Does surgical margin affect recurrence and survival after pulmonary segmentectomy for cT1 lung cancer?

Introduction

Lung cancer is a major cause of cancer-related death worldwide with surgical resection remaining the gold standard of treatment for early-stage tumors. Since the recent publication of three phase III randomized controlled trial (German DRKS 00004897, JCOG 0802 and CALGB 140503 trials), pulmonary segmentectomy is now a valid alternative to lobectomy for peripherally located early-stage non-small cell lung cancer (NSCLC) of less than 2 centimeters (1-3). Thus, the latest National Comprehensive Cancer Network (NCCN) guidelines recommend considering sublobar resection in cases of peripheral T1a-bN0 NSCLC (4). However, they recommend that sublobar resection should achieve surgical parenchymal margins of more than 2 cm or greater than the diameter of the tumor. Actually, locoregional recurrence is an important issue in sublobar resection, and complete R0 resection with sufficient surgical margin is essential to prevent local recurrences. In the JCOG 0802 trial, although frozen section on the resection margins was realized intraoperatively if the resection margin was less than the tumor/margin ratio or <2.0 cm, the incidence of local recurrence was increased after segmentectomy compared to lobectomy (2). According to the recent consensus statement from the European Society of Thoracic Surgeons, the surgical margin should be of at least 1 cm or with a margin-to-tumor (M/T) diameter ratio greater than 1 in case of pulmonary segmentectomy for NSCLC (5,6). However, these recommendations are mainly based on retrospective studies including wedge resections. In addition, these articles used different measurement methods to assess surgical margin, definition of locoregional recurrence and tumor size. Moreover, recent advances in imaging and intraoperative techniques have facilitated the surgeon’s ability to achieve precise resections and complete R0 resection during pulmonary segmentectomy.

The aim of the study was to evaluate the potential correlation between the distance of the surgical margin and recurrence-free survival (RFS) and overall survival (OS), as well as the relationship between the margin-tumor ratio and RFS and OS after pulmonary segmentectomy in patients with early-stage NSCLC in recent practice. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-326/rc).

Methods

Ethical statement

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the local ethics committee (CER-VD in Lausanne, Switzerland) (referral number: N°2024-00173), which waived the need to obtain informed patient consent for the retrospective analysis.

Patients

We conducted a retrospective observational study reviewing the data of all consecutive patients who underwent a pulmonary segmentectomy with mediastinal lymph node dissection for NSCLC (adenocarcinoma, squamous cell carcinoma, large cell carcinoma) of stage cT1N0M0 [8th tumor-node-metastasis (TNM)] from January 2017 to December 2022 at the Lausanne University Hospital. Eligible patients presented no history of previous lung cancer or lung surgery, no previous chemotherapy or radiotherapy. We excluded patients that presented synchronous tumors, nodal involvement, history of prior lung surgery, combined procedures (wedge resection/lobectomy) and histology different than previously cited (carcinoid tumor, small cell lung carcinoma).

All patients received contrast enhanced thoracic computed tomography (CT) scan and a fluorodeoxyglucose (FDG)-positron emission tomography (PET) CT within 30 days prior to the surgery. All patients were individually discussed within the multidisciplinary tumor board before being referred for surgery. In patients with adequate pulmonary functions, video-assisted thoracoscopic surgery (VATS) segmentectomies were performed for lesions smaller than 2 cm in diameter and located in the outer third of the lung. Segmentectomy was also proposed for larger tumors in compromised patients that could not tolerate lobectomy due to poor pulmonary functions. In such cases, centrally located lesions could be resected by multiple segmentectomies. Tumors were staged according to the 8th edition of International Association for the Study of Lung Cancer TNM classification.

