What’s Known

The Chinese visceral adiposity index (CVAI), a novel biomarker of visceral obesity developed and validated principally among easterners, was found to be independently associated with non-alcoholic fatty liver disease (NAFLD) and liver fibrosis.

What’s New

It was found that CVAI was positively related to the risks of metabolic dysfunction-associated steatotic liver disease (MASLD), the new nomenclature of NAFLD, and liver fibrosis in western populations, suggesting that it could be a potential indicator for predicting MASLD and liver fibrosis in clinical practice.

Introduction

Non-alcoholic fatty liver disease (NAFLD) is the most common liver disease in the world, accounting for 25% of all cases of cirrhosis and hepatocellular carcinoma. ¹ NAFLD is expected to become the most prevalent cause of liver transplantation in Western countries by 2030. ² Furthermore, NAFLD is significantly associated with liver-specific and overall mortality. ³ It is an increasing public health concern that poses a global challenge. However, there is presently no approved pharmacotherapy for NAFLD. ⁴ Hepatic fibrosis is the precursor of cirrhosis and a predictor of severe liver disease and liver-related mortality. ⁵ Therefore, it is essential to identify potential risk factors associated with NAFLD and liver fibrosis for the prediction, detection, and management of these diseases.

Obesity is a risk factor for a variety of metabolic diseases, such as metabolic syndrome and type 2 diabetes mellitus (T2DM), and is particularly associated with NAFLD. ² It is worth noting that visceral fat is highly correlated with the severity of NAFLD and significantly increases risks of liver-specific and all-cause mortality in NAFLD patients. ⁶ Imaging examinations, including computed tomography and magnetic resonance imaging, are reliable methods for detecting abdominal adiposity, although they are expensive and involve radiation exposure. Hence, various anthropometric indicators such as waist circumference (WC), lipid accumulation product (LAP), visceral adiposity index (VAI), and Chinese visceral adiposity index (CVAI) have been used to assess abdominal obesity. Remarkably, CVAI appeared to have the strongest association with NAFLD among these abdominal adiposity indices, ⁷ indicating a prospective predictive value in metabolic disorders, T2DM, and NAFLD in the Chinese population. ^{7 - 9} In 2020, NAFLD was renamed metabolic dysfunction-associated fatty liver disease (MAFLD), and new diagnostic criteria were developed that are independent of alcohol intake or other concomitant liver diseases. ¹⁰ In one study, CVAI was found to be positively associated with MAFLD in Chinese adults with T2DM and may serve as an indicator for MAFLD. ¹¹ Recently, metabolic dysfunction-associated steatotic liver disease (MASLD) has been proposed as the latest nomenclature for NAFLD in 2023. ¹² Unlike MAFLD criteria, which require patients to meet two of seven metabolic disorders, MASLD is diagnosed based on one of five cardiovascular risk factors. ¹² However, there is no convincing evidence of an independent relationship between CVAI and MASLD. Additionally, CVAI showed reliable screening value in the diagnosis of NALFD in Easterners, while it is indefinite whether it can be used as a predictor in Westerners. On the other hand, liver fibrosis is an important pathological manifestation of advanced chronic liver disease, particularly MASLD, and has a significant impact on the prognosis of patients with liver disease. However, there is little evidence on the relationship between CVAI and liver fibrosis.

In light of these facts, the present study attempted to determine the relationships between CVAI with MASLD and liver fibrosis in the American population and validate the effectiveness of CVAI in MASLD and fibrosis diagnoses.

