Completion lobectomy following segmentectomy for malignant lung tumors: a multi-institutional study of surgical feasibility, oncologic outcomes, and diagnostic challenges (ESSG-02 study)

Introduction

Anatomical segmentectomy is increasingly performed for early-stage non-small cell lung cancer (NSCLC), particularly in patients with small peripheral tumors or compromised pulmonary function (1-3). As this lung-sparing approach becomes more widely adopted, the number of segmentectomy procedures has steadily increased (4-6).

Despite advances in surgical techniques, local recurrence at the segmental resection margin remains a clinical concern (7). In certain situations, such as when recurrence occurs at the resection margin or when a new lesion develops in the same lobe, completion lobectomy (CL) may be necessary. Performing CL after segmentectomy can be technically demanding because of postoperative adhesions and altered hilar anatomy (8-11). Although some reports have described the feasibility of CL in this setting, these are mostly limited to small, single-institution studies, and the overall evidence remains insufficient (8,12-15).

To address this gap, we conducted a multi-institutional study to evaluate the technical feasibility, perioperative outcomes, and long-term oncologic prognosis of CL following anatomical segmentectomy. We present this article in accordance with the STROBE reporting checklist (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1099/rc).

Methods

Study design

This retrospective multicenter study was conducted within the framework of the Extended Sublobar Surgery Study Group (ESSG) and designated as the ESSG-02 study. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study protocol was approved by the Institutional Review Board (IRB) of Seirei Mikatahara General Hospital (approval No. 23-29), the central institution, and by the IRBs of 9 participating institutions: Kumamoto University (No. 2873), Nagoya City University West Medical Center (No. 60-23-0098), Hiroshima Prefectural Hospital (No. 202311-3), Kobe University (No. B230202), Gunma University Hospital [No. IRB2023-087(2158)], The University of Tokyo (No. 2023360NIe), Saiseikai Utsunomiya Hospital (No. 2023-31), Anjo Kosei Hospital (No. R23-071), and Matsusaka Municipal Hospital (No. J-255-231006-4-3). The requirement for informed consent was waived owing to the retrospective nature of the study.

The objective of this study was to assess the technical feasibility and evaluate the perioperative outcomes and long-term prognosis of CL after anatomical segmentectomy.

Patient selection

This study included patients who underwent CL after segmentectomy for malignant lung tumors between January 2000 and July 2023. The indication for CL was determined at the discretion of each participating institution, without standardized criteria across centers. Preoperative diagnosis of the lesion intended for CL, by bronchoscopy or computed tomography (CT)-guided biopsy, was performed in selected patients when feasible at each institution.

Data collection

Data were collected using the standardized Microsoft Excel case report form (CRF). Patient information was extracted from the electronic or paper medical records at each participating institution. The CRF included 33 variables, including patient demographics, indications for CL, surgical details, perioperative outcomes, and the long-term prognosis. Simple segmentectomy was defined as resection of the right S6, left S6, left upper division, or lingular segment. All other segmentectomies were classified as complex (16).

Statistical analyses

Descriptive statistics were used to summarize the patient characteristics. Continuous variables were presented as medians and ranges, and categorical variables were presented as frequencies and percentages. Overall survival (OS) after CL was estimated using the Kaplan-Meier method, with 95% confidence intervals (CIs). The primary survival analysis focused on patients who underwent CL and were pathologically diagnosed with local recurrence. OS was also analyzed in the entire cohort. In addition, a post-hoc exploratory analysis was conducted to compare the clinical and radiological characteristics between cases of local recurrence and granuloma. For this comparison, the Mann-Whitney U test was used for continuous variables and Fisher’s exact test for categorical variables.

All statistical analyses were performed using the RStudio software program (version 4.3.2; RStudio Team, Boston, MA, USA) and EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan) (17).

Results

Patient and surgical background at initial segmentectomy

Among the 26 patients who underwent CL following segmentectomy during the study period, 8 who underwent CL within 30 days [due to inadequate surgical margins (n=4) or postoperative complications (n=4)] were excluded. Therefore, 18 patients were included in the analysis.

