Survival outcomes and prognostic factors after thoracoscopic pulmonary metastasectomy for hepatocellular carcinoma: a single-center experience from Vietnam

Introduction

Hepatocellular carcinoma (HCC) is one of the most common malignancies worldwide and represents a major public health burden in Asia, particularly in countries with a high prevalence of chronic hepatitis B and C infection (1,2). Despite advances in curative treatments such as liver resection, radiofrequency ablation (RFA), and transarterial chemoembolization (TACE), extrahepatic metastasis remains a significant cause of treatment failure (3). The lung is the most frequent site of extrahepatic spread, accounting for up to 40% of metastatic events in patients with treated HCC (4).

Pulmonary metastasectomy has emerged as a potential therapeutic option in selected patients, especially those with well-controlled intrahepatic disease, adequate cardiopulmonary reserve, and limited metastatic burden (5,6). Several retrospective studies have suggested that complete resection of lung metastases may prolong survival in appropriately selected patients (7). However, the supporting evidence remains heterogeneous, and most available studies originate from Japan and South Korea (8-10). Data from Southeast Asia remain scarce, despite reported regional variations in epidemiology, hepatitis B virus (HBV) genotype distribution, and clinical characteristics of HCC across Asian countries (11).

Furthermore, the increasing use of minimally invasive thoracic surgery, particularly video-assisted thoracoscopic surgery (VATS), has transformed the approach to pulmonary metastasectomy (12). Nevertheless, real-world outcomes, prognostic factors, and survival data from high-volume centers in Vietnam have not been well documented.

This study aims to address this knowledge gap by evaluating surgical outcomes and survival after thoracoscopic resection of pulmonary metastases from HCC in a major tertiary referral center. We also analyze clinical, radiologic, operative, and biomarker-related prognostic factors associated with overall survival (OS), thereby providing new evidence relevant to patient selection and treatment optimization in this population. We present this article in accordance with the STROBE reporting checklist (available at https://vats.amegroups.com/article/view/10.21037/vats-2025-1-64/rc).

Methods

Study design and setting

This retrospective observational study was conducted at the Department of Thoracic Surgery, Cho Ray Hospital, a high-volume tertiary referral center for hepatobiliary and thoracic diseases in southern Vietnam. The study included consecutive patients who underwent thoracoscopic pulmonary metastasectomy for HCC between January 2020 and August 2024. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study protocol was approved by the Institutional Review Board of the University of Medicine and Pharmacy at Ho Chi Minh City (approval code: 24253-ĐHYD; April 2, 2024). Given the retrospective nature of the study, the requirement for informed consent was waived.

Study population

Eligible patients were identified from the institutional surgical database. Inclusion criteria were as follows:

• A confirmed diagnosis of HCC based on dynamic imaging criteria and/or histopathology;
• Radiological and/or histological evidence of a single pulmonary metastasis considered amenable to complete surgical resection
• Well-controlled intrahepatic disease, defined as the absence of active or recurrent hepatic lesions on preoperative abdominal magnetic resonance imaging (MRI);
• No evidence of extrapulmonary metastases on systemic staging;
• Adequate cardiopulmonary reserve and performance status allowing surgical intervention.

Exclusion criteria included uncontrolled intrahepatic tumors, mediastinal lymph node metastasis, diffuse pulmonary metastases not suitable for complete resection, and severe comorbid conditions contraindicating surgery.

Data collection and variables

Clinical data were extracted from medical records, including age, gender, body mass index (BMI), comorbidities, viral hepatitis status [HBV and hepatitis C virus (HCV)], and prior treatments for primary HCC (hepatectomy, RFA, TACE, or combined modalities).

Preoperative laboratory parameters included prothrombin time, total bilirubin, serum albumin, aspartate aminotransferase, and alanine aminotransferase. Pulmonary function tests included forced expiratory volume in one second (FEV1) and forced vital capacity (FVC).

Tumor characteristics and mediastinal lymph node status were assessed using contrast-enhanced chest computed tomography (CT), including maximal tumor diameter and lobe location. While positron emission tomography (PET)/CT was not routinely mandated, systemic staging was rigorously conducted, and any radiological evidence of mediastinal lymph node involvement resulted in exclusion from the surgical cohort.

