Advances in indications of anatomical pulmonary segmentectomy for early-stage lung cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WU Weibing , XU Wenzheng ,  CHEN Liang

Department of Thoracic Surgery, The First Affiliated Hospital with Nanjing Medical University, Nanjing, 210029, P. R. China;

Corresponding?author：

CHEN Liang, Email: clbright0909@njmu.edu.cn

Keywords：

Segmentectomy; early-stage lung cancer; indications; tumor size; ground-glass nodule; pathological subtype; tumor location; review

DOI：

10.7507/1007-4848.202209010

Video：

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Abstract Full text Figures/Tables Video References Cited by

Whether anatomical segmentectomy can replace lobectomy in the treatment of early-stage lung cancer remains controversial. A large number of studies have been conducted for decades to explore whether pulmonary segmentectomy can treat early-stage lung cancer, which is actually to explore the indications of intentional segmentectomy. With the development of scientific researches, it is found that many characteristics affect the malignancy of lung cancer, and the different grades of each characteristic affect the prognosis of patients. It is worth exploring whether different surgical approaches can be used for early-stage lung cancer with different characteristics and different grades. This article reviews the literature and studies to discuss the advances in indications of segmentectomy for early-stage lung in terms of tumor size, consolidation-to-tumor ratio, pathological classification and tumor location, respectively. The objective of this review is to help thoracic surgeons to objectively and scientifically select the surgical method according to the clinical characteristics of early-stage lung cancer.

Citation： WU Weibing, XU Wenzheng, CHEN Liang. Advances in indications of anatomical pulmonary segmentectomy for early-stage lung cancer. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(4): 627-634. doi: 10.7507/1007-4848.202209010 Copy

