Low muscle quality index is associated with increased risk of advanced fibrosis in adult patients with nonalcoholic fatty liver disease: NHANES 2011-2014

doi:10.21203/rs.3.rs-3958902/v1

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Low muscle quality index is associated with increased risk of advanced fibrosis in adult patients with nonalcoholic fatty liver disease: NHANES 2011-2014

https://doi.org/10.21203/rs.3.rs-3958902/v1

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Muscle quality index (MQI) is a novel indicator reflecting the quality of skeletal muscles. The association between MQI and the development of advanced fibrosis in patients with nonalcoholic fatty liver disease (NAFLD) is unknown. We investigated the association of low MQI with advanced fibrosis among adults with NAFLD using a nationally representative sample of the U.S. population. Adults with NAFLD who participated in the National Health and Nutrition Examination Survey (NHANES) 2011–2014 were included. Sex-specific standard was used to define low and extremely low MQI. Univariate and multivariate logistic regressions were used to assess the association between MQI level and advanced fibrosis. In the study, 3,758 participants with NAFLD were included. The prevalence of low and extremely low MQI was 11.7% (95% CI: 10.4%-13.0%) and 2.2% (95% CI: 1.6%-2.8%), respectively. Among these participants, 96 were assessed to have advanced fibrosis. Individuals with low [(odds ratio (OR) 2.45, 95% confidence interval (CI) 1.22–4.91)] and extremely low MQI (OR 10.48, 95% CI 3.20–34.27) were associated with advanced fibrosis in multivariable analysis. A linear trend relationship was also observed between MQI level and the risk of advanced fibrosis (P_trend = 0.001). Subgroup and sensitivity analyses yielded similar results to the main analyses. Decreased MQI is highly prevalent, and is associated with an increased risk of advanced fibrosis in adult US population with NAFLD.

Health sciences/Diseases/Gastrointestinal diseases/Liver diseases

Health sciences/Diseases/Gastrointestinal diseases/Liver diseases/Non alcoholic fatty liver disease

Nonalcoholic fatty liver disease

NAFLD

Muscle quality

Liver fibrosis

NHANES

Nonalcoholic fatty liver disease (NAFLD) is a very common chronic liver disease, which has affected over 30% of the global population, with its prevalence increasing by 50.4% over the past three decades ¹. In the United States, the incidence of advanced fibrosis due to NAFLD is increasing, which can result in serious outcomes such as cirrhosis, hepatocellular carcinoma, liver transplantation, and even death ^2,3. The association between decreased muscle mass and liver fibrosis in NAFLD has been suggested, but it remains controversial ^4,5. Muscle quality index (MQI) is a measure of the quality of muscles, defined as the ratio of muscle strength to muscle mass, and MQI provides a more nuanced understanding of skeletal muscle than simply measuring muscle strength or mass alone ⁶. To our knowledge, the association between MQI and the development of advanced fibrosis in patients with NAFLD has not been studied. Therefore, we investigated the association of low MQI with advanced fibrosis among adults with NAFLD using a nationally representative sample of the U.S. population.

Data Source

We used cross-sectional data obtained from the 2011–2012 and 2013–2014 cycles of the National Health and Nutrition Examination Survey (NHANES), a nationally representative health survey of non-institutionalized US civilians. The MQI data was only available for the two 2-year cycles. The National Center for Health Statistics Research Ethics Review Board granted approval for the NHANES, and written consent was obtained from all participants. Further details about the survey can be found at http://www.cdc.gov/nchs/nhanes.

Data Collection and Definition

NAFLD was defined as a condition in which participants have a U.S. Fatty Liver Index (USFLI) score of ≥ 30 or a Hepatic Steatosis Index (HSI) score of ≥ 36, in the absence of other causes of liver disease (such as positive hepatitis C antibody or positive hepatitis B surface antigen), and without significant alcohol intake (> 4 drinks/day in men and > 3 drinks/day in women) ^7,8. Advanced fibrosis was assessed using three noninvasive scoring systems: the NAFLD fibrosis score (NFS), Fibrosis-4 (FIB-4) score, and AST to platelet ratio index (APRI). Participants with NAFLD were considered to have advanced fibrosis if they met any of the following criteria: (1) NFS > 0.676, (2) FIB-4 score > 2.67, or (3) APRI > 1.5 ^9–11. These scoring systems have been validated as reliable methods for diagnosing NAFLD and advanced fibrosis, and are widely used in NHANES studies ^12–14.

