Recent progress of lymph nodes management of clinical stage ⅠA lung cancer_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

CHEN Donglai , REN Yijiu , ZHU Erjia , SU Hang ,  CHEN Chang

Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University School of Medicine, Shanghai, 200433, P.R.China;

Corresponding author：

CHEN Chang, Email: chenthoracic@163.com

Keywords：

Lung neoplasm; lymph node metastasis; lymphadenectomy; prognosis

DOI：

10.7507/1007-4848.201804063

Video：

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Systematic lymph nodes dissection has been a standard procedure in lung cancer surgery, while the manipulation of mediastinal lymph nodes for early stage lung cancer remains controversial since surgeons have been weighing the advantages and disadvantages of different methods of lymph node dissection. With an increasing in early stage non-small cell lung cancer patients in recent years, there are more and more intensive studies especially focusing on the mediastinal lymph nodes dissection of clinical stage ⅠA lung cancer. In this review, the lymph nodes management of clinical stage ⅠA non-small cell lung cancer, especially systematic lymph nodes dissection and sampling as well as lobe-specific lymph node dissection, are summarized.

Citation： CHEN Donglai, REN Yijiu, ZHU Erjia, SU Hang, CHEN Chang. Recent progress of lymph nodes management of clinical stage ⅠA lung cancer. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2018, 25(10): 890-894. doi: 10.7507/1007-4848.201804063 Copy