Surgical technique

Segmentectomy procedures were conducted by a team of four surgeons, each of whom had previously completed over 100 VATS lobectomies before transitioning to segmentectomy cases. Anatomical resections involved the excision of one or more pulmonary segments to ensure complete removal of the targeted lesion. All surgeries were carried out under general anesthesia with lung isolation achieved via double-lumen endotracheal intubation. A standardized three-port VATS technique was generally used, involving a utility incision at the fourth intercostal space, a 10-mm 30° thoracoscope placed anteriorly in the seventh intercostal space, and a posterior incision. Since 2018, some procedures have also utilized a single-port approach. Segmental resections were performed through precise dissection of the corresponding bronchus and associated arterial and venous branches. Bronchovascular structures were divided using either endoscopic staplers or energy-based instruments.. The intersegmental plane was typically delineated using intravenous injection of indocyanine green (ICG) (25–50 mg), visualized with near-infrared (NIR) fluorescence imaging. In cases where ICG was unavailable, the deflation-inflation method was employed to identify the segmental boundaries. The intersegmental plane was always divided using a surgical stapler. Systemic hilar and mediastinal nodal dissections were performed in all patients. We did not routinely perform frozen sections on the surgical margins to confirm R0 resection or systematically on station 12-13-14 lymph nodes, except if there was clinical suspicion of nodal infiltration. For patients who had positive lymph nodes on the frozen section, we performed a lobectomy and subsequently excluded these patients from the study. Surgical specimens were extracted through a protective bag. No techniques for preventing air leaks, such as pleural tents, buttressing material or pneumoperitoneum were used for these patients. Sealants were rarely applied and when they were, it was at the discretion of the surgeon.

The parenchymal resection margin was defined based on pathological results on a deflated lung, after cutting off the staple line. The surgical margin was considered as the smallest distance from the tumor edge to either the parenchyma, the intersegmental plane, or the bronchus.

Recurrence was confirmed by imaging such as CT or PET-CT and, if necessary, by transthoracic or bronchoscopic biopsy. Local recurrence was defined as a recurrence of a tumor with the same histology at the resection margin, in the same lobe, or in the ipsilateral hilum. Regional recurrence was characterized by the return of disease in mediastinal lymph nodes or within the same (ipsilateral) lung. In contrast, distant recurrence was defined as involvement of N3 lymph nodes, metastases to the opposite lung, pleural or pericardial dissemination, or spread to organs outside the thoracic cavity. New tumor nodules appearing in a different lobe or segment were classified as secondary primaries if they demonstrated distinct radiological features and/or pathological or molecular characteristics.

The post-operative course was managed based on our enhanced recovery after surgery (ERAS) protocol previously reported (7). All cases were discussed again after surgery in a multidisciplinary tumor board to assess the need of adjuvant chemotherapy. The follow-up consisted in chest CT scans every 3 months for the first 2 years, then every 6 months for a total of 5 years.

Data collection

Information was recorded in the authors’ electronic database and encompassed patient demographics, existing comorbid conditions, body mass index (BMI), results from cardiopulmonary function tests, tumor staging, histopathological findings, surgical details, and clinical outcomes monitored for up to 30 days post-discharge,including length of post-operative stay, readmissions, reoperations and cardiopulmonary complications. Air leak was assessed twice daily. Simple segmentectomies were defined as procedures involving the division of a single intersegmental plane, such as S6, left upper division, or lingular segmentectomies. Complex segmentectomies were defined as those requiring division of more than two intersegmental planes, including resections involving two segments.

Statistical analyses

The Kolmogorov-Smirnov and Shapiro-Wilk tests confirmed the abnormal distribution of all continuous variables. Continuous data were presented as means with standard deviations and interquartile ranges (IQRs), while categorical data were reported as counts and percentages. For statistical comparisons, normally distributed numerical variables were analyzed using the unpaired Student’s t-test, and non-normally distributed variables were assessed with the Mann-Whitney U test. Categorical variables were compared using the Chi-squared (χ²) test. All analyses were two-sided, with a significance level set at P<0.05. RFS and OS were estimated using the Kaplan-Meier method, and survival curves were compared using the log-rank test. Cox proportional hazards regression was applied to identify factors influencing OS and RFS, with univariate Cox analysis used to explore associations between clinical variables and both survival outcomes. In our analysis, we included the following variables: age, sex, forced expiratory volume in one second (FEV₁) <80%, diffusing capacity of the lung for carbon monoxide (DLCO) <80%, Charlson comorbidity index, PET uptake, CT ratio, location of the lesion (peripheral, central), single or multiple segmentectomy, simple or complex segmentectomy, lower lobe segmentectomy, resection margin, M/T ratio, pleural invasion, nodal upstaging, tumor size, number of dissected lymph nodes, histology. We did not perform a multivariate analysis, because of the small number of recurrence and death in the cohort. All data were analyzed using STATA software version 18 (StataCorp, College Station, TX, USA).

