The impact of preoperative percutaneous transthoracic needle biopsy on pleural recurrence in clinically early-stage non-small cell lung cancer

Introduction

The diagnosis of early-stage non-small cell lung cancer (NSCLC) typically involves screening with chest computed tomography (CT), followed by surgical resection (1,2). The presence of lung tumor nodules can be identified using high-resolution chest CT scans. Furthermore, CT scans can predict lung cancer with high accuracy without the need for a pathological examination (3,4). Recent studies have focused on the accuracy of noninvasive methods for diagnosing lung cancer using artificial intelligence, achieving accuracy rates exceeding 80% even for pathological subtypes (5,6). Percutaneous transthoracic needle biopsy (PTNB) is commonly used for accurate pathological assessment before surgery, especially for peripheral lesions (7). The importance of pre-surgical pathological diagnosis has grown, particularly for patients who are unsuitable for surgery or those who require neoadjuvant therapy (8). In cases of early lung cancer, obtaining a pathological diagnosis is crucial for addressing legal issues and evaluating treatment plan prior to surgery. However, approximately 10–20% of lung cancer cases result in the unsuccessful collection of sufficient tissue for pathological examination, which leads to diagnostic uncertainty (9). As a result, many cases proceed to surgery without confirmed diagnoses (7,9).

Although PTNB is generally considered a safe diagnostic procedure, it is not without risks. Complications have been reported, including a rare but serious risk of tumor seeding, with rates ranging from 0.06% to 0.2% which can lead to pleural metastasis (10-14). Previous research on the relationship between PTNB and pleural seeding has produced inconsistent findings. Many of these studies have relied on pathological staging to select patients, which may not accurately represent the conditions typically seen in clinical practice (15,16). Consequently, this study seeks to determine whether PTNB increases the risk of pleural recurrence in patients with clinical stage I NSCLC. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-850/rc).

Methods

Study design and patients

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Institutional Review Board of Seoul National University Hospital (IRB No. E-2312-136-1496) and individual consent for this retrospective analysis was waived.

Between January 2018 and December 2020, this study included cases in Seoul National University Hospital of clinical stage I NSCLC that underwent curative surgical resection. The exclusion criteria were metastatic lesions prior to surgery and cases requiring pneumonectomy. A total of 1,733 cases were enrolled, which included 115 cases with a history of lung cancer surgery. Cases of double primary lung cancer that met the Martini and Melamed criteria were also included (17). Tumor staging was determined using the eighth edition of the American Joint Committee on Cancer tumor-node-metastasis (TNM) Staging Manual (18).

Diagnostic procedure of PTNB

According to the National Comprehensive Cancer Network (NCCN) guidelines for the evaluation of pulmonary nodules, tissue diagnosis should be considered when a solid or subsolid nodule suspicious for malignancy measures ≥8 mm, especially if the solid component is present. The recommended diagnostic approach—whether surgical or non-surgical biopsy—should be selected based on lesion characteristics, patient comorbidities, and multidisciplinary evaluation of risks and benefits (19).

At our institution, based on the NCCN guidelines, PTNB is frequently chosen for peripheral lesions with adequate access and solid morphology, particularly when bronchoscopy is not feasible. Although surgical biopsy with intraoperative frozen section is an alternative, several factors influence the decision to proceed with PTNB. These include patient preference (e.g., reluctance to undergo surgery without a confirmed diagnosis), the referring physician’s judgment, concerns regarding potential medicolegal implications of operating without pathological confirmation, and logistical considerations. Conversely, in patients with very early-stage disease where PTNB is technically challenging or not feasible, surgical resection with intraoperative diagnosis may be performed following informed consent.

Assessment of recurrence

Regular clinical visits, including postoperative chest CT scans, were conducted every 6–12 months for at least 5 years after surgery to monitor for recurrence. Pleural recurrence was identified as the appearance of new pleural nodules, malignant pleural effusion, or both in the ipsilateral hemithorax at the time of the first recurrence. Isolated pleural recurrence refers to the presence of pleural nodules or pleural effusions in the ipsilateral hemithorax without any other form of recurrence. Concomitant pleural recurrence involves any pleural recurrence, whether in the ipsilateral or contralateral hemithorax, accompanied by any other type of recurrence. Locoregional recurrence was defined as a recurrence at the resection margin of the lung parenchyma, bronchus, or lymph node enlargement on the ipsilateral side of the previous cancer. All other types of recurrence were categorized as distant recurrence. Both locoregional and distant recurrences, along with any pleural recurrence, were classified as all recurrence. Recurrence was confirmed through biopsy or cytology. In cases where these procedures were not available, an increase in the size and number of metastatic nodules on follow-up CT or high uptake on positron emission tomography-CT scans was considered indicative of recurrence.

