JCOG0802/WJOG4607L study: Could segmentectomy be the standard surgical procedure in early-stage lung cancer?_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

YUAN Yonggang ¹ , MA Ge ² ,  YE Bo ³

1. Department of Thoracic Surgery, Qilu Hospital of Shandong University, Qingdao, 266035, Shandong, P. R. China;
2. Department of Respiratory Medicine, Yidu Central Hospital of Weifang, Weifang, 262512, Shandong, P. R. China;
3. Department of Thoracic Surgery, Shanghai Chest Hospital, Shanghai, 200030, P. R. China;

Corresponding author：

YE Bo, Email: yb1373@shchest.org

Keywords：

Non-small cell lung cancer; lobectomy; segmentectomy; clinical prognosis

DOI：

10.7507/1007-4848.202205027

Video：

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Lobectomy is the standard surgical procedure of non-small cell lung cancer (NSCLC). Based on parenchymal-sparing advantage, better postoperative lung function, rapid recovery and less invasiveness, segmentectomy has been widely used in early peripheral non-small cell carcinoma in recent years. But there was no randomized clinical trials confirming survival benefit of segmentectomy. Led by Asamura, the Japanese Clinical Oncology Group (JCOG) has conducted a series of studies on this topic. Ever since the presentation at the 101st Annual Meeting of the American Society of Thoracic Surgeons (AATS) in 2021, the results of JCOG0802/WJOG4607l have triggered massive debate. This study was aimed at determining whether segmentectomy was non-inferior to lobectomy in overall survival in patients with early peripheral NSCLC (tumor diameter≤2 cm and consolidation tumor ratio>0.5), and the results were published in The Lancet on 22 April 2022. The 5-year overall survival rate was higher in the segmentectomy group than that in the lobectomy group, despite a higher rate of local recurrence, suggesting that segmentectomy should be the standard surgical procedure for those patients. Results of this study provide high-level evidence-based medicine evidence for the safety and effectiveness of segmentectomy, and are expected to promote the application of segmentectomy in those patients or even more other patient populations. However, due to the increased local recurrence rate and unsatisfactory postoperative lung function, there are still problems to be solved to make segmentectomy a standard surgical procedure. This paper interprets this study, discusses its instructiveness in clinical practice and summarizes its limitations.

Citation： YUAN Yonggang, MA Ge, YE Bo. JCOG0802/WJOG4607L study: Could segmentectomy be the standard surgical procedure in early-stage lung cancer?. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(10): 1254-1259. doi: 10.7507/1007-4848.202205027 Copy