Biomarker assessment

Serum tumor biomarkers: alpha-fetoprotein (AFP), alpha-fetoprotein Lens culinaris agglutinin-reactive fraction (AFP-L3), and des-gamma-carboxy prothrombin (DCP) [protein induced by vitamin K absence or antagonist-II (PIVKA-II)] were measured within one month prior to pulmonary metastasectomy. Biomarker elevation was defined as AFP ≥100 ng/mL, AFP-L3 ≥10%, and PIVKA-II ≥40 mAU/mL. Concurrent elevation of all three biomarkers was analyzed as a composite prognostic variable. Due to the small sample size, biomarker analysis primarily focused on comparing patients with concurrent elevation of all three biomarkers (triple elevation) against the rest of the cohort (which included patients with zero, one, or two elevated markers).

Disease-free interval (DFI)

The DFI was defined as the time from the initial curative treatment for HCC, or the last treatment for recurrent intrahepatic disease, to the first radiological detection of pulmonary metastasis.

Surgical procedure and perioperative outcomes

All patients underwent pulmonary metastasectomy using a thoracoscopic approach. The extent of lung resection (wedge resection or lobectomy) was determined based on tumor size, location, and the feasibility of achieving complete resection while preserving lung parenchyma. Intraoperative variables included operative time and estimated blood loss. Surgical margin status was confirmed by intraoperative frozen section analysis. Due to the parenchymal-sparing nature of the procedures and the strict preoperative exclusion of patients with suspicious lymph nodes, routine systematic intraoperative mediastinal lymphadenectomy was not performed.

Postoperative outcomes included chest tube duration, length of hospital stay, and postoperative complications. Postoperative complications were classified according to the Clavien-Dindo classification (13).

Follow-up and outcome measures

Patients were followed through regular outpatient visits. The standard institutional follow-up protocol consisted of clinical examinations, measurement of serum tumor biomarkers (AFP, AFP-L3, and PIVKA-II), and serial imaging studies specifically contrast-enhanced chest CT to monitor the thorax, alongside abdominal MRI or ultrasound to monitor for intrahepatic recurrence. These evaluations were typically performed every 3 to 6 months for the first two years postoperatively, and every 6 to 12 months thereafter, or whenever clinically indicated by symptoms or rising biomarker levels. OS was defined as the time from pulmonary metastasectomy to death from any cause or the date of last follow-up.

Statistical analysis

All statistical analyses were performed using Stata 14.2 software on a Windows (StataCorp, 2015. Stata Statistical Software: Release 14. College Station, TX, StataCorp LP). Continuous variables were assessed for normality using the Shapiro-Wilk test due to the small sample size. Normally distributed variables are summarized as mean ± standard deviation (SD), whereas non-normally distributed variables are presented as median [interquartile range (IQR)]. Differences in means between groups were compared using the t-test for normally distributed variables and the Mann-Whitney U test for non-normally distributed variables. Differences in the frequency distributions of categorical variables were assessed using the Chi-squared test (χ²) or Fisher’s exact test. OS was estimated using the Kaplan-Meier method, and differences between survival curves were compared using the log-rank test. Variables included in the survival analysis were selected based on clinical relevance and established prognostic factors identified in previous literature. These included patient demographics, primary tumor treatment, pulmonary metastasis characteristics, surgical extent, and tumor biomarker profiles. In addition, receiver operating characteristic (ROC) curve analysis was performed to determine the optimal cut-off values for continuous prognostic variables, such as DFI and tumor size, by evaluating their sensitivity and specificity in relation to survival outcomes. This process facilitated the dichotomization of these continuous variables into categorical groups for subsequent Kaplan-Meier survival estimation and log-rank comparisons. Biomarker elevation was defined a priori using established clinical thresholds. All statistical tests were two-sided, and a P value <0.05 was considered statistically significant.

Results

Baseline characteristics

Thirty-three patients met the inclusion criteria (Figure 1). The majority of patients were middle-aged males with well-preserved liver and pulmonary functions. The most common prior curative treatment for primary HCC was liver resection. Detailed demographic and clinical characteristics, including comorbidities and tumor markers, are summarized in Table 1.

Figure 1 Patient selection flow chart. HCC, hepatocellular carcinoma; VATS, video-assisted thoracoscopic surgery.

Pulmonary metastasis characteristics

On preoperative chest CT, the mean diameter of the pulmonary metastatic lesion was 2.3±0.9 cm. The metastatic lesion was most frequently peripherally located and predominantly distributed in the lower lobes. Vascular or bronchial invasion was rarely observed. Detailed tumor characteristics are provided in Table 2.

