Metabolic burden but not metabolic dysfunction-associated steatotic liver disease affects the prognosis of patients with hepatocellular carcinoma after hepatectomy: a retrospective cohort study

Introduction

Hepatocellular carcinoma (HCC) is the most common type of primary liver cancer and affects more than 800,000 patients around the world every year (1,2). The main risk factors for HCC include chronic hepatitis B virus (HBV) or hepatitis C virus infection, alcohol-related liver disease, obesity, diabetes, metabolic dysfunction-associated steatotic liver disease (MASLD) and so on. Although chronic B or C virus infections and alcohol-related liver disease are still the most common etiologies of HCC in many countries, the prevalence of MASLD-associated HCC has rapidly increased over the past two decades (3-6). MASLD has emerged as the most common chronic liver disease, affecting more than 30% of the worldwide adult population (5,7). In China, although more than 80% of HCC cases are attributed to HBV infection, many patients also with concurrent MASLD (8).

MASLD is characterized by abnormal hepatic lipid accumulation together with metabolic disorders and cardiometabolic risk factors, including type 2 diabetes mellitus, hypertension, overweight/obesity and dyslipidemia (9). Previous studies on the influence of concurrent MASLD on the prognosis of patients with HCC after hepatectomy are controversial (10,11). Some investigations have suggested that concurrent MASLD can increase the incidence of postoperative complications and worsen the oncological outcomes of patients with HCC, whereas other investigators have argued that concurrent MASLD does not affect the prognosis of patients with HCC following hepatectomy (10,12-14). Moreover, according to the diagnostic criteria of MASLD, the number of metabolic abnormalities present varies across patients. For example, some patients may have only one metabolic abnormality, such as obesity, while other patients may simultaneously have three metabolic abnormalities, such as obesity, diabetes and hypertension. However, previous studies did not consider the impact of the metabolic burden [defined as the cumulative number of metabolic abnormalities (15)] on the prognosis of HCC patients after hepatectomy. Accordingly, in this study, we attempted to clarify whether concurrent MASLD and the metabolic burden could affect the prognosis of HCC patients after hepatectomy. We present this article in accordance with the STROBE reporting checklist (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0552/rc).

Methods

Data of HCC patients who received primary hepatectomy from 2013 to 2018 at West China Hospital were retrospectively reviewed. Patients with ruptured HCC, recurrent HCC, positive surgical margins or combined HCC-cholangiocarcinoma and who received preoperative anticancer treatments were excluded. After the operation, patients were regularly followed up as provided by our previous reports (16,17). In brief, patients were regularly monitored every 3 months during the first 2 postoperative years and then every 6 months. The follow-up examinations for HCC patients after hepatectomy included liver and renal function, serum alpha-fetoprotein (AFP), blood cell tests, HBV DNA, visceral ultrasonography or computed tomography or magnetic resonance imaging, and chest radiography. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board of West China Hospital of Sichuan University (No. 2026757), and written informed consent was waived because of the retrospective study design.