1.	Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2.	Cahan WG. Radical lobectomy. J Thorac Cardiovasc Surg, 1960, 39: 555-572.
3.	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.
4.	Oudkerk M, Liu S, Heuvelmans MA, et al. Lung cancer LDCT screening and mortality reduction— Evidence, pitfalls and future perspectives. Nat Rev Clin Oncol, 2021, 18(3): 135-151.
5.	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(4): 769-775.
6.	Asamura H, Hishida T, Suzuki K, et al. Radiographically determined noninvasive adenocarcinoma of the lung: Survival outcomes of Japan Clinical Oncology Group 0201. J Thorac Cardiovasc Surg, 2013, 146(1): 24-30.
7.	Maeyashiki T, Suzuki K, Hattori A, et al. The size of consolidation on thin-section computed tomography is a better predictor of survival than the maximum tumour dimension in resectable lung cancer. Eur J Cardiothorac Surg, 2013, 43(5): 915-918.
8.	Tsutani Y, Miyata Y, Mimae T, et al. The prognostic role of pathologic invasive component size, excluding lepidic growth, in stageⅠ lung adenocarcinoma. J Thorac Cardiovasc Surg, 2013, 146(3): 580-585.
9.	Woo T, Okudela K, Mitsui H, et al. Prognostic value of the IASLC/ATS/ERS classification of lung adenocarcinoma in stageⅠdisease of Japanese cases. Pathol Int, 2012, 62(12): 785-791.
10.	Hattori A, Matsunaga T, Takamochi K, et al. Prognostic impact of a ground glass opacity component in the clinical T classification of non-small cell lung cancer. J Thorac Cardiovasc Surg, 2017, 154(6): 2102-2110.e2101.
11.	Hattori A, Matsunaga T, Takamochi K, et al. Importance of ground glass opacity component in clinical stage ⅠA radiologic invasive lung cancer. Ann Thorac Surg, 2017, 104(1): 313-320.
12.	Suzuki K, Koike T, Asakawa T, et al. A prospective radiological study of thin-section computed tomography to predict pathological noninvasiveness in peripheral clinical ⅠA lung cancer (Japan Clinical Oncology Group 0201). J Thorac Oncol, 2011, 6(4): 751-756.
13.	Suzuki K, Watanabe SI, Wakabayashi M, et al. A single-arm study of sublobar resection for ground-glass opacity dominant peripheral lung cancer. J Thorac Cardiovasc Surg, 2022, 163(1): 289-301.e282.
14.	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.
15.	Wittekind C. 2010 TNM system: On the 7th edition of TNM classification of malignant tumors. Pathologe, 2010, 31(5): 331-332.
16.	Suzuki K, Saji H, Aokage K, et al. Comparison of pulmonary segmentectomy and lobectomy: Safety results of a randomized trial. J Thorac Cardiovasc Surg, 2019, 158(3): 895-907.
17.	Okubo Y, Yoshida Y, Yotsukura M, et al. Complex segmentectomy is not a complex procedure relative to simple segmentectomy. Eur J Cardiothorac Surg, 2021, 61(1): 100-107.
18.	Handa Y, Tsutani Y, Mimae T, et al. Surgical outcomes of complex versus simple segmentectomy for stageⅠnon-small cell lung cancer. Ann Thorac Surg, 2019, 107(4): 1032-1039.
19.	Tsutani Y, Miyata Y, Nakayama H, et al. Oncologic outcomes of segmentectomy compared with lobectomy for clinical stageⅠA lung adenocarcinoma: Propensity score-matched analysis in a multicenter study. J Thorac Cardiovasc Surg, 2013, 146(2): 358-364.
20.	Atkins BZ, Harpole DH, Jr, Mangum JH, et al. Pulmonary segmentectomy by thoracotomy or thoracoscopy: Reduced hospital length of stay with a minimally-invasive approach. Ann Thorac Surg, 2007, 84(4): 1107-1112; discussion 1112-1103.
21.	Landreneau RJ, Normolle DP, Christie NA, et al. Recurrence and survival outcomes after anatomic segmentectomy versus lobectomy for clinical stageⅠnon-small-cell lung cancer: A propensity-matched analysis. J Clin Oncol, 2014, 32(23): 2449-2455.
22.	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(12): 1788-1797.
23.	Schuchert MJ, Normolle DP, Awais O, et al. Factors influencing recurrence following anatomic lung resection for clinical stageⅠ non-small cell lung cancer. Lung Cancer, 2019, 128: 145-151.
24.	Liu S, Wang R, Zhang Y, et al. Precise diagnosis of intraoperative frozen section is an effective method to guide resection strategy for peripheral small-sized lung adenocarcinoma. J Clin Oncol, 2016, 34(4): 307-313.
25.	Villalba JA, Shih AR, Sayo TMS, et al. Accuracy and reproducibility of intraoperative assessment on tumor spread through air spaces in stage 1 lung adenocarcinomas. J Thorac Oncol, 2021, 16(4): 619-629.
26.	Keenan RJ, Landreneau RJ, Maley RH, Jr. , et al. Segmental resection spares pulmonary function in patients with stageⅠ lung cancer. Ann Thorac Surg, 2004, 78(1): 228-233.
27.	Kim SJ, Lee YJ, Park JS, et al. Changes in pulmonary function in lung cancer patients after video-assisted thoracic surgery. Ann Thorac Surg, 2015, 99(1): 210-217.
28.	Wang X, Guo H, Hu Q, et al. Pulmonary function after segmentectomy versus lobectomy in patients with early-stage non-small-cell lung cancer: A meta-analysis. J Int Med Res, 2021, 49(9): 3000605211044204.
29.	Martin-Ucar AE, Nakas A, Pilling JE, et al. A case-matched study of anatomical segmentectomy versus lobectomy for stageⅠlung cancer in high-risk patients. Eur J Cardiothorac Surg, 2005, 27(4): 675-679.
30.	Jiang T, Li M, Lin M, et al. Meta-analysis of comparing part-solid and pure-solid tumors in patients with clinical stageⅠA non-small-cell lung cancer in the eighth edition TNM classification. Cancer Manag Res, 2019, 11: 2951-2961.
31.	Aokage K, Saji H, Suzuki K, et al. A non-randomized confirmatory trial of segmentectomy for clinical T1N0 lung cancer with dominant ground glass opacity based on thin-section computed tomography (JCOG1211). Gen Thorac Cardiovasc Surg, 2017, 65(5): 267-272.
32.	Nakagawa K, Watanabe SI, Kunitoh H, et al. The Lung Cancer Surgical Study Group of the Japan Clinical Oncology Group: Past activities, current status and future direction. Jpn J Clin Oncol, 2017, 47(3): 194-199.

1. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2021, 71(3): 209-249.
2. Cahan WG. Radical lobectomy. J Thorac Cardiovasc Surg, 1960, 39: 555-572.
3. 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.
4. Oudkerk M, Liu S, Heuvelmans MA, et al. Lung cancer LDCT screening and mortality reduction— Evidence, pitfalls and future perspectives. Nat Rev Clin Oncol, 2021, 18(3): 135-151.
5. 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(4): 769-775.
6. Asamura H, Hishida T, Suzuki K, et al. Radiographically determined noninvasive adenocarcinoma of the lung: Survival outcomes of Japan Clinical Oncology Group 0201. J Thorac Cardiovasc Surg, 2013, 146(1): 24-30.
7. Maeyashiki T, Suzuki K, Hattori A, et al. The size of consolidation on thin-section computed tomography is a better predictor of survival than the maximum tumour dimension in resectable lung cancer. Eur J Cardiothorac Surg, 2013, 43(5): 915-918.
8. Tsutani Y, Miyata Y, Mimae T, et al. The prognostic role of pathologic invasive component size, excluding lepidic growth, in stageⅠ lung adenocarcinoma. J Thorac Cardiovasc Surg, 2013, 146(3): 580-585.
9. Woo T, Okudela K, Mitsui H, et al. Prognostic value of the IASLC/ATS/ERS classification of lung adenocarcinoma in stageⅠdisease of Japanese cases. Pathol Int, 2012, 62(12): 785-791.
10. Hattori A, Matsunaga T, Takamochi K, et al. Prognostic impact of a ground glass opacity component in the clinical T classification of non-small cell lung cancer. J Thorac Cardiovasc Surg, 2017, 154(6): 2102-2110.e2101.
11. Hattori A, Matsunaga T, Takamochi K, et al. Importance of ground glass opacity component in clinical stage ⅠA radiologic invasive lung cancer. Ann Thorac Surg, 2017, 104(1): 313-320.
12. Suzuki K, Koike T, Asakawa T, et al. A prospective radiological study of thin-section computed tomography to predict pathological noninvasiveness in peripheral clinical ⅠA lung cancer (Japan Clinical Oncology Group 0201). J Thorac Oncol, 2011, 6(4): 751-756.
13. Suzuki K, Watanabe SI, Wakabayashi M, et al. A single-arm study of sublobar resection for ground-glass opacity dominant peripheral lung cancer. J Thorac Cardiovasc Surg, 2022, 163(1): 289-301.e282.
14. 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.
15. Wittekind C. 2010 TNM system: On the 7th edition of TNM classification of malignant tumors. Pathologe, 2010, 31(5): 331-332.
16. Suzuki K, Saji H, Aokage K, et al. Comparison of pulmonary segmentectomy and lobectomy: Safety results of a randomized trial. J Thorac Cardiovasc Surg, 2019, 158(3): 895-907.
17. Okubo Y, Yoshida Y, Yotsukura M, et al. Complex segmentectomy is not a complex procedure relative to simple segmentectomy. Eur J Cardiothorac Surg, 2021, 61(1): 100-107.
18. Handa Y, Tsutani Y, Mimae T, et al. Surgical outcomes of complex versus simple segmentectomy for stageⅠnon-small cell lung cancer. Ann Thorac Surg, 2019, 107(4): 1032-1039.