1.	Churchill ED, Belsey R. Segmental pneumonectomy in bronchiectasis: The lingula segment of the left upper lobe. Ann Surg, 1939, 109(4): 481-499.
2.	Bonfils-Roberts EA, Clagett OT. Contemporary indications for pulmonary segmental resections. J Thorac Cardiovasc Surg, 1972, 63(3): 433-438.
3.	Bennett WF, Smith RA. Segmental resection for bronchogenic carcinoma: A surgical alternative for the compromised patient. Ann Thorac Surg, 1979, 27(2): 169-172.
4.	Tsutani Y, Tsubokawa N, Ito M, et al. Postoperative complications and prognosis after lobar resection versus sublobar resection in elderly patients with clinical stage Ⅰnon-small-cell lung cancer. Eur J Cardiothorac Surg, 2018, 53(2): 366-371.
5.	Brunelli A, Decaluwe H, Gossot D, et al. Perioperative outcomes of segmentectomies versus lobectomies in high-risk patients: An ESTS database analysis. Eur J Cardiothorac Surg, 2020: ezaa308.
6.	Jensik RJ, Faber LP, Milloy FJ, et al. Segmental resection for lung cancer. A fifteen-year experience. J Thorac Cardiovasc Surg, 1973, 66(4): 563-572.
7.	Jensik RJ, Faber LP, Kittle CF. Segmental resection for bronchogenic carcinoma. Ann Thorac Surg, 1979, 28(5): 475-483.
8.	Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stage Ⅰ pulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg, 1994, 107(4): 1087-1093.
9.	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.
10.	Ettinger DS, Wood DE, Aisner DL, et al. NCCN guidelines insights: Non-small cell lung cancer, version 2. 2021. J Natl Compr Canc Netw, 2021, 19(3): 254-266.
11.	Brunelli A, Charloux A, Bolliger CT, et al. ERS/ESTS clinical guidelines on fitness for radical therapy in lung cancer patients (surgery and chemo-radiotherapy). Eur Respir J, 2009, 34(1): 17-41.
12.	Lim E, Baldwin D, Beckles M, et al. Guidelines on the radical management of patients with lung cancer. Thorax, 2010, 65 Suppl 3: iii1-iii27.
13.	Brunelli A, Kim AW, Berger KI, et al. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e166S-e190S.
14.	Rami-Porta R, Bolejack V, Crowley J, et al. The IASLC lung cancer staging project: Proposals for the revisions of the T descriptors in the forthcoming eighth edition of the TNM classification for lung cancer. J Thorac Oncol, 2015, 10(7): 990-1003.
15.	Jang HJ, Lee KS, Kwon OJ, et al. Bronchioloalveolar carcinoma: Focal area of ground-glass attenuation at thin-section CT as an early sign. Radiology, 1996, 199(2): 485-488.
16.	National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
17.	Ohde Y, Nagai K, Yoshida J, et al. The proportion of consolidation to ground-glass opacity on high resolution CT is a good predictor for distinguishing the population of non-invasive peripheral adenocarcinoma. Lung Cancer, 2003, 42(3): 303-310.
18.	Kodama K, Higashiyama M, Yokouchi H, et al. Prognostic value of ground-glass opacity found in small lung adenocarcinoma on high-resolution CT scanning. Lung Cancer, 2001, 33(1): 17-25.
19.	Aoki T, Tomoda Y, Watanabe H, et al. Peripheral lung adenocarcinoma: Correlation of thin-section CT findings with histologic prognostic factors and survival. Radiology, 2001, 220(3): 803-809.
20.	Suzuki K, Asamura H, Kusumoto M, et al. "Early" peripheral lung cancer: Prognostic significance of ground glass opacity on thin-section computed tomographic scan. Ann Thorac Surg, 2002, 74(5): 1635-1639.
21.	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.
22.	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.
23.	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.
24.	Ye T, Deng L, Wang S, et al. Lung Adenocarcinomas manifesting as radiological part-solid nodules define a special clinical subtype. J Thorac Oncol, 2019, 14(4): 617-627.
25.	Yoshizawa A, Motoi N, Riely GJ, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: Prognostic subgroups and implications for further revision of staging based on analysis of 514 stage Ⅰcases. Mod Pathol, 2011, 24(5): 653-664.
26.	Russell PA, Wainer Z, Wright GM, et al. Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol, 2011, 6(9): 1496-1504.
27.	Warth A, Muley T, Meister M, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol, 2012, 30(13): 1438-1446.
28.	Clagett OT, Deterling RA, Jr. A technique for segmental pulmonary resection with particular reference to lingulectomy. J Thorac Surg, 1946, 15: 227-238.
29.	Nomori H, Okada M. Illustrated Textbook of Anatomical Pulmonary Segmentectomy. Heidelberg: Springer, 2012.
