Survival outcomes of segmentectomy versus lobectomy for T1c non-small cell lung cancer: A systematic review and meta-analysis_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

XUE Xinyu ¹ , ZHAO Kai ¹ , CHEN Ningsu ¹ , LI Youping ¹ ,  YU Jiajie ^1,2

1. Research Center of Clinical Epidemiology and Evidence-Based Medicine, Chinese Evidence-Based Medicine Center, West China Hospital of Sichuan University, Chengdu, 610041, P. R. China;
2. Department of Clinical Nutrition, West China Hospital of Sichuan University, Chengdu, 610041, P. R. China;

Corresponding author：

YU Jiajie, Email: 2003xiong@163.com

Keywords：

Lobectomy; segmentectomy; stage T1c; non-small cell lung cancer; systematic review/meta-analysis

DOI：

10.7507/1007-4848.202404016

Video：

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Objective To evaluate the survival outcomes of segmentectomy versus lobectomy for T1c non-small cell lung cancer (NSCLC). Methods We searched PubMed, EMbase, Cochrane Central Register of Controlled Trials (CENTRAL), CNKI (China National Knowledge Infrastructure), and Wanfang Data, with the search time limit set from the inception of the databases to February 2024. Three researchers independently screened the literature, extracted relevant information, and evaluated the risk of bias of the included literature according to the Newcastle-Ottawa Scale (NOS). Meta-analysis was conducted using STATA 15.1. Results A total of 8 retrospective cohort studies were included, involving 7 433 patients. The NOS scores of the included studies were all ≥7 points. Patients who underwent lobectomy had significantly higher five-year overall survival (OS) rates compared to those who underwent segmentectomy (adjusted HR=1.11, 95%CI 0.99-1.24, P=0.042). Compared with lobectomy, segmentectomy showed no significant difference in adjusted three-year OS rate (adjusted HR=0.88, 95%CI 0.62-1.24) and adjusted five-year lung cancer-specific survival (adjusted HR=1.10, 95%CI 0.80-1.51, P=0.556) of patients with T1c NSCLC. Moreover, there were no differences in the five-year adjusted relapse-free survival (adjusted HR=1.23, 95%CI 0.82-1.85, P=0.319), and adverse events (OR=0.57, 95%CI 0.37-0.90, P=0.015) in the segmentectomy group were significantly less than those in the lobectomy group. Subgroup analysis based on whether patients received neoadjuvant therapy showed that among studies that excluded patients who received neoadjuvant therapy, no significant difference in 5-year adjusted OS rate was observed between the segmentectomy group and lobectomy group (adjusted HR=1.02, 95%CI 0.81-1.28, P=0.870). Conclusion Segmentectomy and lobectomy show no significant difference in long-term survival in stage T1c NSCLC patients, with segmentectomy associated with fewer postoperative complications. Further high-quality research is needed to conﬁrm the comparative efﬁcacy and safety of lobectomy and segmentectomy for T1c NSCLC patients.

Citation： XUE Xinyu, ZHAO Kai, CHEN Ningsu, LI Youping, YU Jiajie. Survival outcomes of segmentectomy versus lobectomy for T1c non-small cell lung cancer: A systematic review and meta-analysis. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2025, 32(3): 393-400. doi: 10.7507/1007-4848.202404016 Copy