Definitions

The diagnosis of MASLD was made according to the guidelines released by the Chinese Society of Hepatology, Chinese Medical Association, in 2024 (8). In general, the diagnosis of MASLD was based on the presence of hepatic steatosis combined with at least one of the following metabolic abnormalities, without other liver disease causes or significant alcohol consumption (8). In the current study, metabolic abnormalities included overweight/obesity, hypertension, prediabetes or type 2 diabetes, hypertriglyceridemia and low levels of high-density lipoprotein cholesterol (HDL-C) (8). Overweight/obesity was defined as a body mass index (BMI) ≥24 kg/m² or a waist circumference ≥90 cm in men or ≥85 cm in women (8). Since this was a retrospective study, waist circumference is not a routine measurement indicator for Chinese patients. In reference to other studies, in the current study, waist circumference was assessed using CT scans of an abdominal slice at the level of the umbilicus, which lies at the level of the third lumbar vertebra (18,19). Hypertension was defined as blood pressure ≥130/85 mmHg or on pharmacological treatment (8). Prediabetes or type 2 diabetes was defined as a fasting blood glucose concentration ≥6.1 mmol/L or a 2-h plasma glucose concentration during an oral glucose tolerance test ≥7.8 mmol/L or a hemoglobin A1c concentration ≥5.7% or a previous diagnosis of diabetes (8). Hypertriglyceridemia was defined as a triglyceride concentration ≥1.70 mmol/L or under lipid-lowering treatment (8). HDL-C ≤1.0 mmol/L in men or ≤1.3 mmol/L in women or under lipid-lowering treatment was considered low (8). The albumin-bilirubin (ALBI) grade was calculated with the following formula: ALBI = [log₁₀ bilirubin (µmol/L) × 0.66] + [albumin (g/L) × −0.085] (20,21). ALBI values were divided into 3 grades as follows: grade 1 (less than −2.60), grade 2 (between −2.60 and −1.39), and grade 3 (above −1.39) (20). The prognostic nutritional index (PNI) was calculated as serum albumin concentration (g/L) + 5 × lymphocyte count (10⁹/L) (22). A PNI <45 was defined as a low PNI (22). The fibrosis-4 (FIB-4) index was calculated by the following equation: FIB-4 = [age (years) × aspartate aminotransferase (AST) (U/L)]/[platelet (10⁹/L) × alanine aminotransferase (ALT)^1/2 (U/L)] (23). Patients were considered to have advanced fibrosis when the FIB-4 index was >3.25 (24). Severe postoperative complications were defined as ≥ Clavien-Dindo grade 3 postoperative complications (16,25). Metabolic burden was defined as the cumulative number of metabolic abnormalities including overweight/obesity, hypertension, prediabetes/diabetes and dyslipidemia (including hypertriglyceridemia and/or low HDL-C) (15). In the current study, metabolic burden in HCC patients ranged from 0 to 4. Recurrence-free survival (RFS) was defined as the interval time from operation to recurrence or the last follow-up (17). Overall survival (OS) was defined as the time from operation to death from any cause or the last follow-up (17).

Statistical analysis

Statistical analyses were performed with SPSS 29.0 (SPSS Company, Chicago, IL, USA) for Windows. Categorical variables were compared using χ² or Fisher’s exact tests, whereas continuous variables were analyzed via Student’s t-tests or Mann-Whitney U tests. The Kaplan-Meier method with the log-rank test was used to compare the RFS and OS rates. Logistic regression analysis was carried out to identify the independent risk factors associated with severe postoperative complications. Multivariate Cox regression including all variables with a P value <0.1 in the univariate analysis was performed to identify independent risk factors for RFS and OS. X-tile software (version 3.6.1) was used to calculate the optimal cutoff points of metabolic burden for predicting patient OS. Propensity score matching (PSM) at a 1:1 ratio using the nearest-neighbor matching algorithm was performed to balance the baseline characteristics of patients with and without MASLD. P values <0.05 were considered to indicate statistical significance.

Results

A total of 1,370 patients were included in this study, including 1,147 male patients and 213 female patients. The median patient age in the current study was 52 years. In accordance with the diagnostic criteria, MASLD was observed in 206 patients. In the whole cohort, metabolic burden 0, 1, 2, 3 and 4 were observed in 325, 488, 376, 143 and 38 patients respectively. ALBI grades 1, 2, and 3 liver functions were observed in 713, 657 and 0 patients, respectively. In accordance with the Barcelona Clinical Liver Cancer (BCLC) staging system, 125, 991, 79 and 175 patients had BCLC stage 0, A, B, and C disease, respectively. All patients were split into three groups by the X-tile software: metabolic burden 0 (n=325), metabolic burden 1–2 (n=864) and metabolic burden 3–4 (n=181).

Comparison of postoperative prognosis between patients with and without MASLD

In this study, before PSM, 75 (5.5%) patients, including 13 (6.3%) patients with MASLD and 62 (5.3%) patients without MASLD, experienced severe postoperative complications. No significant difference was observed between the two groups (P=0.57). Because the baseline characteristics of the two groups were not comparable, we used PSM to balance the baseline clinicopathological variables between the two groups (Table 1). After PSM, 202 pairs of patients from the two groups were matched. In the matched cohort, 11 (5.4%) patients with MASLD and 14 (6.9%) patients without MASLD experienced severe postoperative complications (P=0.54).