19. Tsutani Y, Miyata Y, Nakayama H, et al. Oncologic outcomes of segmentectomy compared with lobectomy for clinical stageⅠA lung adenocarcinoma: Propensity score-matched analysis in a multicenter study. J Thorac Cardiovasc Surg, 2013, 146(2): 358-364.
20. Atkins BZ, Harpole DH, Jr, Mangum JH, et al. Pulmonary segmentectomy by thoracotomy or thoracoscopy: Reduced hospital length of stay with a minimally-invasive approach. Ann Thorac Surg, 2007, 84(4): 1107-1112; discussion 1112-1103.
21. Landreneau RJ, Normolle DP, Christie NA, et al. Recurrence and survival outcomes after anatomic segmentectomy versus lobectomy for clinical stageⅠnon-small-cell lung cancer: A propensity-matched analysis. J Clin Oncol, 2014, 32(23): 2449-2455.
22. 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(12): 1788-1797.
23. Schuchert MJ, Normolle DP, Awais O, et al. Factors influencing recurrence following anatomic lung resection for clinical stageⅠ non-small cell lung cancer. Lung Cancer, 2019, 128: 145-151.
24. Liu S, Wang R, Zhang Y, et al. Precise diagnosis of intraoperative frozen section is an effective method to guide resection strategy for peripheral small-sized lung adenocarcinoma. J Clin Oncol, 2016, 34(4): 307-313.
25. Villalba JA, Shih AR, Sayo TMS, et al. Accuracy and reproducibility of intraoperative assessment on tumor spread through air spaces in stage 1 lung adenocarcinomas. J Thorac Oncol, 2021, 16(4): 619-629.
26. Keenan RJ, Landreneau RJ, Maley RH, Jr. , et al. Segmental resection spares pulmonary function in patients with stageⅠ lung cancer. Ann Thorac Surg, 2004, 78(1): 228-233.
27. Kim SJ, Lee YJ, Park JS, et al. Changes in pulmonary function in lung cancer patients after video-assisted thoracic surgery. Ann Thorac Surg, 2015, 99(1): 210-217.
28. Wang X, Guo H, Hu Q, et al. Pulmonary function after segmentectomy versus lobectomy in patients with early-stage non-small-cell lung cancer: A meta-analysis. J Int Med Res, 2021, 49(9): 3000605211044204.
29. Martin-Ucar AE, Nakas A, Pilling JE, et al. A case-matched study of anatomical segmentectomy versus lobectomy for stageⅠlung cancer in high-risk patients. Eur J Cardiothorac Surg, 2005, 27(4): 675-679.
30. Jiang T, Li M, Lin M, et al. Meta-analysis of comparing part-solid and pure-solid tumors in patients with clinical stageⅠA non-small-cell lung cancer in the eighth edition TNM classification. Cancer Manag Res, 2019, 11: 2951-2961.
31. Aokage K, Saji H, Suzuki K, et al. A non-randomized confirmatory trial of segmentectomy for clinical T1N0 lung cancer with dominant ground glass opacity based on thin-section computed tomography (JCOG1211). Gen Thorac Cardiovasc Surg, 2017, 65(5): 267-272.
32. Nakagawa K, Watanabe SI, Kunitoh H, et al. The Lung Cancer Surgical Study Group of the Japan Clinical Oncology Group: Past activities, current status and future direction. Jpn J Clin Oncol, 2017, 47(3): 194-199.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

JCOG0802/WJOG4607L study: Could segmentectomy be the standard surgical procedure in early-stage lung cancer?

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