1.	Kocarnik JM, Compton K, Dean FE, et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: A systematic analysis for the global burden of disease study 2019. JAMA Oncol, 2022, 8(3): 420-444.
2.	Liu X, Li R, Chen X, et al. SYT7 is a key player in increasing exosome secretion and promoting angiogenesis in non-small-cell lung cancer. Cancer Lett, 2023, 577: 216400.
3.	Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
4.	Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin, 2021, 71(1): 7-33.
5.	Hui B, Wang X, Wang X, et al. Organ preservation strategies after neoadjuvant chemoimmunotherapy in resectable non-small cell lung cancer: A multi-center retrospective cohort study. Int J Surg, 2023, 109(8): 2286-2292.
6.	Timmerman R, Paulus R, Galvin J, et al. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA, 2010, 303(11): 1070-1076.
7.	Socinski MA, Crowell R, Hensing TE, et al. Treatment of non-small cell lung cancer, stage Ⅳ: ACCP evidence-based clinical practice guidelines (2nd edition). Chest, 2007, 132(3 Suppl): 277s-289s.
8.	Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
9.	Howington JA, Blum MG, Chang AC, et al. Treatment of stageⅠandⅡ non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e278S-e313S.
10.	Shin S, Kong S, Kang D, et al. Longitudinal changes in pulmonary function and patient-reported outcomes after lung cancer surgery. Respir Res, 2022, 23(1): 224.
11.	Altorki N, Wang X, Kozono D, et al. Lobar or sublobar resection for peripheral stage ⅠA non-small-cell lung cancer. N Engl J Med, 2023, 388(6): 489-498.
12.	Romero D. Sublobar resection is non-inferior to lobectomy in very early stage NSCLC. Nat Rev Clin Oncol, 2023, 20(4): 209.
13.	Kadeetham K, Ngodngamthaweesuk M, Kantathut N, et al. Overall 5-year survival rate and disease-free survival after segmentectomy versus lobectomy in patients with non-small cell lung cancer. SAGE Open Med, 2022, 10: 20503121221142171.
14.	Aokage K, Suzuki K, Saji H, et al. Segmentectomy for ground-glass-dominant lung cancer with a tumour diameter of 3 cm or less including ground-glass opacity (JCOG1211): A multicentre, single-arm, confirmatory, phase 3 trial. Lancet Respir Med, 2023, 11(6): 540-549.
15.	Kneuertz PJ, Abdel-Rasoul M, D'Souza DM, et al. Wedge resection vs. lobectomy for clinical stage Ⅰa non-small cell lung cancer with occult lymph node disease. Ann Thorac Surg, 2023, 115(6): 1344-1351.
16.	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(10335): 1607-1617.
17.	Righi I, Maiorca S, Diotti C, et al. Oncological outcomes of segmentectomy versus lobectomy in clinical stageⅠnon-small cell lung cancer up to two centimeters: Systematic review and meta-analysis. Life (Basel), 2023, 13(4): 947.
18.	Winckelmans T, Decaluwé H, De Leyn P, et al. Segmentectomy or lobectomy for early-stage non-small-cell lung cancer: A systematic review and meta-analysis. Eur J Cardiothorac Surg, 2020, 57(6): 1051-1060.
19.	Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med, 1998, 17(24): 2815-2834.
20.	Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007, 8: 16.
21.	Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372: n71.
22.	Wang L, Ge L, You S, et al. Lobectomy versus segmentectomy in patients with stage T (>2 cm and ≤3 cm) N0M0 non-small cell lung cancer: A propensity score matching study. J Cardiothorac Surg, 2022, 17(1): 110.
23.	Hattori A, Matsunaga T, Fukui M, et al. Oncologic outcomes of segmentectomy for stage ⅠA radiological solid-predominant lung cancer >2 cm in maximum tumour size. Interact Cardiovasc Thorac Surg, 2022, 35(6): ivac246.
24.	Chan EG, Chan PG, Mazur SN, et al. Outcomes with segmentectomy versus lobectomy in patients with clinical T1cN0M0 non-small cell lung cancer. J Thorac Cardiovasc Surg, 2021, 161(5): 1639-1648.
25.	Deng B, Cassivi SD, de Andrade M, et al. Clinical outcomes and changes in lung function after segmentectomy versus lobectomy for lung cancer cases. J Thorac Cardiovasc Surg, 2014, 148(4): 1186-1192.