Operative and postoperative outcomes

Wedge resection was the predominant surgical approach, characterized by short operative times and minimal blood loss. Negative surgical margins were achieved in all cases. Patients experienced short hospital stays with no perioperative mortality or major complications (Table 3).

Survival outcomes

During a median follow-up of 24 months, 12 patients (36.4%) died due to disease progression. The 1-, 2-, and 3-year OS rates were 87.8%, 68.4%, and 55.9%, respectively (Figure 2).

Figure 2 Kaplan-Meier curve for overall survival. Receiver operating characteristic curve analysis was performed to determine optimal cut-off values for continuous variables associated with survival.

For DFI between initial HCC treatment and detection of pulmonary metastasis, the optimal cut-off value was 14.5 months, yielding a sensitivity of 76.2% and specificity of 75.0%, with an area under the curve (AUC) of 0.724 (95% confidence interval: 0.543–0.905; P=0.03) (Figure 3). Patients with early pulmonary metastasis (DFI <14.5 months) demonstrated significantly poorer OS compared with those with later metastasis (DFI ≥14.5 months), with mean survival times of 27.5±4.9 vs. 48.3±4.1 months, respectively (log-rank χ²=6.263, P=0.01) (Figure 4). Similarly, ROC analysis identified an optimal cut-off value for maximal pulmonary tumor diameter of 2.85 cm, with a sensitivity of 50.0% and specificity of 85.7% (AUC =0.724, P=0.03) (Figure 3). Patients with tumors ≥2.85 cm had significantly reduced survival compared with those with smaller lesions (mean survival: 26.7±6.9 vs. 42.1±3.8 months, P=0.03) (Figure 4). Additionally, an exploratory sensitivity analysis was performed applying conventional literature-based cut-off values for DFI (12 months) and maximal tumor size (3.0 cm). The survival trends remained consistent with the primary ROC-derived analysis, wherein a DFI <12 months and a tumor size >3.0 cm consistently correlated with poorer OS trajectories, thereby validating the robustness of these prognostic parameters.

Figure 3 ROC curve analysis used to determine optimal cut-off values for predicting overall survival after thoracoscopic pulmonary metastasectomy for hepatocellular carcinoma. (A) DFI. (B) Pulmonary tumor diameter. The optimal thresholds were 14.5 months for DFI and 2.85 cm for tumor diameter. DFI, disease-free interval; ROC, receiver operating characteristic.

Figure 4 Kaplan-Meier overall survival curves after pulmonary metastasectomy. (A) Stratified by disease-free interval (DFI <14.5 vs. ≥14.5 months). (B) Stratified by pulmonary tumor size (<2.85 vs. ≥2.85 cm). (C) Stratified by concurrent elevation of triple biomarkers (AFP, AFP-L3, and PIVKA-II). AFP, alpha-fetoprotein; AFP-L3, alpha-fetoprotein Lens culinaris agglutinin-reactive fraction; DFI, disease-free interval; PIVKA-II, protein induced by vitamin K absence or antagonist-II.

In addition, concurrent elevation of all three tumor biomarkers (AFP, AFP-L3, and PIVKA-II) was strongly associated with worse prognosis. Patients with triple biomarker elevation had a markedly higher mortality rate (85.7%) and shorter mean survival (20.7±5.5 months) compared with those without triple elevation (44.8±4.0 months, P=0.03) (Figure 4).

Comorbidities, viral hepatitis status, primary HCC treatment modality, and extent of pulmonary resection were not significantly associated with OS (Table 4).

Discussion

The demographic characteristics of patients undergoing pulmonary metastasectomy for HCC in our study showed a high degree of consistency with international reports as well as with the epidemiological profile of HCC in Vietnam. The mean age of the 33 patients at the time of pulmonary metastasectomy was 58.7±10.7 years, which is comparable to the mean or median ages reported in major studies: 57 years (Kitano et al., Japan), 56 years (Kuo et al., Taiwan, China), and 55.5±9.5 years (Kim et al., Korea) (14-16). Similarly, this age is also close to the mean age of the general HCC population in Vietnam (59.8±11.7 years) (17). Regarding gender distribution, our cohort showed a predominance of male patients (87.9%). This proportion is slightly higher than that reported in studies from Korea (Kim et al.) and Japan (Kitano et al.), but aligns closely with the male predominance observed in the overall HCC population in Vietnam, and is almost identical to the proportion reported by Kuo et al. in Taiwan, China (14-17). Even a previous study from Cho Ray Hospital [2015–2020] reported a similar male rate of 91.7% (18). This consistently high proportion of male patients reflects the well-recognized epidemiological pattern of HCC across Asia, where chronic HBV infection remains the predominant risk factor, resulting in a substantially higher incidence of HCC in men (17). Consequently, the demographic profile of patients selected for pulmonary metastasectomy at Cho Ray Hospital is representative of the typical HCC population in the region, thereby strengthening the generalizability of our study cohort to other centers with a similarly high HBV burden.

