All of Us Research Program. J Clin Transl Hepatol. Published online: Jan 27, 2026. doi: 10.14218/JCTH.2025.00393.
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Article History
Received Revised Accepted Published
August 4, 2025 November 30, 2025 December 23, 2025 January 27, 2026
DOI http://dx.doi.org/10.14218/JCTH.2025.00393
  • Journal of Clinical and Translational Hepatology
  • pISSN 2225-0719
  • eISSN 2310-8819
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Metabolic Risk Factors and Clinical Presentations of Metabolic Dysfunction-associated Steatotic Liver Disease Using Data from the All of Us Research Program

Ke-Qin Hu, Seyedeh Neelufar Payrovnaziri, Argyrios Ziogas, Steven Hiek, Kuangda Shan, Tevan Luong, Jenny Fang, Hoda Anton-Culver
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