Patients and Methods

Study Population

For conducting this cross-sectional study, the data were obtained from the National Health and Nutrition Examination Survey (NHANES) database between January 2017 and March 2020 (www.cdc.gov/nchs/nhanes/). The NHANES is an ongoing, national, and cross-sectional survey conducted in the United States, which collected demographic, clinical, dietary, and health-related questionnaires and examination data. The NHANES recruited a total of 15560 participants from January 2017 to March 2020. 5403 participants were excluded due to not having vibration-controlled transient elastography (VCTE) results, 386 with ineligible VCTE results due to being pregnant or having implantable electronic device, and 748 with incomplete VCTE exam (fasting time<3 hours, <10 valid liver stiffness measurements, or median (M/[IQR] interquartile range>30% stiffness), resulting in a population of 9023. Of them, 5325 participants were excluded due to unavailable information on the calculation of CVAI and diagnosis of MASLD. Participants with missing data on aspartate aminotransferase (AST), smoking, alcohol consumption, physical activity, or statin use were also excluded. Finally, 3242 American patients were included in our analysis (figure 1).

Figure 1. The flowchart indicates the participants of the study.

The Institutional Ethics Review Board of the National Center for Health Statistics (NCHS) approved the survey protocol (Protocol#2018-01). Moreover, each participant provided written informed consent before participating in the study.

Sociodemographic, Laboratory, and Clinical Data

In the NHANES database, demographic information including age, sex, race, smoking status, alcohol consumption, physical activity, and history of medication was gathered through household interviews using an interviewer-administered questionnaire. Participants underwent anthropometric and laboratory evaluations using a Mobile Examination Center (MEC). The website () provided information about the measuring procedure. Anthropometric data, such as height (cm), weight (Kg), and WC (cm) were extracted. In addition, laboratory data including alanine aminotransferase (ALT), aspartate aminotransferase (AST), gamma-glutamyl transpeptidase (GGT), total cholesterol (TC), triglyceride (TG), high-density lipoprotein (HDL), hemoglobin A1c (HbA1c), fasting plasma glucose (FPG) were extracted for this study.

Body mass index (BMI) was calculated by dividing the weight (Kg) by height in (m) squared. The smoking status was determined using the self-report questionnaire. Alcohol abuse was defined as consumption of ≥30 g/day in men and ≥20 g/day in women. ¹³ Participants who engaged in moderate/vigorous job or recreational activities were categorized as having had physical activity. ¹³ Hypertension was defined as a systolic blood pressure ≥140 mmHg and/or a diastolic blood pressure ≥90 mmHg, as reported by a health practitioner, or current use of anti-hypertensive medications. ¹⁴ Diabetes mellitus can be diagnosed in the following conditions: 1) reported by a health professional, 2) utilizing anti-diabetic medications, 3) HbA1c (%)>6.5; 4) FPG (mmol/L) ≥7.0 mmol/L, 5) random blood glucose (mmol/L) ≥11.1 mmol/L. ¹⁵ Viral hepatitis was defined as the presence of hepatitis B virus surface antigen (HBsAg) and hepatitis C virus (HCV) RNA or antibodies.

The calculations of LAP, VAI, and CVAI were consistent with the previously reported formula. ⁷

For men:

LAP=[WC (cm)-65]×TG (mmol/L)

VAI=WC (cm)÷[39.68+1.88×BMI (Kg/m²)]×[TG (mmol/L)÷1.03]×[1.31÷HDL (mmol/L)]

CVAI=-267.93+0.68×age (year)+0.03×BMI (Kg/m²)+4.00×WC (cm)+22.00×LgTG (mmol/L)-16.32×HDL (mmol/L)

For women:

LAP=[WC (cm)-58]×TG (mmol/L)

VAI=WC (cm)÷[36.58+1.89×BMI (Kg/m²)]×[TG (mmol/L)÷0.81]×[1.52÷HDL (mmol/L)]

CVAI=-187.32+1.71×age (year)+4.32×BMI (Kg/m²)+1.12×WC (cm)+39.76×LgTG (mmol/L)-11.66×HDL (mmol/L)