26.	Hattori A, Matsunaga T, Takamochi K, et al. The oncological outcomes of segmentectomy in clinical-T1b lung adenocarcinoma with a solid-dominant appearance on thin-section computed tomography. Surg Today, 2016, 46(8): 914-921.
27.	Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: The role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg, 2005, 129(1): 87-93.
28.	Ogawa H, Uchino K, Tanaka Y, et al. Outcomes of segmentectomy for cT1bN0M0 lung adenocarcinoma and squamous cell carcinoma: A possible association with pathological invasion. Eur J Cardiothorac Surg, 2015, 48(1): 77-82.
29.	Fang Z, He J, Fang W, et al. Long-term outcomes of thoracoscopic anatomic resections and systematic lymphadenectomy for elderly high-risk patients with stage ⅠB non-small-cell lung cancer. Heart Lung Circ, 2016, 25(4): 392-397.
30.	Cao J, Yuan P, Wang Y, et al. Survival rates after lobectomy, segmentectomy, and wedge resection for non-small cell lung cancer. Ann Thorac Surg, 2018, 105(5): 1483-1491.
31.	Carr SR, Schuchert MJ, Pennathur A, et al. Impact of tumor size on outcomes after anatomic lung resection for stage 1A non-small cell lung cancer based on the current staging system. J Thorac Cardiovasc Surg, 2012, 143(2): 390-397.
32.	Shao S, Song G, Wang Y, et al. Selection of the surgical approach for patients with stage ⅠA lung squamous cell carcinoma: A population-based propensity score matching analysis. Front Oncol, 2022, 12: 946800.
33.	Wang W, Sun Y, Li H, et al. Surgical modality for stage ⅠA non-small cell lung cancer among the elderly: Analysis of the Surveillance, Epidemiology, and End Results database. J Thorac Dis, 2020, 12(11): 6731-6742.
34.	Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stageⅠpulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg, 1994, 107(4): 1087-1093.
35.	Whitson BA, Groth SS, Andrade RS, et al. Survival after lobectomy versus segmentectomy for stageⅠ non-small cell lung cancer: A population-based analysis. Ann Thorac Surg, 2011, 92(6): 1943-1950.
36.	Yamashita S, Tokuishi K, Anami K, et al. Thoracoscopic segmentectomy for T1 classification of non-small cell lung cancer: A single center experience. Eur J Cardiothorac Surg, 2012, 42(1): 83-88.
37.	Woo W, Lee J, Jin DH, et al. Segmentectomy quality remains important in ground-glass-dominant stageⅠ lung cancer. Thorac Cancer, 2024, 15(1): 57-65.
38.	Galanis M, Leivaditis V, Gioutsos K, et al. Segmentectomy versus lobectomy. Which factors are decisive for an optimal oncological outcome? Kardiochir Torakochirurgia Pol, 2023, 20(3): 179-186.
39.	Isaka T, Ito H, Yokose T, et al. Long-term changes in psoas muscle mass after lobectomy and segmentectomy for early-stage lung cancer. J Cachexia Sarcopenia Muscle, 2023, 14(6): 2540-2549.
40.	Cannone G, Verzeletti V, Busetto A, et al. Three-dimensional imaging-guided lung anatomic segmentectomy: A single-center preliminary experiment. Medicina (Kaunas), 2023, 59(12): 2079.
41.	Zaraca F, Kirschbaum A, Pipitone MD, et al. Prospective randomized study on the efficacy of three-dimensional reconstructions of bronchovascular structures on preoperative chest CT scan in patients who are candidates for pulmonary segmentectomy surgery: The PATCHES (prospective randomized study efficacy of three-dimensional reconstructions segmentecomy) study protocol. Trials, 2023, 24(1): 594.
42.	Hattori A, Suzuki K, Takamochi K, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer with radiologically pure-solid appearance in Japan (JCOG0802/WJOG4607L): A post-hoc supplemental analysis of a multicentre, open-label, phase 3 trial. Lancet Respir Med, 2024, 12(2): 105-116.
43.	Sim JK, Choi J, Lee SY. Perioperative immunotherapy in stageⅠB-Ⅲ non-small cell lung cancer: A critical review of its rationale and considerations. Korean J Intern Med, 2023, 38(6): 787-796.
44.	O'Brien J, Bodor JN. Perioperative immunotherapy in non-small cell lung cancer. Curr Treat Options Oncol, 2023, 24(12): 1790-1801.
45.	Zhang W, Chen S, Lin X, et al. Lobectomy versus segmentectomy for stage ⅠA3 (T1cN0M0) non-small cell lung cancer: A meta-analysis and systematic review. Front Oncol, 2023, 13: 1270030.