A hand dynamometer was used to measure handgrip strength (HGS), and dual-energy X-ray absorptiometry (DXA) was utilized to evaluate appendicular skeletal muscle mass (ASM). MQI was defined as the ratio of muscle strength and muscle mass, and computed as (dominant + non-dominant HGS) /ASM (kg/kg). In addition, MQI-Arm (dominant HGS/dominant arm ASM) and MQI-appendicular (dominant HGS/ASM) were also calculated. MQI was categorized as normal, low and extremely low, with 1 SD and 2 SD sex-specific standard deviations below the mean being used as cutoffs, respectively (Supplemental Table 1) ¹⁵. Anthropometric, sociodemographic, and laboratory data were also collected including age, sex, ethnicity, marital status, income, education, height, weight, platelet count, neutrophil count, lymphocyte count, alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), gamma-glutamyltransferase (γ-GGT), and uric acid.

Family income was assessed using poverty-income ratio (PIR) values, which are based on the ratio of family income to poverty. It was categorized into three groups: low (PIR ≤ 1.3), middle (1.3 < PIR < 3.5), and high income (PIR ≥ 3.5) ¹⁶. Diabetes mellitus (DM) was defined by a fasting glucose level ≥ 126 mg/dl, random glucose level ≥ 200mg/dl, HbA1c of ≥ 6.5%, self- reported medical history of diabetes, or treatment with anti-diabetic medication. Hypertension was defined by systolic blood pressure measure ≥ 140 mmHg, and/or diastolic blood pressure ≥ 90 mmHg, self-reported medical history of hypertension, or use of antihypertensive drugs. Hyperlipidemia was defined as an elevated triglyceride level (≥ 150 mg/dL) or cholesterol level (total cholesterol ≥ 200 mg/dL, LDL ≥ 130 mg/dL, or HDL < 40 mg/dL in men and < 50 mg/dL in women) or use of cholesterol-lowering agents ¹⁷. Physical activity (PA) was categorized according to the 2018 PA Guidelines. PA was considered "high" level if participants engaged in ≥ 150 minutes per week of moder-ate-intensity PA, or ≥ 75 minutes per week of vigorous-intensity PA, or an equivalent combination. Otherwise, it was considered "low" level ¹⁸.

Statistical Analysis

All results were presented using proper weighting procedures according to NHANES guidelines. Weighted mean ± standard errors and proportions (95% confidence intervals) were used for continuous and categorical variables, respectively. The chi-squared test or linear regression was used for comparing baseline characteristics when appropriate. Univariable and multivariable logistic regression were performed to evaluate the association between MQI level and advanced fibrosis. Test for linear trend was performed using MQI level as a continuous variable in the multivariable model. Subgroup analyses were performed according to the important factors, and the interaction was assessed using the likelihood ratio test. All analyses were performed using R software (version 4.1.2) and the ‘survey’ package, which accounts for the complex survey design of NHANES data. Two-sided p < 0.05 were considered significant.

The study included 3,758 adult individuals with NAFLD (Fig. 1), representing over 84.9 million non-institutionalized US civilians. Among these individuals, the prevalence (95% CI) of low and extremely low MQI was 11.7% (10.4%-13.0%) and 2.2% (1.6%-2.8%), respectively, corresponding to an estimated 9.9 million and 1.9 million individuals in the US. Of the participants with NAFLD, 96 were assessed to have advanced fibrosis. Baseline characteristics of the included participants are summarized in Table 1.