Definition of MASLD and Significant Fibrosis

VCTE is a well-studied method with high diagnostic accuracy for evaluating steatosis and fibrosis in large populations. ¹⁶ The elastography measurements were obtained in the NHANES MEC, using the FibroScan^® (model 502 V2 Touch) equipped with a medium or extra-large wand (probe). Examinations were considered reliable only when measures, taken after a fasting period of at least three hours, proved valid for 10 times, and each valid measure exhibited an interquartile IQR/M <30%. Previous studies defined liver steatosis as a median Controlled Attenuation Parameter (CAP) ≥274 dB/m and severe liver fibrosis as a median Liver Stiffness Measurement (LSM) ≥8.0 KPa. ^{17 , 18} MASLD was defined as steatosis along with one of the five cardiovascular risk factors, and no other discernible reason, such as excessive drinking, viral hepatitis, or steatogenic pharmaceutical use (amiodarone, valproate, methotrexate, tamoxifen, and corticosteroid). ¹²

Statistical Analysis

Continuous variables were expressed as median (interquartile range), and categorical variables were presented as frequency (percentages). To compare characteristics between groups, the Kruskal-Wallis test was used for continuous variables, and the Chi square test was used for categorical variables. Logistic regression analysis was used to investigate the associations between CVAI and MASLD or liver fibrosis. Model 1 was a crude model with no adjusted variable. Model 2 was adjusted for covariables including age, sex, race, HbA1c, FPG, ALT, AST, GGT, and TC. In Model 3, covariables were further adjusted for smoking status, alcohol abuse, physical activity, statin use, hypertension, and diabetes. Moreover, the restricted cubic spline (RCS) was used to investigate the relationships between CVAI, MASLD, and fibrosis on a continuous scale. We used the area under the receiver operating characteristic (AUROC) curve to evaluate the predictive performances of abdominal indices. The DeLong test was utilized to compare AUROCs. The optimal cut-offs were selected according to the highest Youden index. All analyses were conducted using R software, version 4.2.2 (R Development Core Team, New Zealand). P≤0.05 indicated statistical significance.

Results

Characteristics of the Participants

A total of 3242 participants were enrolled in this study for final analysis (figure 1). In the US population, 825 participants were diagnosed with MASLD, and 316 participants had hepatic fibrosis. The baseline characteristics of participants according to the quartiles of CVAI are shown in table 1. Individuals with high CVAI values were older, had less frequent physical activity, higher prevalence of hypertension, and diabetes, as well as had higher BMI, WC, ALT, AST, GGT, TC, TG, HbA1c, FPG, LAP, VAI, and CVAI while lower HDL than the group of people having low values of CVAI. The proportions of MASLD and liver fibrosis were significantly higher in the groups with higher CVAI.

Association between CVAI and MASLD

Multivariate logistic regression models were performed to investigate the relationship between CVAI and MASLD diagnosed by VCTE (table 2). After adjusting for age, sex, race, HbA1c, FPG, ALT, AST, GGT, TC, smoking status, alcohol overuse, physical activity, statin use, hypertension, and diabetes in model 3, High CVAI values (Q2-Q4 groups) had a significant positive association with MASLD compared to the Q1 reference group (odds ratio (OR)=3.66, 95% Confidence interval (CI)=2.44-5.63 for Q2, OR=7.95, 95% CI=5.31-12.23 for Q3 and OR=14.84, 95% CI=9.80-23.06 for Q4, P<0.001). Furthermore, the multivariable-adjusted spline model revealed a monotonically increasing correlation between CVAI and the risk of MASLD (figure 2A).

Figure 2. The associations between CVAI and (A) metabolic dysfunction-associated steatotic liver disease and (B) liver fibrosis on a continuous scale are shown. Solid lines represent odds ratios (OR), and the shade area represents 95% confidence intervals (CI). The model was adjusted for age, sex, race, alanine aminotransferase, aspartate aminotransferase, gamma-glutamyl transpeptidase, total cholesterol, triglyceride, hemoglobin A1c, fasting plasma glucose, smoking status, alcohol overuse, physical activity, statin use, hypertension, and diabetes.