The primary endpoint was cumulative incidence rate for each type of recurrence (isolated pleural recurrence and all recurrence). Secondary endpoint was overall survival (OS).

Statistical analysis

Continuous variables were compared using Student’s t-test, while categorical variables were analyzed using Pearson’s Chi-squared test or Fisher’s exact test. The normality of the continuous variables was analyzed by using both Shapiro-Wilk test and Kolmogorov-Smirnov analysis. Propensity scores were calculated using a multivariate logistic regression model, which included variables such as age, gender, type of surgery, pathological type, clinical tumor (T) stage, pathological tumor size, and the presence of lymphatic or visceral pleural invasion (VPI). Propensity score matching (PSM) was conducted at a 1:1 ratio with a caliper value of 0.13, and a standardized mean difference of less than 0.10 was used to ensure balance between groups. We have evaluated the appropriateness of PSM by area under curve metric. Area under curve value was 0.77 which is over 0.7 meaning the propensity score model was well analyzed (Figure S1).

Fine-Gray subdistribution hazard models were utilized to identify risk factors for recurrence and competing events, both before and after PSM. For isolated pleural recurrence, competing events included all other types of recurrence and death. For overall recurrence, the competing event was death. The cumulative incidence of recurrence was analyzed using Gray’s test, while OS was estimated using the Kaplan-Meier method with the log-rank test. All statistical analyses were performed using SPSS (version 26.0; IBM-SPSS Inc.) and R (version 4.0.2; http://www.R-project.org). A two-sided approach was adopted for all analyses, with statistical significance set at P<0.05.

Results

Baseline characteristics

Of the 1,733 cases treated surgically for stage I NSCLC, 699 (40.3%) underwent PTNB prior to surgery, while 1,034 (59.7%) underwent either a bronchoscopy biopsy (n=142, 13.7%) before surgery or an intraoperative wedge resection biopsy (n=892, 86.3%) during the operation before the curative resection. The clinical and pathologic characteristics of the PTNB and non-PTNB groups are summarized in Table 1. The PTNB group was older, with an average age of 66.2±9.7 years compared to 63.1±10.1 years in the non-PTNB group (P<0.001). Lobectomy was more commonly performed than sublobar resection in the PTNB group (88.3% vs. 11.7%; in the non-PTNB group, 59.5% vs. 40.5%, P<0.001). There was a significant difference in histology distribution between the groups (P<0.001). The clinical T stage was higher in the PTNB group (≥ cT1c, P<0.001), and the pathologic tumor size was larger compared to the non-PTNB group (2.5±1.0 vs. 1.8±0.9 cm, P<0.001). The incidence of VPI and lymphatic invasion was also higher in the PTNB group (33.5% vs. 13.1%, P<0.001; 32.2% vs. 11.8%, P<0.001). Out of 1,733 patients, 1,060 were included after PSM, with 530 patients from each of the PTNB and non-PTNB groups (Figure 1). After matching variables such as age, sex, type of surgery, histologic subtype, clinical T stage, pathological tumor size, and the presence of VPI and lymphatic invasion, the characteristics were well balanced between the two groups (Table 2).

Figure 1 Flow diagram of patient enrollment. NSCLC, non-small cell lung cancer; PTNB, percutaneous transthoracic needle biopsy.

Recurrence patterns and post-recurrence treatments

Among the 1,733 patients included in the study, 203 (11.7%) experienced recurrence during the follow-up period: 138 (19.7%) in the PTNB group and 65 (6.3%) in the non-PTNB group. The median interval from biopsy to the diagnosis of isolated pleural recurrence was 14.3 months [range, 7.9–61.0 months; interquartile range (IQR), 12.3–27.7 months].

Before PSM, the overall recurrence rate was significantly higher in the PTNB group compared to the non-PTNB group (19.7% vs. 6.3%, P<0.001) (Table 3). After PSM, among the 1,060 matched patients, 136 (12.8%) developed recurrence, with a significantly higher incidence in the PTNB group than in the non-PTNB group [95 (17.9%) vs. 41 (7.7%), P<0.001]. The rate of isolated pleural recurrence remained significantly higher in the PTNB group (P=0.047), whereas the incidence of concomitant pleural recurrence did not differ significantly between the two groups (P=0.62). Other recurrence patterns, including locoregional and distant metastases, were also more frequently observed in the PTNB group (Table 4). Among the 136 patients who developed recurrence, 117 (86.0%) received post-recurrence treatment. Tyrosine kinase inhibitor (TKI) therapy was administered to 28 patients (29.5%) in the PTNB group and 12 patients (29.3%) in the non-PTNB group (Table S1).

