Liver fibrosis is closely related to metabolic factors in metabolic fatty liver disease associated with hepatitis B virus infection

establishment of the study

As shown in Fig. 1, a total of 681 patients with biopsy-proven steatosis were included in the data screening. A total of 175 subjects with steatosis were excluded as they did not meet the diagnostic criteria for MAFLD, while 105 subjects were excluded due to incomplete data. Among the 401 patients diagnosed with MAFLD, 256 patients were overweight/obese, 64 patients had T2DM, and 81 patients with normal or lean weight had metabolic disorders. The mean age of the included patients was 43.14 ± 11.31 years; 44.64% (179/401) of patients had MAFLD with HBV infection (MAFLD + HBV group) and 55.36% (222/401) of patients had MAFLD without HBV infection (MAFLD group).

The proportion of male patients was higher in the MAFLD + HBV group than in the MAFLD group (88.82% vs. 72.52%, P < 0.001). No significant differences were observed in age, SBP, DBP, BMI, FPG, HDL-c, SUA or ALB levels between the MAFLD and MAFLD + HBV groups (P>0.05). However, the MAFLD + HBV group had lower levels of liver enzymes, LDL-c, TG and TC, as well as lower rates of obesity, hypertension, DM2, low HDL-c, hypertriglyceridemia, hypercholesterolemia and hyperuricemia than the MAFLD group (P< 0.05) (Table 1).

Table 1 Comparison of clinical features between fatty liver disease associated with metabolic dysfunction with and without hepatitis B virus infection before and after propensity score matching.

After PSM, 83 pairs were finally matched and there were no statistically significant differences in gender, age, BMI, DBP, SBP, FPG, LDL-c, TC, liver enzyme levels or rates of hypertension, T2DM, low HDL-c, hypertriglyceridemia , hypercholesterolemia or hyperuricemia between the two groups (P> 0.05) (Table 1).

Comparison of histological features in MAFLD patients with and without HBV infection

After PSM, sex, age, BMI, liver enzymes and metabolic factors were comparable between patients with and without HBV infection. Inflammation scores and liver fibrosis stages were higher in the MAFLD + HBV group than in the MAFLD group, while steatosis and ballooning scores were lower (P< 0.05) (Fig. 2). In the multivariate analysis, model 1 was adjusted for age and sex, while model 2 was adjusted for model 1 plus metabolic parameters, including BMI, DM2, low HDL-c, hypertriglyceridemia, hypercholesterolemia, high LDL-c, hypertension and hyperuricemia . Results indicated that HBV infection was associated with lower fatty liver scores (OR: 0.251, 95% CI: 0.117–0.542, P< 0.001) and balloon scores (OR: 0.119, 95% CI: 0.049–0.294, P< 0.001) even higher stages of liver fibrosis (OR: 3.140, 95% CI: 1.479–6.663, P= 0.003) in patients with MAFLD (Table 2). However, no significant differences in inflammation were observed between patients with and without HBV infection after adjusting for confounders.

Figure 2

Comparison of histopathological features between fatty liver disease associated with metabolic dysfunction with and without hepatitis B virus (HBV) infection. (AN) Comparison of the score of hepatic steatosis secreted by HBV infection; (B) comparison of the ballooning score segregated by HBV infection; (Ç) comparison of the inflammation score secreted by HBV infection; (D) comparison of the stage of fibrosis secreted by HBV infection.

Table 2 Odds ratio of hepatitis B virus infection to liver fibrosis in the population with fatty liver disease associated with metabolic dysfunction.

Comparison of clinical and histological features of patients with and without liver fibrosis in HBV-infected MAFLD

Of the 179 patients in the MAFLD + HBV group, 18.44% (33/179) of patients had chronic HBeAg-positive infection, 27.37% (49/179) of patients had chronic HBeAg-positive hepatitis, 22.91% ( 41/179) of the patients had HBeAg negative chronic infection and 31.28% (56/179) had HBeAg negative chronic hepatitis. Furthermore, 75.98% (136/179) of patients were HBV-DNA positive and 43.58% (78/179) of patients in the MAFLD + HBV group had significant liver fibrosis (S ≥ 2). There were no statistically significant differences in sex, age, SBP, DBP, BMI, ALT, AST, LDL-c, HDL-c, TG or TC between patients with and without liver fibrosis. Furthermore, the rates of HBeAg-positive, HBV-DNA-positive, hypertension, low HDL-c, hypertriglyceridemia, hypercholesterolemia and hyperuricemia did not differ significantly between patients with and without liver fibrosis.P>0.05). Among patients in the MAFLD + HBV group, those with liver fibrosis had higher levels of GGT and FPG, and a higher percentage of T2DM and obesity/overweight status than those without (P< 0.05) (Table 3). For histological comparison, the proportion of patients with active inflammation (inflammation score ≥ 2) was significantly higher among those with liver fibrosis than those without liver fibrosis (85.90% vs. 37.62%, P< 0.001), while the proportions of severe steatosis and ballooning degeneration did not differ significantly between the two groups (P>0.05).

Table 3 Comparison of clinical characteristics between MAPLD patients with hepatitis B virus infection according to the presence of significant liver fibrosis.

Risk factors for liver fibrosis in MAFLD patients with HBV infection

Univariate and multivariate logistic regression analyzes were performed to further explore risk factors for liver fibrosis in MAFLD patients with HBV infection. Univariate analysis confirmed that DM2 (OR: 5.540, 95% CI: 1.72–17.63; P= 0.004) and elevated GGT levels (OR: 2.991, 95% CI: 1.612–5.550; P= 0.001) were risk factors for liver fibrosis (Table 4). Multivariate regression analysis, considering sex, age, metabolic factors, viral factors and liver enzymes, revealed that hypertension (OR: 2.640, 95% CI: 1.091–6.368; P= 0.031), DM2 (OR: 4.939, 95% CI: 1.121–21.796; P= 0.035) and elevated GGT levels (OR: 3.980, 95% CI: 1.735–9.132; P= 0.001) were independent risk factors for liver fibrosis in MAFLD patients with HBV infection.

Table 4 Risk factors for liver fibrosis in patients with fatty liver disease associated with metabolic dysfunction with hepatitis B virus infection.
Liver fibrosis is closely related to metabolic factors in metabolic fatty liver disease associated with hepatitis B virus infection

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