Association between CVAI and Liver Fibrosis

Hepatic fibrosis represents the prognosis of chronic liver disease. Logistic regression analyses were also executed to investigate the association between CVAI and significant fibrosis diagnosed by VCTE in the NHANES group (table 2). In all models, high CVAI had a significantly positive association with fibrosis. The association between high CVAI (Q3 and Q4 groups) and hepatic fibrosis was still significant (OR=2.44, 95% CI=1.39-4.43 for Q3 group and OR=7.46, 95% CI=4.36-13.30 for Q4 group, respectively, P<0.001) after further adjustment for age, sex, race, HbA1c, FPG, ALT, AST, GGT, TC, smoking status, excessive alcohol consumption, physical activity, statin use, hypertension, and diabetes in model 3. Moreover, a monotonically increasing association was found between CVAI and hepatic fibrosis (figure 2B).

Diagnostic Ability of CVAI for MASLD

The AUROC values together with the optimal cut-offs and ROC curves of abdominal obesity indices were displayed in table 3 and figure 3A. The CVAI showed a valuable diagnostic role for MASLD in the US general population, with the AUROCs of 0.759 (95% CI=0.742-0.777), which was significantly higher than WC (OR=0.729, 95% CI=0.711-0.748), LAP (OR=0.739, 95% CI=0.721-0.757), and VAI (OR=0.739, 95% CI=0.721-0.757). The optimal CVAI cut-off for diagnosing MASLD was 136.654, with a sensitivity of 0.608 and a specificity of 0.790. The diagnostic performance was further evaluated in several subgroups divided by BMI and sex. The CVAI had the highest AUROC value in all subgroups compared to WC, LAP, and VAI (table 3).

Figure 3. The receiver operating characteristic curves of abdominal obesity indices for (A) metabolic dysfunction-associated steatotic liver disease and (B) liver fibrosis are shown.

Diagnostic Ability of CVAI for Liver Fibrosis

The CVAI also showed significantly higher AUROC value (OR=0.771, 95% CI=0.742-0.800) in hepatic fibrosis detection than those of WC (OR=0.754, 95% CI=0.723-0.785), LAP (OR=0.701, 95% CI=0.670-0.731), and VAI (OR=0.621, 95% CI=0.590-0.652). The best cut-off values of CVAI, WC, LAP, and VAI were 160.717 (sensitivity 0.737, specificity 0.691), 109.650 (sensitivity 0.649, specificity 0.773), 53.062 (sensitivity 0.658, specificity 0.693), and 1.613 (sensitivity 0.554, specificity 0.651), respectively. In the subgroup analyses, the CVAI outperformed WC, LAP, and VAI in fibrosis diagnosis, with the highest values of AUROC (table 4 and figure 3B).

Discussion

In this large-scale cross-sectional study, the associations between CVAI and MASLD or hepatic fibrosis among Americans were investigated. There were significant positive correlations between CVAI and the probability of MASLD and hepatic fibrosis. The ROC curves indicated that CVAI had a satisfactory performance for screening MASLD and liver fibrosis. Therefore, CVAI might serve as a biomarker for both MASLD and liver fibrosis with diagnostic value in the American population.

The CVAI is a novel index based on age, BMI, WC, TG, and HDL, which reflects the amount of visceral fat. Previous investigations on NAFLD and chronic hepatitis C reported an association between visceral obesity and liver damage, including steatosis and disease progression. ^{19 - 21} Excessive accumulation of visceral adipose tissue was associated with chronic systemic inflammation and was related to increased hepatic inflammation and fibrosis. ^{22 , 23} Visceral adipose tissue could lead to the release of free fatty acids, secretion of adipokines, and infiltration of immune cells, which in turn could trigger lipotoxicity, promote the production of proinflammatory mediators, and drive insulin resistance and metabolic disorders, and ultimately contribute to the stimulation of inflammation, tissue regeneration, and fibrogenesis. ^{1 , 6 , 24} Furthermore, the positive associations between CVAI and obesity-related metabolic diseases were reported. ^{7 , 9 , 25 , 26}