Results

In total, 291 patients (median age 69 years, sex ratio male/female: 141/150) underwent pulmonary segmentectomy for early stage cT1N0 NSCLC by VATS (n=291) with a conversion rate of 2.4% (n=7). Most patients presented cardiovascular comorbidities (50%) and decreased pulmonary function: 121 patients (42%) and 186 patients (64%) had a FEV₁ below 80%, had a diffusing capacity of the lungs for carbon monoxide DLCO below 80%, respectively (Table 1). Pure ground-glass opacity, consolidation ratio <0.5, and consolidation ratio ≥0.5 were observed in 17 (5.8%), 39 (13.4%), and 235 (80.8%) patients, respectively. Pure solid lesions were observed in 162 patients (55.6%). Lesions were located peripherally in the outer third of the lung in 73.8% of cases and predominantly distributed in the upper lobes (62.5%). Segmentectomies were performed on the left side in 139 cases (47.8%) and on the right side in 152 cases (52.2%). Single segmentectomies were performed in 183 cases (62.9%), while multiple segmentectomies were performed in 108 cases (37.1%). A total of 156 cases (53.6%) were defined as complex segmentectomies. The median number of segments resected was 1 (IQR, 1–2). The median tumor size was 15 (IQR, 10–20) mm, with 76% of tumors measuring less than 2 cm. The median number of lymph nodes removed was 7 (IQR, 4–12). The median surgical margin was 13 (IQR, 7–22) mm. In 94 cases (32%), the margin was less than 1 cm, and in 176 cases (60%), it was less than 2 cm. The M/T ratio was less than 1 in 148 cases (51%). Regarding resection margins, a complete R0 resection was achieved in 99.6% of cases. An R1 resection was reported in only 1 case (0.4%), where microscopic infiltration of a second T1mi tumor was found on the surgical margin. Visceral pleural invasion was found in 14.4% of cases.

During the post-operative course, the median post-operative hospital length of stay was 4 (IQR, 3–7) days, and the duration of chest tube drainage was 2 (IQR, 1–4) days. Regarding postoperative complications, cardiopulmonary events occurred in 63 cases (21.6%).

Survival and recurrence

During the follow-up (median: 28.4 months), 19 patients (6.5%) died and 22 patients (7.5%) presented recurrence: distant in 19 cases (6.5%), and local in 3 cases (1%) (Table 2). Additionally, 10 patients (3.4%) developed a secondary primary lung cancer. After surgery, adjuvant treatment was decided in 47 patients (16%). Completion lobectomy was performed in 4 cases: one due to a second lesion found at the resection margin (R1), one due to post-operative complications, and one where the lesion was not present in the operative specimen after definitive pathology. One completion lobectomy was performed for local recurrence 8 months after segmentectomy S1 and underwent a completion right upper lobectomy by VATS. Of the 3 cases (1%) with local recurrence, they were all pure solid tumors (tumor diameters of 12 mm and 15 and 22 mm). Two recurrences occurred near the suture line, while one was identified in an adjacent ipsilateral segment still consistent with direct extension from the primary site. The recurrence was after 27, 27, and 5 months after surgical margin respectively of 10, 20, and 30 mm. Two patients were considered ‘compromised’ (poor pulmonary function), while the other had normal pulmonary reserve.

RFS was estimated at 86% at 3 years (Figure 1). On univariate analysis, disease-free survival was significantly associated with DLCO <80% (HR =5.070; P=0.03), uptake on PET >3 (HR =4.56; P=0.006), visceral pleural invasion (HR =3.04; P=0.02), pure solid lesion (HR =5.41; P=0.007) and nodal upstaging (pN+) (HR =2.26; P=0.02) were significantly associated with local or distant recurrence. However, a margin less than 10 mm (HR =0.85; P=0.83) or an M/T ratio below 1 (HR =0.82; P=0.30) were not associated with local or distant recurrence (Table 3).