Table 1

Baseline characteristics of adult NAFLD patients stratified by MQI level.
Variables	Total (n = 3758)	Normal (n = 3162)	Low (n = 507)	Extremely low (n = 89)	P value
Age (years)	39.51 ± 0.42	39.26 ± 0.43	40.54 ± 0.84	43.57 ± 1.69	0.020
Sex (%)					0.974
Female	51.14(46.55,55.73)	86.31(84.60,88.03)	11.53(10.10,12.96)	2.15(1.31, 3.00)
Male	48.86(43.81,53.91)	85.98(83.15,88.81)	11.81(9.69,13.94)	2.21(0.91, 3.50)
Ethnicity (%)					< 0.001
Non-Hispanic white	63.90(53.23,74.58)	87.98(86.03,89.93)	9.97(8.48,11.46)	2.05(1.26, 2.85)
Non-Hispanic black	12.17(9.82,14.52)	74.98(70.86,79.10)	20.64(17.54,23.73)	4.38(2.48, 6.29)
Mexican	9.82(7.02,12.62)	85.89(82.99,88.79)	12.78(10.14,15.43)	1.33(0.33, 2.32)
others	14.11(12.17,16.06)	87.67(83.98,91.37)	10.87(7.54,14.21)	1.45(0.66, 2.25)
Married (%)					< 0.001
No	46.23(43.21,49.24)	83.28(80.82,85.73)	14.05(12.05,16.05)	2.67(1.63, 3.71)
Yes	53.77(46.54,61.01)	88.62(87.07,90.18)	9.62(8.24,11.01)	1.75(1.25, 2.26)
Family income (%)					0.115
Low	22.47(19.59,25.36)	83.07(80.20,85.95)	14.38(11.77,16.99)	2.54(1.81, 3.28)
Middle	31.76(27.19,36.32)	85.65(82.44,88.86)	12.40(9.57,15.24)	1.95(0.96, 2.94)
High	40.55(34.59,46.51)	88.23(86.00,90.46)	10.02(8.10,11.94)	1.75(0.79, 2.71)
Education (%)					0.540
Less than high school	13.65(11.31,15.98)	84.70(81.19,88.20)	13.30(10.12,16.48)	2.00(0.52, 3.48)
High school or higher	86.33(77.30,95.36)	86.40(84.68,88.13)	11.39(10.10,12.67)	2.21(1.53, 2.89)
Smoking (%)					0.603
Never	61.31(55.49,67.14)	86.24(84.43,88.05)	11.72(10.31,13.14)	2.04(1.25, 2.83)
Former	18.98(15.72,22.23)	87.49(84.02,90.96)	10.75(7.66,13.84)	1.76(0.35, 3.17)
Current	17.87(16.12,19.62)	84.49(81.81,87.17)	12.54(9.76,15.32)	2.97(1.30, 4.64)
BMI category (kg/m²) (%)					< 0.001
<25	22.90(19.95,25.85)	98.89(98.30,99.48)	0.95(0.46, 1.45)	0.16(-0.06, 0.37)
25–30	34.51(30.35,38.68)	94.01(92.54,95.49)	4.97(3.54, 6.40)	1.02(0.18, 1.86)
≥30	42.59(38.43,46.74)	72.93(69.73,76.13)	22.86(20.04,25.69)	4.21(3.07, 5.35)
ALT (IU/L)	26.21 ± 0.37	25.92 ± 0.39	28.45 ± 1.14	25.80 ± 1.25	0.080
AST (IU/L)	24.72 ± 0.23	24.59 ± 0.25	25.62 ± 0.55	25.04 ± 0.75	0.173
ALP (U/L)	64.94 ± 0.63	64.28 ± 0.66	68.85 ± 1.12	69.93 ± 5.43	0.001
γ-GGT (IU/L)	26.48 ± 0.66	26.10 ± 0.72	29.17 ± 1.17	27.09 ± 2.58	0.045
Uric acid (umol/L)	319.17 ± 1.82	314.80 ± 1.79	345.82 ± 5.08	349.62 ± 7.28	< 0.001
Neutrophil-to-lymphocyte ratio	2.15 ± 0.03	2.14 ± 0.03	2.21 ± 0.06	2.38 ± 0.14	0.176
Hypertension (%)					< 0.001
No	71.60(63.81,79.38)	89.43(88.20,90.67)	8.84(7.88, 9.80)	1.72(1.08, 2.37)
Yes	28.40(26.11,30.69)	77.88(74.66,81.09)	18.80(15.91,21.68)	3.33(2.14, 4.52)
Diabetes mellitus (%)					< 0.001
No	90.46(81.56,99.36)	88.17(86.80,89.54)	10.12(9.02,11.22)	1.71(1.03, 2.39)
Yes	9.54(8.36,10.72)	67.01(62.25,71.77)	26.38(20.49,32.28)	6.60(3.26, 9.95)
Hyperlipidemia (%)					< 0.001
No	31.69(27.79,35.59)	89.84(88.15,91.53)	9.19(7.69,10.68)	0.97(0.26, 1.69)
Yes	68.31(61.75,74.87)	84.44(82.40,86.48)	12.82(11.14,14.50)	2.74(1.96, 3.51)
Physical activity level (%)					< 0.001
Low	14.06(11.92,16.20)	83.55(80.35,86.75)	12.40(10.00,14.80)	4.05(2.01, 6.09)
High	67.44(60.77,74.11)	88.64(87.08,90.19)	10.00(8.73,11.28)	1.36(0.86, 1.86)
MQI (kg/kg)	3.33 ± 0.02	3.48 ± 0.02	2.46 ± 0.01	1.86 ± 0.06	< 0.001
MQI-arm (kg/kg)	12.57 ± 0.08	13.10 ± 0.06	9.67 ± 0.10	7.52 ± 0.13	< 0.001
MQI-appendicular (kg/kg)	1.71 ± 0.01	1.79 ± 0.01	1.27 ± 0.01	0.95 ± 0.03	< 0.001
Advanced fibrosis (%)					< 0.001
No	97.62(88.49,106.74)	87.23(85.76,88.69)	11.12(9.94,12.30)	1.65(1.05, 2.25)
Yes	2.38(1.69, 3.08)	42.09(30.29,53.90)	34.12(23.36,44.89)	23.78(16.33,31.24)
Data are presented as the weighted mean ± standard errors or weighted frequency (95% confidence intervals) as appropriate. The linear regressions were used for continuous variables, and the Chi-square tests were used for categorical variables in difference analyses. BMI, body mass index; ALT, alanine aminotransferase; AST, aspartate aminotransferase; ALP, alkaline phosphatase; γ-GGT, gamma-glutamyltransferase; MQI, muscle quality index.