In our retrospective study conducted at Cho Ray Hospital, involving 33 patients who underwent pulmonary metastasectomy for HCC, the 3-year OS rate was 55.9%, while the 1-year and 2-year OS rates were 87.8% and 68.4%, respectively. These findings demonstrate a favorable mid-term survival prognosis that is comparable to other international reports on pulmonary metastasectomy for HCC for highly selected patients (15,19). For instance, a recent systematic review and meta-analysis estimated the cumulative 5-year OS after surgery to be 48% (20). Other cohort studies have reported comparable outcomes, such as the study by Kitano et al. (45 patients), which documented a 5-year OS of 40.9%, and the study by Kuo et al. (34 patients), which reported a 5-year OS of 27.5% (14,15). The notably higher survival rates observed in our study can be largely attributed to the strict patient-selection strategy employed. Our inclusion criteria required patients to have well-controlled intrahepatic disease (no evidence of recurrence on abdominal MRI), absence of extrapulmonary metastasis, and sufficient cardiopulmonary reserve to tolerate surgery. Pulmonary metastasectomy is widely accepted as a valuable therapeutic option for prolonging survival in HCC; however, its benefit is limited to appropriately selected patients (19,21).

Regarding the surgical approach, our study demonstrated a clear alignment with contemporary trends in thoracic surgery. Most pulmonary metastasectomy procedures in our study (90.9%) were performed using wedge resection via VATS. The primary objective of pulmonary metastasectomy, regardless of the surgical approach, is to achieve complete resection (R0) while preserving as much normal lung parenchyma as possible, and wedge resection remains the preferred option for peripheral lesions (15,19) The predominance of VATS in our study [similarly, 60 of 63 patients in a recent Korean series also underwent VATS (16)] reflects the widespread adoption of this technique. This trend is supported by evidence showing that VATS offers OS and disease-free survival outcomes comparable to those of open thoracotomy, while providing the added benefits of reduced postoperative pain and shorter hospital stay (19,22).

Our clinical results further reinforce this perspective; we observed a median length of hospital stay of 4 days (IQR, 3–5 days) with no major complications or mortality, which is consistent with the established safety and favorable recovery profile of VATS. The preferential use of VATS helps explain the high safety profile and rapid postoperative recovery seen in our study, consistent with the principle that minimally invasive approaches facilitate easier repeat resections—an especially important consideration for patients with chronic conditions such as cirrhosis (19).

Our study identified three major adverse prognostic factors associated with reduced OS, which closely align with those reported in the literature and reflect aggressive tumor biology. We found that a shorter time to pulmonary metastasectomy (or DFI) of less than 14.5 months was significantly associated with poorer prognosis (P=0.01). This finding is entirely consistent with previous studies, in which a short DFI (commonly <12 months) is recognized as an independent negative prognostic factor for OS (14,15). Kuo et al. [2007] similarly reported that a DFI <12 months was significantly associated with worse survival (P=0.01), as it reflects a more aggressive tumor biology and a higher likelihood of early recurrence (15). Our study demonstrated that pulmonary metastatic nodules ≥2.85 cm were associated with reduced survival (P=0.03). This result mirrors the findings of numerous studies, which commonly report smaller pulmonary metastasectomy size (often <3 cm) as a favorable prognostic factor (16,19). A recent 2024 study also identified maximal metastatic tumor diameter as a significant predictor of OS [hazard ratio (HR) 1.086, P=0.001] (16). Concurrent elevation of AFP, AFP-L3, and PIVKA-II in our study was strongly associated with poorer prognosis (P=0.03). This is consistent with findings from other studies in which elevated preoperative AFP levels (commonly ≥100 or ≥500 ng/mL) are recognized as independent adverse predictors (14,15,19,22). Likewise, a DCP level >40 mAU/mL has also been considered a negative prognostic factor for OS (14). Conversely, lower AFP levels (<100 ng/mL) after pulmonary metastasectomy have been associated with better outcomes, underscoring the notion that increased biomarker levels reflect more biologically aggressive disease (19).