The baseline characteristics at the time of initial segmentectomy are summarized in Table S1. Primary lung cancer was diagnosed in 14 patients (77.8%), while 4 patients (22.2%) had metastatic lung tumors.

The details of the initial segmentectomies are presented in Table 1. Right-sided segmentectomy was performed in 88.9% of cases. Simple segmentectomy was performed in 7 patients (38.9%), all involving resection of the superior segment of the lower lobe (S6). Video-assisted thoracic surgery (VATS) was performed in 5 patients (27.8%). Intersegmental plane separation included stapling in 9 patients (50.0%), electrocautery in 4 (22.2%), and a combination of both in 2 (11.1%).

Patient characteristics at CL

The patient characteristics at the time of CL are shown in Table 2. The median patient age was 70 years old, and the median interval from the initial segmentectomy to the CL was 32 months. Most patients had a preserved performance status and pulmonary function. The most common indication for CL, based on preoperative clinical diagnosis, was local recurrence at the segmental resection margin (n=13, 72.2%), followed by metachronous primary lung cancer (n=3, 16.7%), and metastatic lung tumors (n=2, 11.1%), both occurring in the same lobe.

Surgical procedures for CL

Details of the surgical procedures for the CL are summarized in Table 3. Lobectomy was performed in 17 patients (94.4%), while bilobectomy was performed in 1 patient. VATS was performed in 5 patients (27.8%) without any conversion to thoracotomy. Intrathoracic adhesions were observed in 17 (94.4%) patients. Taping of the main pulmonary artery (PA) was performed in 5 patients (27.8%), including one case in which taping was required for hemostasis after PA injury. Intraoperative injury to the PA occurred in 2 patients (11.1%), involving the interlobar PA and A7. Extensive pulmonary parenchymal injury during adhesion dissection occurred in two patients. The median operative time was 251 min, and the median blood loss was 198 mL.

Postoperative outcomes and the survival following CL

The postoperative outcomes following CL are summarized in Table 4. Postoperative complications occurred in 5 patients (27.8%), with prolonged air leak (≥7 days) being the most common. One patient developed empyema that required open-window thoracostomy. The median duration of chest drainage was three days, and the median postoperative hospital stay was 8 days. No 30-day mortalities occurred.

Pathological diagnoses after CL included local recurrence in 9 patients (50.0%), metachronous primary lung cancer in 5 (27.8%), and granuloma in 4 (22.2%). Among the 13 patients clinically diagnosed with local recurrence prior to CL, 3 (23.1%) were ultimately diagnosed with granuloma.

The Kaplan-Meier survival curve for patients who underwent CL and were pathologically diagnosed with local recurrence (n=9) is shown in Figure 1. The 5-year OS rate was 58.3% (95% CI, 18.0–84.4%), and the median OS was 87.2 months (95% CI, 17.0–not reached). The survival curve for the entire cohort (n=18) is shown in Figure S1. No deaths occurred among patients with metachronous primary lung cancer (n=5) or granuloma (n=4) during the follow-up period, resulting in a 5-year OS of 100% for both groups.

Figure 1 Overall survival after completion lobectomy for local recurrence. CI, confidence interval; CL, completion lobectomy; OS, overall survival.

At the time of the analysis, 13 patients (72.2%) were alive, and 5 (27.8%) had died. Among the deceased patients, 4 had undergone CL for local recurrence of primary lung cancer and subsequently developed systemic metastases. The remaining patient died of coronavirus disease 2019 (COVID-19).

A comparison of clinical and radiological features between local recurrence and granuloma

A post-hoc exploratory comparison was conducted between patients with true local recurrence (n=10) and those with granuloma (n=3) among 13 patients clinically diagnosed with local recurrence prior to CL. The clinical and radiological characteristics are compared in Table 5.