1. Kocarnik JM, Compton K, Dean FE, et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: A systematic analysis for the global burden of disease study 2019. JAMA Oncol, 2022, 8(3): 420-444.
2. Liu X, Li R, Chen X, et al. SYT7 is a key player in increasing exosome secretion and promoting angiogenesis in non-small-cell lung cancer. Cancer Lett, 2023, 577: 216400.
3. Aberle DR, Adams AM, Berg CD, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
4. Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin, 2021, 71(1): 7-33.
5. Hui B, Wang X, Wang X, et al. Organ preservation strategies after neoadjuvant chemoimmunotherapy in resectable non-small cell lung cancer: A multi-center retrospective cohort study. Int J Surg, 2023, 109(8): 2286-2292.
6. Timmerman R, Paulus R, Galvin J, et al. Stereotactic body radiation therapy for inoperable early stage lung cancer. JAMA, 2010, 303(11): 1070-1076.
7. Socinski MA, Crowell R, Hensing TE, et al. Treatment of non-small cell lung cancer, stage Ⅳ: ACCP evidence-based clinical practice guidelines (2nd edition). Chest, 2007, 132(3 Suppl): 277s-289s.
8. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
9. Howington JA, Blum MG, Chang AC, et al. Treatment of stageⅠandⅡ non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e278S-e313S.
10. Shin S, Kong S, Kang D, et al. Longitudinal changes in pulmonary function and patient-reported outcomes after lung cancer surgery. Respir Res, 2022, 23(1): 224.
11. Altorki N, Wang X, Kozono D, et al. Lobar or sublobar resection for peripheral stage ⅠA non-small-cell lung cancer. N Engl J Med, 2023, 388(6): 489-498.
12. Romero D. Sublobar resection is non-inferior to lobectomy in very early stage NSCLC. Nat Rev Clin Oncol, 2023, 20(4): 209.
13. Kadeetham K, Ngodngamthaweesuk M, Kantathut N, et al. Overall 5-year survival rate and disease-free survival after segmentectomy versus lobectomy in patients with non-small cell lung cancer. SAGE Open Med, 2022, 10: 20503121221142171.
14. Aokage K, Suzuki K, Saji H, et al. Segmentectomy for ground-glass-dominant lung cancer with a tumour diameter of 3 cm or less including ground-glass opacity (JCOG1211): A multicentre, single-arm, confirmatory, phase 3 trial. Lancet Respir Med, 2023, 11(6): 540-549.
15. Kneuertz PJ, Abdel-Rasoul M, D'Souza DM, et al. Wedge resection vs. lobectomy for clinical stage Ⅰa non-small cell lung cancer with occult lymph node disease. Ann Thorac Surg, 2023, 115(6): 1344-1351.
16. 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(10335): 1607-1617.
17. Righi I, Maiorca S, Diotti C, et al. Oncological outcomes of segmentectomy versus lobectomy in clinical stageⅠnon-small cell lung cancer up to two centimeters: Systematic review and meta-analysis. Life (Basel), 2023, 13(4): 947.
18. Winckelmans T, Decaluwé H, De Leyn P, et al. Segmentectomy or lobectomy for early-stage non-small-cell lung cancer: A systematic review and meta-analysis. Eur J Cardiothorac Surg, 2020, 57(6): 1051-1060.
19. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med, 1998, 17(24): 2815-2834.
20. Tierney JF, Stewart LA, Ghersi D, et al. Practical methods for incorporating summary time-to-event data into meta-analysis. Trials, 2007, 8: 16.
21. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ, 2021, 372: n71.
22. Wang L, Ge L, You S, et al. Lobectomy versus segmentectomy in patients with stage T (>2 cm and ≤3 cm) N0M0 non-small cell lung cancer: A propensity score matching study. J Cardiothorac Surg, 2022, 17(1): 110.
23. Hattori A, Matsunaga T, Fukui M, et al. Oncologic outcomes of segmentectomy for stage ⅠA radiological solid-predominant lung cancer >2 cm in maximum tumour size. Interact Cardiovasc Thorac Surg, 2022, 35(6): ivac246.
24. Chan EG, Chan PG, Mazur SN, et al. Outcomes with segmentectomy versus lobectomy in patients with clinical T1cN0M0 non-small cell lung cancer. J Thorac Cardiovasc Surg, 2021, 161(5): 1639-1648.
25. Deng B, Cassivi SD, de Andrade M, et al. Clinical outcomes and changes in lung function after segmentectomy versus lobectomy for lung cancer cases. J Thorac Cardiovasc Surg, 2014, 148(4): 1186-1192.
26. Hattori A, Matsunaga T, Takamochi K, et al. The oncological outcomes of segmentectomy in clinical-T1b lung adenocarcinoma with a solid-dominant appearance on thin-section computed tomography. Surg Today, 2016, 46(8): 914-921.
27. Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: The role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg, 2005, 129(1): 87-93.
28. Ogawa H, Uchino K, Tanaka Y, et al. Outcomes of segmentectomy for cT1bN0M0 lung adenocarcinoma and squamous cell carcinoma: A possible association with pathological invasion. Eur J Cardiothorac Surg, 2015, 48(1): 77-82.
29. Fang Z, He J, Fang W, et al. Long-term outcomes of thoracoscopic anatomic resections and systematic lymphadenectomy for elderly high-risk patients with stage ⅠB non-small-cell lung cancer. Heart Lung Circ, 2016, 25(4): 392-397.
30. Cao J, Yuan P, Wang Y, et al. Survival rates after lobectomy, segmentectomy, and wedge resection for non-small cell lung cancer. Ann Thorac Surg, 2018, 105(5): 1483-1491.
31. Carr SR, Schuchert MJ, Pennathur A, et al. Impact of tumor size on outcomes after anatomic lung resection for stage 1A non-small cell lung cancer based on the current staging system. J Thorac Cardiovasc Surg, 2012, 143(2): 390-397.
32. Shao S, Song G, Wang Y, et al. Selection of the surgical approach for patients with stage ⅠA lung squamous cell carcinoma: A population-based propensity score matching analysis. Front Oncol, 2022, 12: 946800.
33. Wang W, Sun Y, Li H, et al. Surgical modality for stage ⅠA non-small cell lung cancer among the elderly: Analysis of the Surveillance, Epidemiology, and End Results database. J Thorac Dis, 2020, 12(11): 6731-6742.
34. Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stageⅠpulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg, 1994, 107(4): 1087-1093.
35. Whitson BA, Groth SS, Andrade RS, et al. Survival after lobectomy versus segmentectomy for stageⅠ non-small cell lung cancer: A population-based analysis. Ann Thorac Surg, 2011, 92(6): 1943-1950.
36. Yamashita S, Tokuishi K, Anami K, et al. Thoracoscopic segmentectomy for T1 classification of non-small cell lung cancer: A single center experience. Eur J Cardiothorac Surg, 2012, 42(1): 83-88.
37. Woo W, Lee J, Jin DH, et al. Segmentectomy quality remains important in ground-glass-dominant stageⅠ lung cancer. Thorac Cancer, 2024, 15(1): 57-65.
38. Galanis M, Leivaditis V, Gioutsos K, et al. Segmentectomy versus lobectomy. Which factors are decisive for an optimal oncological outcome? Kardiochir Torakochirurgia Pol, 2023, 20(3): 179-186.
39. Isaka T, Ito H, Yokose T, et al. Long-term changes in psoas muscle mass after lobectomy and segmentectomy for early-stage lung cancer. J Cachexia Sarcopenia Muscle, 2023, 14(6): 2540-2549.
40. Cannone G, Verzeletti V, Busetto A, et al. Three-dimensional imaging-guided lung anatomic segmentectomy: A single-center preliminary experiment. Medicina (Kaunas), 2023, 59(12): 2079.
41. Zaraca F, Kirschbaum A, Pipitone MD, et al. Prospective randomized study on the efficacy of three-dimensional reconstructions of bronchovascular structures on preoperative chest CT scan in patients who are candidates for pulmonary segmentectomy surgery: The PATCHES (prospective randomized study efficacy of three-dimensional reconstructions segmentecomy) study protocol. Trials, 2023, 24(1): 594.
42. Hattori A, Suzuki K, Takamochi K, et al. Segmentectomy versus lobectomy in small-sized peripheral non-small-cell lung cancer with radiologically pure-solid appearance in Japan (JCOG0802/WJOG4607L): A post-hoc supplemental analysis of a multicentre, open-label, phase 3 trial. Lancet Respir Med, 2024, 12(2): 105-116.
43. Sim JK, Choi J, Lee SY. Perioperative immunotherapy in stageⅠB-Ⅲ non-small cell lung cancer: A critical review of its rationale and considerations. Korean J Intern Med, 2023, 38(6): 787-796.
44. O'Brien J, Bodor JN. Perioperative immunotherapy in non-small cell lung cancer. Curr Treat Options Oncol, 2023, 24(12): 1790-1801.
45. Zhang W, Chen S, Lin X, et al. Lobectomy versus segmentectomy for stage ⅠA3 (T1cN0M0) non-small cell lung cancer: A meta-analysis and systematic review. Front Oncol, 2023, 13: 1270030.

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Survival outcomes of segmentectomy versus lobectomy for T1c non-small cell lung cancer: A systematic review and meta-analysis

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