30.	Wu WB, Xu XF, Wen W, et al. Three-dimensional computed tomography bronchography and angiography in the preoperative evaluation of thoracoscopic segmentectomy and subsegmentectomy. J Thorac Dis, 2016, 8(Suppl 9): S710-S715.
31.	Wu WB, Xia Y, Pan XL, et al. Three-dimensional navigation-guided thoracoscopic combined subsegmentectomy for intersegmental pulmonary nodules. Thorac Cancer, 2019, 10(1): 41-46.
32.	Wu WB, Xu XF, Wen W, et al. Thoracoscopic pulmonary sub-subsegmentectomy based on three-dimensional images. Ann Thorac Surg, 2016, 102(5): e389-e391.
33.	Landreneau RJ, Hazelrigg SR, Ferson PF, et al. Thoracoscopic resection of 85 pulmonary lesions. Ann Thorac Surg, 1992, 54(3): 415-419.
34.	Koike T, Yamato Y, Yoshiya K, et al. Intentional limited pulmonary resection for peripheral T1 N0 M0 small-sized lung cancer. J Thorac Cardiovasc Surg, 2003, 125(4): 924-928.
35.	Okada M, Koike T, Higashiyama M, et al. Radical sublobar resectionfor small-sized non-small cell lung cancer: A multicenter study. J Thorac Cardiovasc Surg, 2006, 132(4): 769-775.
36.	Rami-Porta R, Ball D, Crowley J, et al. The IASLC Lung Cancer Staging Project: Proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol, 2007, 2(7): 593-602.
37.	Padilla J, Calvo V, Pe?alver JC, et al. Surgical results and prognostic factors in early non-small cell lung cancer. Ann Thorac Surg, 1997, 63(2): 324-326.
38.	Mulligan CR, Meram AD, Proctor CD, et al. Lung cancer staging: A case for a new T definition. Ann Thorac Surg, 2006, 82(1): 220-226.
39.	Asamura H, Goya T, Koshiishi Y, et al. How should the TNM staging system for lung cancer be revised? A simulation based on the Japanese Lung Cancer Registry populations. J Thorac Cardiovasc Surg, 2006, 132(2): 316-319.
40.	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(12): 915-924.
41.	Lee KS, Kim Y, Han J, et al. Bronchioloalveolar carcinoma: Clinical, histopathologic, and radiologic findings. Radiographics, 1997, 17(6): 1345-1357.
42.	Aquino SL, Chiles C, Halford P. Distinction of consolidative bronchioloalveolar carcinoma from pneumonia: Do CT criteria work? AJR Am J Roentgenol, 1998, 171(2): 359-363.
43.	Akira M, Atagi S, Kawahara M, et al. High-resolution CT findings of diffuse bronchioloalveolar carcinoma in 38 patients. AJR Am J Roentgenol, 1999, 173(6): 1623-1629.
44.	Nakamura K, Saji H, Nakajima R, et al. A phase Ⅲrandomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L). Jpn J Clin Oncol, 2010, 40(3): 271-274.
45.	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.
46.	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.
47.	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.
48.	Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol, 2011, 6(2): 244-285.
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50.	Nitadori J, Bograd AJ, Kadota K, et al. Impact of micropapillary histologic subtype in selecting limited resection vs lobectomy for lung adenocarcinoma of 2 cm or smaller. J Natl Cancer Inst, 2013, 105(16): 1212-1220.
51.	Eguchi T, Kameda K, Lu S, et al. Lobectomy is associated with better outcomes than sublobar resection in spread through air spaces (STAS)-positive T1 lung adenocarcinoma: A propensity score-matched analysis. J Thorac Oncol, 2019, 14(1): 87-98.
52.	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.
53.	Sawabata N, Ohta M, Matsumura A, et al. Optimal distance of malignant negative margin in excision of nonsmall cell lung cancer: A multicenter prospective study. Ann Thorac Surg, 2004, 77(2): 415-420.
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60.	Nomori H, Shiraishi A, Yamazaki I, et al. Extent of segmentectomy that achieves greater lung preservation than lobectomy. Ann Thorac Surg, 2021, 112(4): 1127-1133.
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1. Churchill ED, Belsey R. Segmental pneumonectomy in bronchiectasis: The lingula segment of the left upper lobe. Ann Surg, 1939, 109(4): 481-499.
2. Bonfils-Roberts EA, Clagett OT. Contemporary indications for pulmonary segmental resections. J Thorac Cardiovasc Surg, 1972, 63(3): 433-438.
3. Bennett WF, Smith RA. Segmental resection for bronchogenic carcinoma: A surgical alternative for the compromised patient. Ann Thorac Surg, 1979, 27(2): 169-172.
4. Tsutani Y, Tsubokawa N, Ito M, et al. Postoperative complications and prognosis after lobar resection versus sublobar resection in elderly patients with clinical stage Ⅰnon-small-cell lung cancer. Eur J Cardiothorac Surg, 2018, 53(2): 366-371.
5. Brunelli A, Decaluwe H, Gossot D, et al. Perioperative outcomes of segmentectomies versus lobectomies in high-risk patients: An ESTS database analysis. Eur J Cardiothorac Surg, 2020: ezaa308.