In the local recurrence group, 5 patients (50.0%) had a preoperative pathological diagnosis confirmed by CT-guided biopsy, whereas none in the granuloma group had a confirmed preoperative diagnosis. All patients with granuloma underwent intersegmental division using staplers during the initial segmentectomy. The tumor morphology on CT was nodular in all patients with local recurrence. In the granuloma group, 1 patient (33.3%) showed temporary tumor shrinkage on follow-up CT. The median interval from the appearance of the lesion to the performance of CL at the segmentectomy margin was 3 months in the local recurrence group and 11 months in the granuloma group. The median standardized maximum uptake value (SUVmax) on positron emission tomography (PET)-CT was 2.5 in the local recurrence group and 5.4 in the granuloma group.

Discussion

In this multi-institutional study, CL following segmentectomy was associated with a higher incidence of intraoperative PA injury and postoperative complications than standard lobectomy, consistent with previous reports (18,19). However, there was no perioperative mortality, and the 5-year OS rate was 58.3%, with a median OS of 87.2 months in patients with local recurrence confirmed after CL. These findings suggest that CL can be performed safely and may provide encouraging long-term outcomes.

A summary of previous reports on CL after segmentectomy is presented in Table 6. To our knowledge, this is the largest multi-institutional study thus far to focus specifically on CL in this context. With appropriate patient selection, CL may be safely performed using VATS. CL can be more easily completed via VATS when initial segmentectomy does not involve dissection of the interlobar fissure (13). This is often the case in procedures such as basal segmentectomy or posterior basal (S10) segmentectomy performed via the pulmonary ligament approach. Therefore, a careful evaluation of the initial surgery is essential to determine the optimal surgical approach for CL. This includes a review of the operative procedure, surgical records, and any available video documentation.

Nevertheless, PA injury was observed in 11.1% of cases in this study, whereas previous reports have described rates of 25–30% (12-15). Therefore, there are cases in which thoracotomy should be selected over VATS, prioritizing safety rather than strictly adhering to a minimally invasive approach. Reported postoperative complication rates vary widely (10–55%) (12-15,20) and are often attributed to prolonged air leaks due to dissection of adhesions. In our study, intrathoracic adhesions were present in 94.4% of cases, highlighting the importance of meticulous dissection to avoid lung injury. When a lung injury occurs, appropriate repair is essential to prevent persistent air leakage. Notably, none of the reports, including ours, have documented perioperative mortality or prolonged hospitalization. These findings support that CL is a feasible and reasonable treatment option when performed with due attention to safety (12-15,20).

Although data on long-term prognosis remain limited, a recent report demonstrated that CL was associated with a significantly higher 5-year OS compared with non-surgical management (60.0% vs. 27.3%) (21). While that study primarily included patients who had undergone wedge resection, a comparable 5-year OS of 58.3% was observed in our patients who underwent CL for local recurrence. Taken together, these findings suggest that CL may be a viable treatment strategy after sublobar resection. However, the wide CIs of the survival estimates indicate considerable uncertainty, and the results should be interpreted with caution. Conversely, among the five patients who died in our study, four developed distant metastases despite undergoing CL for local recurrence. This underscores the importance of achieving adequate surgical margins during the initial segmentectomy.

Radiotherapy is sometimes selected as a non-surgical local treatment for patients with local recurrence. Although not limited to recurrence after segmentectomy, previous studies have reported that the 5-year OS for patients with locally recurrent NSCLC treated with radiotherapy ranges from 29.5% to 48.5%, whereas that for those treated with concurrent chemoradiotherapy ranges from 43.9% to 53.0% (22-24). Although based on limited patient numbers, outcomes with chemoradiotherapy appear more favorable than those with radiotherapy alone. Regarding safety, the incidence of radiation pneumonitis has been reported to range from 10% to 34%, mostly grade 2, while severe cases were rare and the overall tolerability was considered acceptable (25,26). Although a direct comparison between surgical and non-surgical treatments was not performed in the present study, these findings suggest that radiotherapy may serve as a potential therapeutic option for patients who are medically unfit for surgery or who decline CL.