In the current study, the median follow-up time was 38 months for patients without MASLD and 40 months for patients with MASLD, respectively. Before PSM, the 5-year RFS and OS rates of patients with MASLD were 43.4% and 59.7%, respectively, which were similar to those of patients without MASLD (RFS: 39.4%, OS: 56.0%; P_RFS=0.16, P_OS=0.26). After PSM, the 5-year RFS rate of patients with MASLD was 44.7%, which was comparable to that of patients without MASLD (40.2%, P=0.33; Figure 1A). The 5-year OS rates of the two groups were also similar after PSM (MASLD vs. non-MASLD: 61.2% vs. 60.7%; P=0.69; Figure 1B).

Figure 1 Comparison of recurrence-free survival (A) and overall survival (B) between patients with and without MASLD after PSM. MASLD, metabolic dysfunction-associated steatotic liver disease; PSM, propensity score matching.

Factors associated with postoperative complications

As shown in Table 2, multivariate analysis revealed that only ALBI grade 2 [odds ratio (OR) =2.463; 95% confidence interval (CI): 1.495–4.057; P<0.001] and the metabolic burden (0 for reference; 1–2: OR =2.159; 95% CI: 1.046–4.457; P=0.04; 3–4: OR =3.769; 95% CI: 1.637–8.677; P=0.002) were independent risk factors for postoperative complications. Concurrent MASLD did not contribute to postoperative complications. The incidence of severe postoperative complications was 2.8% in patients with metabolic burden 0, 5.7% in patients with metabolic burden 1–2, and 9.4% in patients with metabolic burden 3–4 in the whole cohort (P_{for trend}=0.007).

Factors associated with postoperative RFS

As listed in Table 3, in the multivariate analysis, a tumor size >5 cm (HR =1.472; 95% CI: 1.254–1.727; P<0.001), a high preoperative AFP level (HR =1.271; 95% CI: 1.084–1.490; P=0.003), an ALBI grade of 2 (HR =1.287; 95% CI: 1.106–1.498; P=0.001), the presence of MVI (HR =1.717; 95% CI: 1.431–2.059; P<0.001), advanced BCLC stage (HR =1.757; 95% CI: 1.461–2.112; P<0.001), poor tumor differentiation (HR =1.209; 95% CI: 1.034–1.414; P=0.02) and metabolic burden (0 for reference; 1–2: HR =1.319; 95% CI: 1.089–1.597; P=0.005; 3–4: HR =1.550; 95% CI: 1.201–2.000; P<0.001) independently associated with postoperative RFS. MASLD was not an independent risk factor for RFS. The 5-year RFS rates of patients with metabolic burden 0, 1–2 and 3–4 were 50.5%, 38.4%, and 29.6%, respectively (P_{for trend}=0.04, Figure 2A).

Figure 2 Comparison of recurrence-free (A) and overall (B) survival in patients with metabolic burden 0, 1–2 and 3–4 in the entire cohort.

Factors associated with postoperative OS

As presented in Table 4, multivariate analysis revealed a tumor size >5 cm (HR =1.974; 95% CI: 1.622–2.403; P<0.001), high preoperative AFP levels (HR =1.333; 95% CI: 1.104–1.609; P=0.003), ALBI grade 2 (HR =1.491; 95% CI: 1.245–1.785; P<0.001), the presence of MVI (HR =1.894; 95% CI: 1.549–2.314; P<0.001), poor tumor differentiation (HR =1.299; 95% CI: 1.079–1.564; P=0.006), advanced BCLC stage (HR =1.788; 95% CI: 1.455–2.197; P<0.001), and metabolic burden (0 for reference; 1–2: HR =1.447; 95% CI: 1.148–1.825; P=0.002; 3–4: HR =2.076; 95% CI: 1.543–2.794; P<0.001) independently associated with postoperative OS. MASLD was also not independently related to OS. The 5-year OS rates of patients with metabolic burden 0, 1–2 and 3–4 were 65.2%, 56.2%, and 43.7%, respectively (P_{for trend}=0.001, Figure 2B).

Discussion

Previous studies concerning the effects of MASLD on the postoperative outcomes of patients with HCC after hepatectomy are controversial (10,12,26). In this study, we confirmed that concurrent MASLD did not affect either postoperative complications or long-term oncological prognosis in HCC patients after hepatectomy. However, metabolic burden can adversely influence both the short-term and long-term outcomes of patients with HCC after hepatectomy. The more metabolic burden patients have, the more likely they are to suffer from severe postoperative complications and poor oncological outcomes for HCC patients after hepatectomy.