In univariable analysis, compared with normal group, the risk of advanced fibrosis was higher in low MQI group [odds ratio (OR) 6.36, 95% confidence interval (CI) 3.40–11.90], and numerically higher in participants with extremely low MQI (OR 29.84, 95% CI 15.34–58.05) (Table 2; Supplemental Table 2). After adjusting for age, ethnicity, smoking, BMI category, ALT, AST, ALP, γ-GGT, uric acid, and neu-trophil-to-lymphocyte ratio, participants with low MQI (OR 3.69, 95% CI 1.78–7.66) and extremely low MQI (OR 12.87, 95% CI 5.73–28.94) remained a significantly higher association with advanced fibrosis. In another multivariable model that further adjusted for hypertension, DM, hyperlipidemia, and PA level, the association with advanced fibrosis persisted for the low MQI group (OR 2.45, 95% CI 1.22–4.91) and extremely low MQI group (OR 10.48, 95% CI 3.20–34.27). Notably, a linear trend relationship was observed between MQI level and the risk of advanced fibrosis (P_trend =0.001) (Table 2; Supplemental Table 2).

Table 2

Univariable and multivariable analysis of MQI, MQI-arm, MQI-appendicular for advanced fibrosis among adults with NAFLD.
Variables	Univariable model		Multivariable model 1		Multivariable model 2		P _trend
Variables	OR (95% CI)	P value	OR (95% CI)	P value	OR (95% CI)	P value	P _trend
MQI							0.001
Normal	Reference		Reference		Reference
Low	6.36(3.40,11.90)	< 0.001	3.69(1.78, 7.66)	0.001	2.45(1.22, 4.91)	0.015
Extremely low	29.84(15.34,58.05)	< 0.001	12.87(5.73,28.94)	< 0.001	10.48(3.20,34.27)	< 0.001
MQI-arm							0.038
Normal	Reference		Reference		Reference
Low	5.22(2.86, 9.51)	< 0.001	2.35(1.09, 5.06)	0.031	1.47(0.68, 3.19)	0.301
Extremely low	29.75(16.07,55.07)	< 0.001	13.70(6.42,29.23)	< 0.001	4.91(1.27,19.00)	0.024
MQI-appendicular							< 0.001
Normal	Reference		Reference		Reference
Low	5.66(3.17,10.13)	< 0.001	2.66(1.25, 5.65)	0.014	3.06(1.41, 6.60)	0.008
Extremely low	28.94(14.27,58.66)	< 0.001	13.36(5.77,30.95)	< 0.001	7.12(1.64,30.95)	0.012
Survey-weight adjusted logistic regressions were used in the univariable and multivariable model. The multivariate model 1 was adjusted for age, ethnicity, smoking, BMI category, ALT, AST, ALP, γ-GGT, uric acid, and neutrophil-to-lymphocyte ratio using appropriate sampling weights. The multivariate model 2 was adjusted for hypertension, diabetes mellitus, hyperlipidemia, and physical activity level in addition to model 1 using appropriate sampling weights. OR, odds ratio; CI, confidence interval; MQI, muscle quality index; BMI, body mass index; ALP, alkaline phosphatase; γ-GGT, gamma-glutamyltransferase.