6. Jensik RJ, Faber LP, Milloy FJ, et al. Segmental resection for lung cancer. A fifteen-year experience. J Thorac Cardiovasc Surg, 1973, 66(4): 563-572.
7. Jensik RJ, Faber LP, Kittle CF. Segmental resection for bronchogenic carcinoma. Ann Thorac Surg, 1979, 28(5): 475-483.
8. Warren WH, Faber LP. Segmentectomy versus lobectomy in patients with stage Ⅰ pulmonary carcinoma. Five-year survival and patterns of intrathoracic recurrence. J Thorac Cardiovasc Surg, 1994, 107(4): 1087-1093.
9. 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.
10. Ettinger DS, Wood DE, Aisner DL, et al. NCCN guidelines insights: Non-small cell lung cancer, version 2. 2021. J Natl Compr Canc Netw, 2021, 19(3): 254-266.
11. Brunelli A, Charloux A, Bolliger CT, et al. ERS/ESTS clinical guidelines on fitness for radical therapy in lung cancer patients (surgery and chemo-radiotherapy). Eur Respir J, 2009, 34(1): 17-41.
12. Lim E, Baldwin D, Beckles M, et al. Guidelines on the radical management of patients with lung cancer. Thorax, 2010, 65 Suppl 3: iii1-iii27.
13. Brunelli A, Kim AW, Berger KI, et al. Physiologic evaluation of the patient with lung cancer being considered for resectional surgery: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. Chest, 2013, 143(5 Suppl): e166S-e190S.
14. Rami-Porta R, Bolejack V, Crowley J, et al. The IASLC lung cancer staging project: Proposals for the revisions of the T descriptors in the forthcoming eighth edition of the TNM classification for lung cancer. J Thorac Oncol, 2015, 10(7): 990-1003.
15. Jang HJ, Lee KS, Kwon OJ, et al. Bronchioloalveolar carcinoma: Focal area of ground-glass attenuation at thin-section CT as an early sign. Radiology, 1996, 199(2): 485-488.
16. National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
17. Ohde Y, Nagai K, Yoshida J, et al. The proportion of consolidation to ground-glass opacity on high resolution CT is a good predictor for distinguishing the population of non-invasive peripheral adenocarcinoma. Lung Cancer, 2003, 42(3): 303-310.
18. Kodama K, Higashiyama M, Yokouchi H, et al. Prognostic value of ground-glass opacity found in small lung adenocarcinoma on high-resolution CT scanning. Lung Cancer, 2001, 33(1): 17-25.
19. Aoki T, Tomoda Y, Watanabe H, et al. Peripheral lung adenocarcinoma: Correlation of thin-section CT findings with histologic prognostic factors and survival. Radiology, 2001, 220(3): 803-809.
20. Suzuki K, Asamura H, Kusumoto M, et al. "Early" peripheral lung cancer: Prognostic significance of ground glass opacity on thin-section computed tomographic scan. Ann Thorac Surg, 2002, 74(5): 1635-1639.
21. 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.
22. 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.
23. 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.
24. Ye T, Deng L, Wang S, et al. Lung Adenocarcinomas manifesting as radiological part-solid nodules define a special clinical subtype. J Thorac Oncol, 2019, 14(4): 617-627.
25. Yoshizawa A, Motoi N, Riely GJ, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: Prognostic subgroups and implications for further revision of staging based on analysis of 514 stage Ⅰcases. Mod Pathol, 2011, 24(5): 653-664.
26. Russell PA, Wainer Z, Wright GM, et al. Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol, 2011, 6(9): 1496-1504.
27. Warth A, Muley T, Meister M, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol, 2012, 30(13): 1438-1446.
28. Clagett OT, Deterling RA, Jr. A technique for segmental pulmonary resection with particular reference to lingulectomy. J Thorac Surg, 1946, 15: 227-238.
29. Nomori H, Okada M. Illustrated Textbook of Anatomical Pulmonary Segmentectomy. Heidelberg: Springer, 2012.
30. Wu WB, Xu XF, Wen W, et al. Three-dimensional computed tomography bronchography and angiography in the preoperative evaluation of thoracoscopic segmentectomy and subsegmentectomy. J Thorac Dis, 2016, 8(Suppl 9): S710-S715.
31. Wu WB, Xia Y, Pan XL, et al. Three-dimensional navigation-guided thoracoscopic combined subsegmentectomy for intersegmental pulmonary nodules. Thorac Cancer, 2019, 10(1): 41-46.
32. Wu WB, Xu XF, Wen W, et al. Thoracoscopic pulmonary sub-subsegmentectomy based on three-dimensional images. Ann Thorac Surg, 2016, 102(5): e389-e391.
33. Landreneau RJ, Hazelrigg SR, Ferson PF, et al. Thoracoscopic resection of 85 pulmonary lesions. Ann Thorac Surg, 1992, 54(3): 415-419.