Regarding the role of metastatic nodule number, while many previous studies have considered nodule count to be prognostically important-with fewer nodules generally associated with better outcomes (15,19,21). this factor could not be evaluated as a predictor in our analysis because our strict selection criteria resulted in a cohort comprising exclusively patients with a single, isolated pulmonary metastasis. Interestingly, a recent study even reported a paradoxical finding in which a greater number of metastatic nodules was associated with a reduced risk of postoperative recurrence (HR 0.491, P=0.01) (16). This highlights that the prognostic relevance of nodule count remains controversial (15).

Pulmonary metastasectomy for HCC is generally considered only in highly selected patients with favorable tumor biology, limited metastatic burden, and well-controlled intrahepatic disease. In the modern era, systemic therapies, including targeted therapy and immune checkpoint inhibitors, have significantly improved outcomes for patients with advanced HCC. Although systemic treatment remains the cornerstone for most patients with metastatic disease, several studies have suggested that surgical resection of pulmonary metastases may provide survival benefits in carefully selected cases. Therefore, pulmonary metastasectomy may represent a complementary component of a multidisciplinary treatment strategy in the current immunotherapy era.

This study has limitations inherent to its retrospective design, small sample size (n=33), although this cohort size is highly comparable to other previously published single-center series on this highly selected population and the limited number of observed events (12 deaths), which statistically precluded a robust multivariable survival analysis or stable exploratory penalized regression models. Therefore, the identified prognostic factors should be interpreted as associations rather than independent predictors and future multicenter studies employing advanced penalized modeling are required to confirm their statistical independence. Furthermore, as this study is based on a surgical database, the exact number of patients with HCC and lung metastases who were evaluated but deemed ineligible for surgery could not be accurately determined, which may introduce potential selection bias. Owing to the retrospective design of this study, the exact numerical distances of the parenchymal resection margins were not consistently documented in pathological reports, limiting our ability to analyze the impact of margin width on oncological outcomes. Due to the retrospective design and small sample size, we were unable to evaluate whether the triple biomarker profile predicts pulmonary versus systemic recurrence or to perform robust subgroup analyses of individual or partial biomarker elevations. Larger prospective studies are needed to clarify these associations and refine patient selection. Furthermore, because our study period extended up to August 2024 with a median follow-up of only 24 months, the relatively short follow-up duration precluded the evaluation of long-term oncological outcomes, such as 5-year OS, which should be addressed in future studies with extended observation periods. Finally, because many patients were managed by their local oncologists upon disease progression, detailed data regarding specific recurrence patterns (e.g., local intrapulmonary versus bilateral disease) and the incidence of re-do pulmonary operations could not be systematically analyzed, highlighting the need for future studies with comprehensive long-term tracking.

Conclusions

Pulmonary metastasectomy is a safe and effective treatment option for carefully selected patients with pulmonary metastases from HCC, yielding favorable mid-term survival outcomes. Wedge resection via VATS predominated and was associated with excellent perioperative safety. In our preliminary exploratory analysis, early pulmonary metastasis (DFI <14.5 months), larger metastatic tumor size (≥2.85 cm), and concurrent elevation of AFP, AFP-L3, and PIVKA-II demonstrated an association with significantly worse survival in univariate models. Because the small sample size precluded multivariable analysis, these variables cannot yet be established as definitive independent predictors. These exploratory findings emphasize the importance of biologically informed patient selection when considering pulmonary metastasectomy (PM) as part of a multimodal treatment strategy, warranting further validation in larger prospective cohorts.

Acknowledgments

This study was conducted in the Department of Thoracic Surgery, Cho Ray Hospital. We would like to thank the medical staff who helped with the data collection.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://vats.amegroups.com/article/view/10.21037/vats-2025-1-64/rc

Data Sharing Statement: Available at https://vats.amegroups.com/article/view/10.21037/vats-2025-1-64/dss

Peer Review File: Available at https://vats.amegroups.com/article/view/10.21037/vats-2025-1-64/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://vats.amegroups.com/article/view/10.21037/vats-2025-1-64/coif). The 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. The study protocol was approved by the Institutional Review Board of the University of Medicine and Pharmacy at Ho Chi Minh City (approval code: 24253-ĐHYD; April 2, 2024). Given the retrospective nature of the study, the requirement for informed consent was waived.

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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