When stratified by sex, BMI category, hypertension, DM, hyperlipidemia, and PA level, the association of low MQI group and extremely low MQI group with advanced fibrosis remained significant in most subgroups (Supplemental Table 3). The lower rate of outcome events may account for the absence of statistical significance in some subgroups and the wide confidence intervals.

When using MQI-arm and MQI-appendicular to define MQI, similar results were found in univariable and multivariable analysis, except that no statistical difference was found for low MQI-arm in full multivariable analysis (Table 2; Supplemental Table 4; Supplemental Table 5).

This is the first study that assessed the impact of MQI on the risk of advanced fibrosis in general adult population with NAFLD. We found that low MQI was associated with an increased risk of advanced fibrosis, and this association persisted even after some important confounders were taken into account including age, gender, obesity, physical activity and metabolic disorders ¹⁹. More importantly, the association exhibited a linear trend.

Decreased muscle mass and strength are very common in patients with NAFLD ^4,20. Notably, previous research found that the rate of muscle mass and strength loss did not parallel to each other, muscle strength declined at a faster rate than muscle mass, resulting in a progressive disparity between the two; this ongoing discrepancy implies a deterioration in muscle quality that may potentially lead to impaired physical abilities ¹⁹. MQI seems to be the best marker of muscle quality ¹⁹, and was found to be associated with metabolic derangements, systemic inflammation, and even mortality ^21–23. Lee et al. indicated that low muscle mass was independently associated with advanced fibrosis in subjects with NAFLD ⁴; however, the conclusion could not be supported by the study of Choe et al. ⁵. In addition, the association between handgrip strength and advanced fibrosis also could not be proven in patients with NAFLD ²⁰. Relative to muscle mass or strength alone, MQI can reflect the intricate intramuscular changes ⁶, such as intramuscular and intermuscular fat infiltration, which is extremely common in patients with NAFLD ²⁴. Interestingly, Hsieh et al. found that myosteatosis, but not sarcopenia, was significantly associated with fibrosis progression in NAFLD patients, which supports our results ²⁴.

The strengths of this study included the use of a representative sample of the US population and a rigorous methodology. However, there are several limitations to our study. First, we used non-invasive formulas to define NAFLD and advanced fibrosis instead of liver biopsy or elastography, due to the unavailability of liver biopsy or elastography in NHANES 2011–2014. However, these noninvasive formulas have been validated as reliable methods for NAFLD and liver fibrosis in the US and other populations, and are widely used in NHANES studies ¹⁴. Second, although a linear trend was found, the cross-sectional study design limits our ability to establish a causal relationship between MQI level and advanced fibrosis.

In conclusion, decreased MQI is highly prevalent, and is associated with an increased risk of advanced fibrosis in adult US population with NAFLD. Resistance exercise training has been demonstrated to be an effective and feasible approach to activate underutilized muscles, thereby enhancing muscle quality ⁶. This improvement in muscle quality may help prevent the progression of liver fibrosis in individuals with NAFLD.

Data Availability Statement:

Data from the National Health and Nutrition Examination Survey are publicly available online at https://www.cdc.gov/nchs/nhanes/index.htm (accessed on 15 February 2023)

Author contributions:

X.T. and C.Q.: study concept and design.

X.T., Q.R., Z.W., and S.T.: acquisition of data.

X.T. and N.L.: analysis and interpretation of data.

X.T. and Q.R.: drafting of the manuscript and preparing all Tables or Figures.

X.T., S.D., J.W., and C.Q.: critical revision of the manuscript for important intellectual content.

Acknowledgments:

None.

Funding:

This study was supported by grants from Xi'an Science and Technology Plan Project(22YXYJ0122).

Conflicts of Interest:

The authors declare that they do not have any conflict of interest.

Ethics Statement:

This study protocol was reviewed and approved by NCHS Ethics Review Board, approval number (Protocol #2011-17). Written informed consent was collected from all participants enrolled in the National Health and Nutrition Examination Survey. Further details can be found at https://www.cdc.gov/nchs/nhanes/irba98.htm.

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No competing interests reported.

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Low muscle quality index is associated with increased risk of advanced fibrosis in adult patients with nonalcoholic fatty liver disease: NHANES 2011-2014

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