34. Koike T, Yamato Y, Yoshiya K, et al. Intentional limited pulmonary resection for peripheral T1 N0 M0 small-sized lung cancer. J Thorac Cardiovasc Surg, 2003, 125(4): 924-928.
35. Okada M, Koike T, Higashiyama M, et al. Radical sublobar resectionfor small-sized non-small cell lung cancer: A multicenter study. J Thorac Cardiovasc Surg, 2006, 132(4): 769-775.
36. Rami-Porta R, Ball D, Crowley J, et al. The IASLC Lung Cancer Staging Project: Proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol, 2007, 2(7): 593-602.
37. Padilla J, Calvo V, Pe?alver JC, et al. Surgical results and prognostic factors in early non-small cell lung cancer. Ann Thorac Surg, 1997, 63(2): 324-326.
38. Mulligan CR, Meram AD, Proctor CD, et al. Lung cancer staging: A case for a new T definition. Ann Thorac Surg, 2006, 82(1): 220-226.
39. Asamura H, Goya T, Koshiishi Y, et al. How should the TNM staging system for lung cancer be revised? A simulation based on the Japanese Lung Cancer Registry populations. J Thorac Cardiovasc Surg, 2006, 132(2): 316-319.
40. 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(12): 915-924.
41. Lee KS, Kim Y, Han J, et al. Bronchioloalveolar carcinoma: Clinical, histopathologic, and radiologic findings. Radiographics, 1997, 17(6): 1345-1357.
42. Aquino SL, Chiles C, Halford P. Distinction of consolidative bronchioloalveolar carcinoma from pneumonia: Do CT criteria work? AJR Am J Roentgenol, 1998, 171(2): 359-363.
43. Akira M, Atagi S, Kawahara M, et al. High-resolution CT findings of diffuse bronchioloalveolar carcinoma in 38 patients. AJR Am J Roentgenol, 1999, 173(6): 1623-1629.
44. Nakamura K, Saji H, Nakajima R, et al. A phase Ⅲrandomized trial of lobectomy versus limited resection for small-sized peripheral non-small cell lung cancer (JCOG0802/WJOG4607L). Jpn J Clin Oncol, 2010, 40(3): 271-274.
45. 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.
46. 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.
47. 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.
48. Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol, 2011, 6(2): 244-285.
49. Sica G, Yoshizawa A, Sima CS, et al. A grading system of lung adenocarcinomas based on histologic pattern is predictive of disease recurrence in stage I tumors. Am J Surg Pathol, 2010, 34(8): 1155-1162.
50. Nitadori J, Bograd AJ, Kadota K, et al. Impact of micropapillary histologic subtype in selecting limited resection vs lobectomy for lung adenocarcinoma of 2 cm or smaller. J Natl Cancer Inst, 2013, 105(16): 1212-1220.
51. Eguchi T, Kameda K, Lu S, et al. Lobectomy is associated with better outcomes than sublobar resection in spread through air spaces (STAS)-positive T1 lung adenocarcinoma: A propensity score-matched analysis. J Thorac Oncol, 2019, 14(1): 87-98.
52. 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.
53. Sawabata N, Ohta M, Matsumura A, et al. Optimal distance of malignant negative margin in excision of nonsmall cell lung cancer: A multicenter prospective study. Ann Thorac Surg, 2004, 77(2): 415-420.
54. Schuchert MJ, Pettiford BL, Keeley S, et al. Anatomic segmentectomy in the treatment of stage Ⅰ non-small cell lung cancer. Ann Thorac Surg, 2007, 84(3): 926-932.
55. 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(8): 2400-2405.
56. Lewis RJ, Caccavale RJ, Sisler GE, et al. Video-assisted thoracic surgical resection of malignant lung tumors. J Thorac Cardiovasc Surg, 1992, 104(6): 1679-1685.
57. Takahashi N, Sawabata N, Kawamura M, et al. Optimal sublobar resection for c-stage Ⅰ non-small cell lung cancer: Significance of margin distance to tumor size ratio and margin cytology (supplementary analysis of KLSG-0801): Complete republication. Gen Thorac Cardiovasc Surg, 2019, 67(8): 690-696.
58. Horinouchi H, Nomori H, Nakayama T, et al. How many pathological T1N0M0 non-small cell lung cancers can be completely resected in one segment? Special reference to high-resolution computed tomography findings. Surg Today, 2011, 41(8): 1062-1066.
59. Keenan RJ, Landreneau RJ, Maley RH, et al. Segmental resection spares pulmonary function in patients with stage Ⅰ lung cancer. Ann Thorac Surg, 2004, 78(1): 228-233.
60. Nomori H, Shiraishi A, Yamazaki I, et al. Extent of segmentectomy that achieves greater lung preservation than lobectomy. Ann Thorac Surg, 2021, 112(4): 1127-1133.
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Advances in indications of anatomical pulmonary segmentectomy for early-stage lung cancer

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