Risk factors for pleural recurrence in the matched group

Univariate analysis of recurrence types in the matched cohort is presented in Table 5. Both preoperative PTNB and the presence of VPI were significant risk factors for isolated pleural recurrence and all recurrence. The subdistribution hazard ratio (sHR) for PTNB were 3.33 [95% confidence interval (CI): 1.09–10.20; P=0.03] for isolated pleural recurrence and 2.48 (95% CI: 1.72–3.59; P<0.001) for all recurrence types. Similarly, VPI was associated with increased risk for both isolated pleural recurrence (sHR =4.66; 95% CI: 1.78–12.20; P=0.002) and all recurrence (sHR =2.56; 95% CI: 1.83–3.60; P<0.001). In addition to PTNB and VPI, other variables identified as significant risk factors for all recurrence in univariate analysis included male sex, non-adenocarcinoma histology, clinical T2a stage, larger pathological tumor size, and the presence of lymphatic invasion. However, lymphatic invasion was not a significant predictor of isolated pleural recurrence (sHR=2.39; 95% CI: 0.91–6.28; P=0.07).

Multivariate analyses are summarized in Table 6. Variables with P values <0.1 in univariate analysis or with established clinical relevance were included in the multivariate model: PTNB, VPI, and lymphatic invasion. In this model, both PTNB and VPI remained independent risk factors for isolated pleural recurrence, with sHRs of 3.74 (95% CI: 1.06–13.20; P=0.040) and 3.12 (95% CI: 1.10–8.90; P=0.03), respectively. For all recurrence types, PTNB, VPI, and lymphatic invasion were all statistically significant predictors (P<0.001 for each).

Cumulative incidence rate and OS analysis in the matched group

The 5-year cumulative incidence rate of ipsilateral pleural recurrence was 3.6% in the PTNB group and 1.0% in the non-PTNB group. This difference was statistically significant (P<0.001). Regarding all recurrences, the PTNB group exhibited a higher cumulative incidence rate compared to the non-PTNB group, which was also statistically significant (21.9% vs. 9.1% at 5 years, P<0.001) (Figure 2).

Figure 2 Cumulative incidence curve of propensity-matched groups for (A) isolated pleural recurrence and (B) all recurrence. CI, confidence interval; PTNB, percutaneous transthoracic needle biopsy.

The median follow-up period was 44.0 months, ranging from 0.2 to 70 months. Among the 1,060 matched cases, 21 patients died. There was no significant difference in OS between the groups (97.9% vs. 97.3%, P=0.43) (Figure 3).

Figure 3 Kaplan-Meier survival curve of propensity-matched groups. CI, confidence interval; PTNB, percutaneous transthoracic needle biopsy.

Subgroup analysis: low-risk groups

A subgroup analysis was performed to evaluate the impact of PTNB in patients considered to be at low risk for pleural recurrence. This group was defined as patients without VPI or lymphatic invasion. After excluding cases with either VPI or lymphatic invasion, 332 patients in the PTNB group and 810 in the non-PTNB group were eligible for analysis.

Baseline characteristics in this subgroup differed between the two groups in several variables, including age, surgical procedure, histologic subtype, clinical T stage, and pathological tumor size. Patients in the PTNB group were generally older, underwent fewer sublobar resections, had a higher proportion of non-adenocarcinoma histology, presented with higher clinical T stage, and had larger pathologic tumors compared to those in the non-PTNB group (Table 7).

Following PSM, 320 patients remained in each group, with balanced baseline characteristics across variables (Table 8).

Univariate and multivariate Fine-Gray subdistribution hazard models were applied to identify risk factors for recurrence. In the univariate analysis, PTNB remained a significant independent risk factor for isolated pleural recurrence (sHR =2.29; 95% CI: 1.19–4.38; P=0.01), along with pathologic tumor size (sHR =1.86; 95% CI: 1.50–2.30; P<0.001). Similar associations were observed for all recurrence types: PTNB (sHR =2.13; 95% CI: 1.13–4.01; P=0.01) and tumor size (sHR =1.80; 95% CI: 1.42–2.28; P<0.001) were both significant predictors (Table 9). Due to the low incidence of isolated pleural recurrence in this subgroup (n=5, 0.8%), clinical T stage could not be included in the final regression model (Table S2).

For the final multivariate model, clinically relevant variables were included: PTNB, histologic subtype, and pathologic tumor size. PTNB, non-adenocarcinoma histology, and larger tumor size were all independently associated with both isolated pleural recurrence and all types of recurrence (all P<0.001) (Table 10).