Figure 1 Kaplan Maier curve for overall survival (A) and recurrence-free survival (B) of the entire cohort (n=291).

OS was estimated at 94% at 3 years (Figure 1). On univariate analysis, a high Charlson comorbidity index >5 (HR =4.72; P=0.006), uptake >3 of FDG on PET (HR =3.15; P=0.03), visceral pleural invasion (HR =2.85; P=0.03), pure solid lesion (HR =3.76; P=0.04) and nodal upstaging (HR =3.30; P=0.003) were significantly associated with poorer survival. Neither the margin of less than 10 mm (HR =1.11; P=0.74) or an M/T ratio below 1 (HR =1.67; P=0.30) were significantly associated with poorer survival (Table 4).

Discussion

This study assesses recurrence rates and OS in patients undergoing segmentectomy for early-stage (cT1N0M0) NSCLC, with a particular emphasis on cases demonstrating narrow surgical margins (<2 or <1 cm). Our findings suggest that limited resection margins (surgical margin <10 mm or a tumor size-to-distance ratio <1) do not adversely affect mid-term outcomes or increase recurrence rates, within our relatively short median follow-up of 28.4 months, provided that a complete pathological resection is achieved. This challenges the longstanding surgical assumption regarding the necessity for optimal margin sizes, as patients undergoing segmentectomy with restricted surgical margins exhibited prognoses comparable to those with margins exceeding 2 cm.

The demographics of our patient’s cohort with a median age of 69 years and a high prevalence of cardiovascular comorbidities (50%), aligns with typical lung cancer populations characterized by older age and associated comorbidities such as smoking (8). Despite a relatively high rate of compromised pulmonary function (82% of patients with FEV₁ and/or DLCO below 80% of predicted value), most surgeries were performed using a VATS approach (99.3%), with a low conversion rate to open surgery (2.4%). These results align with existing evidence supporting the feasibility of VATS even in patients with impaired lung function, offering reduced postoperative morbidity and shorter hospital stays compared to open surgery (9).

Interestingly, 51% of patients presented with an M/T ratio below 1, yet this was not associated with significant differences in recurrence (P=0.30) or OS (P=0.65). This challenges the prevailing belief that larger surgical margins are imperative for ensuring local control and supports emerging evidence suggesting that smaller margins may still yield satisfactory oncological outcomes in carefully selected early-stage NSCLC patients (3,10). However, our findings underscore the critical importance of complete R0 resection, as even a single case of R1 resection was associated with worse outcomes.

Past studies have reported conflicting results regarding resection margin and survival outcomes (11-13). For example, as reported by Sienel et al., no local recurrence was observed in patients with resections >10 mm (13). However, 23% of patients with 10 mm margins developed a local recurrence (13). Nevertheless, in our study neither the tumor-to-margin distance nor the M/T ratio emerged as significant predictors of recurrence or survival. These observations imply that the integrity of the resection may supersede margin size as a critical determinant of prognosis, as also suggested by Maurizi et al. (14). Potential reasons for our different findings may include advanced intraoperative techniques (ICG fluorescence to define resection planes), improved imaging modalities, and a predominantly early-stage cohort with a high incidence of more indolent histology (such as adenocarcinoma).

Measurement techniques vary across studies, highlighting their inconsistencies and inherent limitations (15). In practice, the surgical margin tends to be underestimated. Discrepancies in margin measurement were noted, particularly due to lung tissue deflation during pathological examination and the assessment of margins after staple line removal, which likely resulted in an underestimation of the true margin by some millimeters. Additional variability arose from differences between microscopic and macroscopic measurements, and inconsistencies between radiologic and pathologic assessments. We performed all measurements on a deflated lung, a practice that reflects current trends among surgeons in most centers specializing in oncological thoracic surgery. Therefore, both factors—the deflated lung measurements and the exclusion of tissue lined with surgical clips—likely contribute to explaining our findings.

Moreover, although segmentectomies demonstrating favorable oncologic outcomes in this study, factors such as high PET uptake, low DLCO, pleural invasion, and nodal upstaging were associated with increased recurrence and poorer OS, highlighting their importance as markers of aggressive tumor biology or advanced disease (16,17). In such contexts, more intensive and regular follow-up should be considered to promptly detect and address potential recurrences.