The findings of the present study were consistent with a recent study by Zhao and others, who enrolled 24191 Chinese participants and found that CVAI was independently associated with the risk of MASLD. ²⁷ However, several differences existed between the findings of this study and those of the present study, including ethnicity and the diagnostic criteria of MASLD. The assessment of MASLD was based on the MAFLD standards proposed by Zhao and colleagues in 2020. ²⁷ In fact, MASLD is the latest nomenclature of NAFLD, with significantly different diagnostic criteria compared to MAFLD. MAFLD might identify more patients because its definition is independent of excessive alcohol consumption and viral hepatitis. ²⁸ A previous study also reported that CVAI was significantly related to NAFLD prevalence and had the highest diagnostic value for NAFLD compared to WC, VAI, and LAP. ⁷ Similar findings were found in this study when MASLD, the new term of NAFLD, was adopted. Moreover, an independent relationship between CVAI and NAFLD was revealed in specific populations, such as early postmenopausal women, lean adults, and T2DM patients. ^{11 , 29 , 30} On the other hand, hepatic fibrosis has been repeatedly shown to be the histological alteration with the highest prognostic significance in a range of chronic liver diseases, including NAFLD. Studies on the relationship between CVAI and liver fibrosis are inadequate. One recent research based on 147 biopsy-confirmed NAFLD patients provided evidence for an independent relationship between CVAI and liver fibrosis. However, the study group seemed insufficient and lacked a healthy control population. ³¹ All these studies were conducted in Asian populations. CVAI is a novel visceral obesity biomarker established based on Chinese data and validated primarily among Chinese. Furthermore, different ethnic groups had different body fat characteristics, and there were associations between strong ethnic heterogeneity in anthropometric measures and NAFLD. ^{32 , 33} Therefore, the correlations between CVAI and MASLD or liver fibrosis are worth further exploring among various ethnic populations living in different regions. The consistency of the results in Caucasians strengthened the hypothesis of positive relationships between CVAI and MASLD or hepatic fibrosis. However, the findings of the present study were different from certain previous investigations. ^{29 - 31} Significant heterogeneity existed across different analyses because of the diagnostic criteria (NAFLD, MAFLD, or MASLD), subjects being investigated (T2DM patients, lean individuals, or general population), ethnicity (Asian or Caucasian), and the study design (prospective or cross-sectional). Further subgroup analyses were performed to test the robustness of the findings. It is worth mentioning that CVAI seemed to outperform other traditional obesity indices in predicting both MASLD and fibrosis among the different subgroups. The reason might be that traditional obesity indices such as WC were more strongly associated with subcutaneous fat than visceral adipose tissue. However, CVAI was a reliable surrogate biomarker of visceral obesity. ³⁴ According to the results of the present study, the CVAI, a novel index established and validated primarily among eastern populations, indicated promising predictive value in western populations, ensuring the generalizability and inclusiveness of CVAI.

There are some limitations that need to be noted. First, fatty liver and hepatic fibrosis were diagnosed by VCTE in NHANES rather than a liver biopsy. However, VCTE was a well-validated method in diagnosing steatosis and fibrosis, with high sensitivity and specificity. ^{35 , 36} Second, this cross-sectional design could not determine the causal relationships between CVAI and MASLD or fibrosis, which required further investigation in prospective studies.

Conclusion

This study was the first study that investigated the correlations between CVAI, MASLD, and fibrosis in the general US population with the largest sample size. CVAI was positively associated with MASLD and liver fibrosis. The CVAI had a satisfactory ability to distinguish MASLD and fibrosis and might be a novel indicator for identifying MASLD and liver fibrosis patients in clinical practice.

Authors’ Contribution

H.L, M.D, G.L, and J.C conceived and designed the study; performed the analysis; and wrote and reviewed the manuscript. All authors have read and approved the final manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Conflict of Interest:

None declared.

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