Discussion

This study demonstrates a potential association between preoperative PTNB and an increased risk of isolated pleural recurrence in patients with clinical stage I NSCLC. While PTNB remains an important diagnostic tool—particularly for peripheral lung nodules—its possible role in iatrogenic tumor dissemination warrants further attention, especially when curative-intent resection is already planned.

Lung cancer diagnosis has increasingly relied on high-resolution CT, with surgical decisions frequently made based on radiologic findings (1-3). Pathologic confirmation via PTNB is often reserved for patients with ambiguous imaging findings or for those deemed medically inoperable (20-22). However, even in patients who are surgical candidates, tissue confirmation is sometimes pursued to guide preoperative treatment planning. Despite its reported diagnostic accuracy of up to 90%, PTNB has a failure rate of around 9%, which may be even higher in early-stage, small, or subsolid nodules (7,9). Consequently, there has been growing interest in noninvasive diagnostic approaches, including the use of artificial intelligence and radiomics, which have demonstrated promising accuracy in identifying malignancy and histologic subtypes (4-6).

Although PTNB is considered a safe procedure with a low complication rate (9), a critical concern is the potential for tumor cell dissemination into the pleural cavity via the needle tract (10-16). While rare, pleural seeding has been reported, and several retrospective studies have suggested an association between PTNB and pleural metastasis (15,16). These studies, however, have largely relied on pathologic staging and may not fully reflect real-world clinical practice where decisions are made based on clinical staging. In our study, we focused exclusively on patients who underwent curative-intent resection and evaluated outcomes based on clinical staging.

We observed that the PTNB group had more advanced clinical T stage, larger tumors, and higher incidences of VPI and lymphatic invasion. These characteristics could partially explain the higher recurrence rates. Given that PTNB is typically performed for peripheral lesions, the higher VPI rate in this group may reflect anatomic proximity to the pleura. Prior research, including work by Inoue et al. (12), has suggested that subpleural location may itself be a risk factor for pleural recurrence.

To address these baseline differences, we performed rigorous PSM. Even after adjustment, PTNB remained a significant risk factor for isolated pleural recurrence. Additionally, in a separate subgroup analysis of patients without VPI or lymphatic invasion—considered a low-risk population—PTNB was still associated with increased risk of both isolated and overall recurrence. This supports the hypothesis that PTNB itself may play a role in localized tumor seeding. However, given the low incidence of isolated pleural recurrence, these findings should be interpreted with caution.

Interestingly, despite a higher recurrence rate in the PTNB group, OS did not differ significantly between groups. This discrepancy may be explained by the effectiveness of post-recurrence treatment. Among patients who experienced recurrence, the majority received systemic therapies such as chemotherapy or TKIs, which likely mitigated the impact of recurrence on long-term outcomes (23).

Pleural recurrence is generally considered a manifestation of systemic disease, often resulting from lymphatic spread or direct pleural invasion (24-26). In contrast, PTNB-related recurrence may reflect a distinct, iatrogenic mechanism of local dissemination. Our findings suggest that VPI is associated with both isolated and concomitant pleural recurrence, likely reflecting biologically aggressive disease. Meanwhile, isolated pleural recurrence after PTNB may result from direct mechanical seeding rather than systemic progression.

Nevertheless, the evidence for a direct causal relationship between PTNB and pleural recurrence remains circumstantial. The rarity of this event, coupled with the retrospective nature of our study, precludes definitive conclusions. While our findings highlight a potential risk, they do not negate the clinical value of PTNB, especially when non-surgical management is under consideration.

This study has several limitations. First, although PSM was employed to reduce selection bias, residual confounding remains possible. Second, procedural details of PTNB, such as needle size, number of passes, or operator experience, were not available. Third, multiple statistical comparisons were performed without formal correction, increasing the risk of type I error. Lastly, the low incidence of isolated pleural recurrence limited the statistical power for subgroup analyses.

Conclusions

Preoperative PTNB was statistically correlated with an increased isolated pleural recurrence in clinical stage I NSCLC, even in patients without VPI or lymphatic invasion. However, the absolute incidence of this event was low, and no significant difference in OS was observed. While PTNB remains a valuable diagnostic tool, clinicians should carefully weigh its risks and benefits in patients who are already candidates for curative resection. Further prospective studies are needed to clarify the causal relationship between PTNB and pleural recurrence.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-850/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-850/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-850/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-850/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. This study was approved by the Institutional Review Board of Seoul National University Hospital (IRB No. E-2312-136-1496) and individual consent for this retrospective analysis 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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