Several investigations have confirmed that diabetes mellitus and obesity are associated with a high incidence of postoperative complications (27-29). For example, Tsai et al. (28) suggested that diabetes mellitus is related to a high risk of septicemia and acute renal failure in HCC patients after hepatectomy. Luo et al. (30) confirmed that preoperative diabetes mellitus was associated with postoperative liver failure in patients after hepatectomy. Recently, a meta-analysis performed by Liu et al. (31) confirmed that obesity could increase the risk of postoperative complications, surgical site infections and intraoperative open conversion for patients with liver tumors following laparoscopic hepatectomy. Some investigators have even suggested that obesity adversely affects the postoperative outcomes of HCC patients following hepatectomy (32). Moreover, several studies have revealed that high blood pressure and dyslipidemia are associated with a high risk of cardiovascular and cerebrovascular accidents (33,34). Recently, Qiu et al. (33) reported that the more metabolic syndrome risk factors patients had, the less likely they were to achieve textbook outcomes after hepatectomy in HCC patients.

Many studies have also suggested that several metabolic risk factors, such as diabetes mellitus and obesity, negatively impact the oncological outcomes of patients with HCC after hepatectomy (35,36). Zhang et al. (37) suggested that diabetes mellitus was an independent risk factor for the incidence of MVI, which is a strong risk factor for recurrence. Shinkawa et al. (38) reported that the coexistence of obesity and diabetes mellitus increased late recurrence and worsened outcomes in HCC patients after hepatectomy. Moreover, we confirmed that concurrent cardiometabolic risk factors increase the risk of postoperative complications. Many studies have suggested that postoperative complications can increase the risk of postoperative recurrence and mortality (39,40).

In accordance with the guidelines, the diagnosis of MASLD was based on the presence of hepatic steatosis and at least one cardiometabolic risk factor (8,41). Although all confirmed MASLD patients had at least one risk factor, not all patients with metabolic abnormalities had hepatic steatosis. Moreover, the influence of hepatic steatosis on the prognosis of patients who receive hepatectomy is under debate (42,43). van Keulen et al. confirmed that hepatic steatosis did not increase the risk of postoperative complications or 90-day mortality for patients who underwent major hepatectomy (42). Mahlmann et al. also suggested that hepatic steatosis did not contribute to postoperative complications (43). Some studies have even suggested that compared with patients without hepatic steatosis, patients with hepatic steatosis may have better RFS and OS (44,45). This may explain why MASLD is not an independent risk factor for postoperative prognosis, whereas concurrent metabolic burden is.

There are several limitations in this study. As a retrospective study, some clinical data were unavailable. For example, abdominal circumference is not routinely measured in many Chinese centers. However, abdominal circumference is among the very important criteria for diagnosing overweight and obesity. Although we referred to other published studies and used the CT measurement method to calculate the abdominal circumference, there might still be some errors. Moreover, we do not know whether controlling MASLD and its associated metabolic burden would improve the prognosis of patients. However, this is a very interesting issue that is worth exploring in future research. Furthermore, although the diagnosis of MASLD is generally similar across different guidelines, some differences still exist (8,41). Since all the participants in our study came from China, the diagnostic criteria for MASLD in this study were based on Chinese guidelines.

Conclusions

Our study confirmed that concurrent MASLD neither increased the risk of postoperative complications nor affected the long-term prognosis of HCC patients after hepatectomy. However, different from concurrent MASLD, we confirmed that metabolic burden could affect the prognosis of HCC patients after hepatectomy. The more metabolic burden patients have, the more likely they are to have a poor prognosis after hepatectomy.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0552/rc

Data Sharing Statement: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0552/dss

Peer Review File: Available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0552/prf

Funding: This study was supported by the National Natural Science Foundation of China (No. 82572143) and the Natural Science Foundation of Sichuan province (No. 2024NSFSC0637).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jgo.amegroups.com/article/view/10.21037/jgo-2026-0552/coif). C.L. reports that this study was supported by the National Natural Science Foundation of China (No. 82572143) and the Natural Science Foundation of Sichuan province (No. 2024NSFSC0637). The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board of West China Hospital of Sichuan University (No. 2026757), and written informed consent was waived because of the retrospective study design.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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