Among our cases, invasive adenocarcinoma was present in 73%, predominantly at the pT1b stage, with a nodal upstaging rate of 4.8%. All patients with nodal involvement received adjuvant systemic therapy, in accordance with current treatment guidelines. Most recurrences, particularly distant metastases, were observed within 2 years post-treatment, which aligns with recurrence patterns documented in other studies (18).

Although completion lobectomy can be technically challenging due to adhesions and fibrosis, thoracoscopic techniques remain viable options, with thoracotomy reserved for specific cases (19,20). In our experience, we performed this procedure in four cases, all successfully completed via VATS.

The observed postoperative complication rates, predominantly cardiovascular (21.6%), are consistent with other series, emphasizing the necessity for meticulous perioperative management, especially in patients with pre-existing cardiovascular conditions (21). The relatively low re-hospitalization rate (3.4%) suggests effective management of these complications.

This study presented several limitations. In any case, preoperative images were utilized to ascertain the feasibility of resectability and the potential to perform a segmentectomy with an adequate safety margin from surrounding tissue. Many patients for whom segmentectomy was technically feasible, but where the surgical margin was considered borderline by the surgeons, were likely proceeded with lobectomy instead. However, due to the retrospective nature of this study, this aspect could not be analyzed. This study, while insightful, is also limited by its retrospective design and single-institution scope, potential measurement biases concerning the surgical margins, and the absence of data on air space spread, a recognized risk factor for recurrence. However, the findings pertain to a cohort with small, peripheral tumors, typically characterized by more indolent biological behavior. Thus, these results might not be applicable to patients with larger or more aggressive tumors, where achieving wider surgical margins is crucial for optimal outcomes. The low recurrence rate may also be influenced by the prevalence of low-grade histology adenocarcinomas within our cohort. Additionally, the follow-up duration might have been insufficient to capture late recurrences, and a 15% loss to follow up further limits the study’s conclusions. In fact, long-term follow-up is crucial not only for monitoring recurrences but also for assessing the potential development of new primary tumors, which constitute a well-recognized risk in patients with a history of NSCLC. Furthermore, frozen section analysis of stations 10 and 11 was not routinely performed, potentially affecting staging accuracy. Lymphatic invasion was not systematically reported with immunohistochemistry in all cases.

Conclusions

While ensuring clear surgical margins remains crucial, the precise size of the margin may be less significant than previously thought in midterm analysis, as long as a complete R0 resection is achieved, particularly when assessed on the deflated surgical specimen. However, future research is imperative to confirm these observations and guide best practices.

Acknowledgments

The manuscript was presented as poster at the annual ESTS meeting in Barcelona in June 2024.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-326/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-326/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2025-326/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-2025-326/coif). M.G. reports payment from Ethicon, Medela (to institution). 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 local ethics committee (CER-VD in Lausanne, Switzerland) (referral number: N°2024-00173), which waived the need to obtain informed patient consent for the retrospective analysis. The CER-VD is the ethical commission of the region of Vaud (VD) (the region of Lausanne). It is the commission that delivers the authorization for the Lausanne University Hospital.

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/.