Another important clinical issue is the differentiation between local recurrence and granuloma. In preoperative CT assessments before CL, previous reports have suggested that features such as vascular or bronchial invasion, the presence of calcification, and tumor morphology may be useful in this distinction (27-31). Although our sample size was limited, our findings were consistent with those of previous reports, suggesting that vascular or bronchial involvement and changes in tumor size over time may aid in differentiating granuloma from recurrence. Interestingly, in our cohort, granulomas demonstrated a higher SUVmax on PET-CT than in cases of recurrence, suggesting that the SUVmax may not be a reliable discriminator. This paradoxical finding may reflect inflammatory activity and macrophage accumulation within granulomatous lesions. During granuloma formation, helper T cells and macrophages produce cytokines such as interferon-γ, tumor necrosis factor-α, interleukin-4, and interleukin-13. These cytokines promote macrophage activation and aggregation, leading to enhanced glycolytic activity and fluorodeoxyglucose accumulation within these lesions (32,33). These immunometabolic mechanisms may account for the elevated SUVmax observed in benign granulomatous lesions (34-37). A preoperative diagnosis, therefore, remains essential in determining the indications for CL, rather than relying solely on PET-CT findings. At the same time, given the small number of cases in this exploratory analysis, these results should be interpreted with caution, and future prospective studies incorporating advanced imaging or molecular diagnostic techniques are needed to validate these observations.

Limitations

Several limitations of this study warrant mention. First, although cases were collected from multiple institutions, the rarity of CL inherently limits the sample size. As a result, the findings of this study should be regarded as hypothesis-generating rather than conclusive. Second, the study period spanned more than 20 years, during which significant changes occurred in understanding, techniques, and indications for segmentectomy. Consequently, there may have been variability in surgical decision-making and procedures at the time of the initial surgery, and detailed operative data were unavailable for some patients. In particular, information on surgical margin assessment during the initial segmentectomy was inconsistently available across institutions. As a result, relevant data could not be systematically collected in this study. Third, the indication for CL was determined at the discretion of each participating institution, and no standardized criteria were applied across centers, which may have introduced additional heterogeneity. In addition, surgical techniques and perioperative management for CL likely evolved over time with advances in minimally invasive approaches. However, due to the limited number of cases, subgroup analyses by surgical era or institutional volume were not feasible. Fourth, this study did not include a direct comparison between CL and non-surgical treatment modalities, such as radiation or chemotherapy. Because it was a surgeon-initiated, multi-institutional retrospective study, it was difficult to identify non-surgically treated cases across all institutions. Therefore, the superiority of CL over the other treatment options cannot be conclusively established. Future studies with larger cohorts and comparative analyses are needed to further validate the safety and efficacy of CL.

Conclusions

This study represents the largest multi-institutional investigation to date focusing on CL after segmentectomy. Although CL is associated with a higher rate of intraoperative complications than standard lobectomy, it can be performed without perioperative mortality and may offer favorable long-term outcomes. However, distinguishing local recurrence from granuloma remains a diagnostic challenge. A thorough preoperative evaluation and definitive diagnosis where possible are essential for appropriate patient selection and surgical planning.

Acknowledgments

We thank the patients, their families, and all ESSG members. We would also like to thank Dr. Yoshimasa Maniwa and Dr. Shinya Tane for their assistance in coordinating IRB approval at participating institutions. We also extend our gratitude to Ms. Rina Watanabe (Design SATO) for her assistance in designing the figures.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1099/rc

Data Sharing Statement: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1099/dss

Peer Review File: Available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1099/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tlcr.amegroups.com/article/view/10.21037/tlcr-2025-1099/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work, ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board of Seirei Mikatahara General Hospital (approval No. 23-29) and by the IRBs of the other 9 participating institutions: Kumamoto University (No. 2873), Nagoya City University West Medical Center (No. 60-23-0098), Hiroshima Prefectural Hospital (No. 202311-3), Kobe University (No. B230202), Gunma University Hospital [No. IRB2023-087(2158)], The University of Tokyo (No. 2023360NIe), Saiseikai Utsunomiya Hospital (No. 2023-31), Anjo Kosei Hospital (No. R23-071), and Matsusaka Municipal Hospital (No. J-255-231006-4-3). The requirement for informed consent was waived owing to the retrospective observational 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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