References

1. Stamatis G, Leschber G, Schwarz B, et al. Survival outcomes in a prospective randomized multicenter Phase III trial comparing patients undergoing anatomical segmentectomy versus standard lobectomy for non-small cell lung cancer up to 2 cm. Lung Cancer 2022;172:108-16. [Crossref] [PubMed]
2. Saji H, Okada M, Tsuboi M, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer (JCOG0802/WJOG4607L): a multicentre, open-label, phase 3, randomised, controlled, non-inferiority trial. Lancet 2022;399:1607-17. [Crossref] [PubMed]
3. Altorki NK, Wang X, Wigle D, et al. Perioperative mortality and morbidity after sublobar versus lobar resection for early-stage non-small-cell lung cancer: post-hoc analysis of an international, randomised, phase 3 trial (CALGB/Alliance 140503). Lancet Respir Med 2018;6:915-24. [Crossref] [PubMed]
4. Riely GJ, Wood DE, Ettinger DS, et al. Non-Small Cell Lung Cancer, Version 4.2024, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw 2024;22:249-74. [Crossref] [PubMed]
5. Kim DH, Na KJ, Park IK, et al. Long-Term Outcomes in Stage I Lung Cancer After Segmentectomy with a Close Resection Margin. J Chest Surg 2021;54:361-8. [Crossref] [PubMed]
6. Riquet M, Achour K, Foucault C, et al. Microscopic residual disease after resection for lung cancer: a multifaceted but poor factor of prognosis. Ann Thorac Surg 2010;89:870-5. [Crossref] [PubMed]
7. Batchelor TJP, Rasburn NJ, Abdelnour-Berchtold E, et al. Guidelines for enhanced recovery after lung surgery: recommendations of the Enhanced Recovery After Surgery (ERAS®) Society and the European Society of Thoracic Surgeons (ESTS). Eur J Cardiothorac Surg 2019;55:91-115. [Crossref] [PubMed]
8. Owonikoko TK, Ragin CC, Belani CP, et al. Lung cancer in elderly patients: an analysis of the surveillance, epidemiology, and end results database. J Clin Oncol 2007;25:5570-7. [Crossref] [PubMed]
9. Scott WJ, Allen MS, Darling G, et al. Video-assisted thoracic surgery versus open lobectomy for lung cancer: a secondary analysis of data from the American College of Surgeons Oncology Group Z0030 randomized clinical trial. J Thorac Cardiovasc Surg 2010;139:976-3. [Crossref] [PubMed]
10. Okada M, Koike T, Higashiyama M, et al. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg 2006;132:769-75. [Crossref] [PubMed]
11. El-Sherif A, Fernando HC, Santos R, et al. Margin and local recurrence after sublobar resection of non-small cell lung cancer. Ann Surg Oncol 2007;14:2400-5. [Crossref] [PubMed]
12. Masai K, Sakurai H, Sukeda A, et al. Prognostic Impact of Margin Distance and Tumor Spread Through Air Spaces in Limited Resection for Primary Lung Cancer. J Thorac Oncol 2017;12:1788-97. [Crossref] [PubMed]
13. Sienel W, Stremmel C, Kirschbaum A, et al. Frequency of local recurrence following segmentectomy of stage IA non-small cell lung cancer is influenced by segment localisation and width of resection margins--implications for patient selection for segmentectomy. Eur J Cardiothorac Surg 2007;31:522-8. [Crossref] [PubMed]
14. Maurizi G, D'Andrilli A, Ciccone AM, et al. Margin Distance Does Not Influence Recurrence and Survival After Wedge Resection for Lung Cancer. Ann Thorac Surg 2015;100:918-25. [Crossref] [PubMed]
15. Nagano M, Sato M. Impact of surgical margin after sublobar resection of lung cancer: a narrative review. J Thorac Dis 2023;15:5750-9. [Crossref] [PubMed]
16. Liu J, Dong M, Sun X, et al. Prognostic Value of 18F-FDG PET/CT in Surgical Non-Small Cell Lung Cancer: A Meta-Analysis. PLoS One 2016;11:e0146195. [Crossref] [PubMed]
17. Rivera MP, Mehta AC, Wahidi MM. Establishing the diagnosis of lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest 2013;143:e142S-65S.
18. Demicheli R, Fornili M, Ambrogi F, et al. Recurrence dynamics for non-small-cell lung cancer: effect of surgery on the development of metastases. J Thorac Oncol 2012;7:723-30. [Crossref] [PubMed]
19. Meacci E, Refai M, Nachira D, et al. Uniportal Video-Assisted Thoracoscopic Surgery Completion Lobectomy Long after Wedge Resection or Segmentectomy in the Same Lobe: A Bicenter Study. Cancers (Basel) 2024;16:1286. [Crossref] [PubMed]
20. Takahashi Y, Miyajima M, Tada M, et al. Outcomes of completion lobectomy long after segmentectomy. J Cardiothorac Surg 2019;14:116. [Crossref] [PubMed]
21. Ichinokawa H, Takamochi K, Fukui M, et al. Surgical results and prognosis of lung cancer in elderly Japanese patients aged over 85 years: comparison with patients aged 80-84 years. Gen Thorac Cardiovasc Surg 2021;69:67-75. [Crossref] [PubMed]