1.	Gould MK, Donington J, Lynch WR, et al. Evaluation of individuals with pulmonary nodules: when is it 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): e93S-e120S.
2.	Kataoka Y, Hirano K, Narabayashi T, et al. Concordance between the response evaluation criteria in solid tumors version 1.1 and the immune-related response criteria in patients with non-small cell lung cancer treated with nivolumab: a multicenter retrospective cohort study. Cancer Chemother Pharmacol, 2018, 81(2): 333-337.
3.	De Leyn P, Dooms C, Kuzdzal J, et al. Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer. Eur J Cardiothorac Surg, 2014, 45(5): 787-798.
4.	Erickson CJ, Fernandez FG, Reddy RM. Minimally invasive and open approaches to mediastinal nodal assessment. Ann Surg Oncol, 2018, 25(1): 64-67.
5.	Meng D, Zhou Z, Wang Y, et al. Lymphadenectomy for clinical early-stage non-small-cell lung cancer: a systematic review and meta-analysis. Eur J Cardiothorac Surg, 2016, 50(4): 597-604.
6.	Mokhles S, Macbeth F, Treasure T, et al. Systematic lymphadenectomy versus sampling of ipsilateral mediastinal lymph-nodes during lobectomy for non-small-cell lung cancer: a systematic review of randomized trials and a meta-analysis. Eur J Cardiothorac Surg, 2017, 51(6): 1149-1156.
7.	Flores RM, Nicastri D, Bauer T, et al. Computed tomography screening for lung cancer: mediastinal lymph node resection in stage ⅠA non-small cell lung cancer manifesting as subsolid and solid nodules. Ann Surg, 2017, 265(5): 1025-1033.
8.	Riquet M, Rivera C, Pricopi C, et al. Is the lymphatic drainage of lung cancer lobe-specific? A surgical appraisal. Eur J Cardiothorac Surg, 2015, 47(3): 543-549.
9.	Detterbeck FC, Boffa DJ, Kim AW, et al. The eighth edition lung cancer stage classification. Chest, 2017, 151(1): 193-203.
10.	Watanabe Y, Shimizu J, Tsubota M, et al. Mediastinal spread of metastatic lymph nodes in bronchogenic carcinoma. Mediastinal nodal metastases in lung cancer. Chest, 1990, 97(5): 1059-1065.
11.	陈建, 申屠阳. 早期肺癌肺叶特异性淋巴结清扫的研究进展. 中国肺癌杂志, 2011, 14(1): 63-68.
12.	Riquet M, Assouad J, Bagan P, et al. Skip mediastinal lymph node metastasis and lung cancer: a particular N2 subgroup with a better prognosis. Ann Thorac Surg, 2005, 79(1): 225-233.
13.	Dai C, Xie H, Kadeer X, et al. Relationship of lymph node micrometastasis and micropapillary component and their joint influence on prognosis of patients with stage i lung adenocarcinoma. Am J Surg Pathol, 2017, 41(9): 1212-1220.
14.	Guerrera F, Renaud S, Tabbó F, et al. Epidermal growth factor receptor mutations are linked to skip N2 lymph node metastasis in resected non-small-cell lung cancer adenocarcinomas. Eur J Cardiothorac Surg, 2017, 51(4): 680-688.
15.	Li H, Hu H, Wang R, et al. Lung adenocarcinoma: Are skip N2 metastases different from non-skip? J Thorac Cardiovasc Surg, 2015, 150(4): 790-795.
16.	He Z, Xia Y, Tang S, et al. Detection of occult tumor cells in regional lymph nodes is associated with poor survival in pN0 non-small cell lung cancer: a meta-analysis. J Thorac Dis, 2016, 8(3): 375-385.
17.	Martin LW, D'Cunha J, Wang X, et al. Detection of occult micrometastases in patients with clinical stage i non-small-cell lung cancer: a prospective analysis of mature results of CALGB 9761(Alliance). J Clin Oncol, 2016, 34(13): 1484-1491.
18.	Koike T, Koike T, Yamato Y, et al. Predictive risk factors for mediastinal lymph node metastasis in clinical stage ⅠA non-small-cell lung cancer patients. J Thorac Oncol, 2012, 7(8): 1246-1251.
19.	Bao F, Yuan P, Yuan X, et al. Predictive risk factors for lymph node metastasis in patients with small size non-small cell lung cancer. J Thorac Dis, 2014, 6(12): 1697-1703.
20.	Tsutani Y, Miyata Y, Nakayama H, et al. Prediction of pathologic node-negative clinical stage ⅠA lung adenocarcinoma for optimal candidates undergoing sublobar resection. J Thorac Cardiovasc Surg, 2012, 144(6): 1365-1371.
21.	Hattori A, Suzuki K, Maeyashiki T, et al. The presence of air bronchogram is a novel predictor of negative nodal involvement in radiologically pure-solid lung cancer. Eur J Cardiothorac Surg, 2014, 45(4): 699-702.
22.	Kudo Y, Matsubayashi J, Saji H, et al. Association between high-resolution computed tomography findings and the IASLC/ATS/ERS classification of small lung adenocarcinomas in Japanese patients. Lung Cancer, 2015, 90(1): 47-54.
23.	Ma K, Chang D, He B, et al. Radical systematic mediastinal lymphadenectomy versus mediastinal lymph node sampling in patients with clinical stage ⅠA and pathological stage T1 non-small cell lung cancer. J Cancer Res Clin Oncol, 2008, 134(12): 1289-1295.
24.	Darling GE, Allen MS, Decker PA, et al. Number of lymph nodes harvested from a mediastinal lymphadenectomy: results of the randomized, prospective American College of Surgeons Oncology Group Z0030 trial. Chest, 2011, 139(5): 1124-1129.
25.	Darling GE, Allen MS, Decker PA, et al. Randomized trial of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in the patient with N0 or N1(less than hilar) non-small cell carcinoma: results of the American College of Surgery Oncology Group Z0030 Trial. J Thorac Cardiovasc Surg, 2011, 141(3): 662-670.
26.	Maniwa T, Okumura T, Isaka M, et al. Recurrence of mediastinal node cancer after lobe-specific systematic nodal dissection for non-small-cell lung cancer. Eur J Cardiothorac Surg, 2013, 44(1): e59-e64.
27.	Adachi H, Sakamaki K, Nishii T, et al. Lobe-specific lymph node dissection as a standard procedure in surgery for non-small cell lung cancer: a propensity score matching study. J Thorac Oncol, 2017, 12(1): 85-93.
28.	Hishida T, Saji H, Watanabe SI, et al. A randomized Phase Ⅲ trial of lobe-specific vs. systematic nodal dissection for clinical Stage I-II non-small cell lung cancer (JCOG1413). Jpn J Clin Oncol, 2018, 48(2): 190-194.
29.	Shapiro M, Kadakia S, Lim J, et al. Lobe-specific mediastinal nodal dissection is sufficient during lobectomy by video-assisted thoracic surgery or thoracotomy for early-stage lung cancer. Chest, 2013, 144(5): 1615-1621.
30.	Funatsu T, Matsubara Y, Ikeda S, et al. Preoperative mediastinoscopic assessment of N factors and the need for mediastinal lymph node dissection in T1 lung cancer. J Thorac Cardiovasc Surg, 1994, 108(2): 321-328.
31.	Baisi A, Raveglia F, De Simone M, et al. Micrometastasis and skip metastasis as predictive factors in non-small-cell lung cancer staging. Eur J Cardiothorac Surg, 2013, 43(5): 1075.
32.	Wu Yl, Huang ZF, Wang SY, et al. A randomized trial of systematic nodal dissection in resectable non-small cell lung cancer. Lung Cancer, 2002, 36(1): 1-6.
33.	Sugi K, Nawata K, Fujita N, et al. Systematic lymph node dissection for clinically diagnosed peripheral non-small-cell lung cancer less than 2 cm in diameter. World J Surg, 1998, 22(3): 290-295.
34.	Dong S, Du J, Li W, et al. Systematic mediastinal lymphadenectomy or mediastinal lymph node sampling in patients with pathological stage Ⅰ NSCLC: a meta-analysis. World J Surg, 2015, 39(2): 410-416.
35.	Zhang J, Mao T, Gu Z, et al. Comparison of complete and minimal mediastinal lymph node dissection for non-small cell lung cancer: Results of a prospective randomized trial. Thorac Cancer, 2013, 4(4): 416-421.
36.	Huang X, Wang J, Chen Q, et al. Mediastinal lymph node dissection versus mediastinal lymph node sampling for early stage non-small cell lung cancer: a systematic review and meta-analysis. PLoS One, 2014, 9(10): e109979.
37.	David EA, Cooke DT, Chen Y, et al. Does lymph node count influence survival in surgically resected non-small cell lung cancer? Ann Thorac Surg, 2017, 103(1): 226-235.
38.	Liang W, He J, Shen Y, et al. Impact of examined lymph node count on precise staging and long-term survival of resected non-small-cell lung cancer: a population study of the US SEER database and a Chinese multi-institutional registry. J Clin Oncol, 2017, 35(11): 1162-1170.
39.	Liu R, Chen J, Xu S. Examined lymph node count in non-small-cell lung cancer: will it be a decision making approach in treatment of NSCLC? J Thorac Dis, 2017, 9(5): E480-E482.
40.	Taylor MD, Lapar DJ, Thomas CJ, et al. Lymph node ratio predicts recurrence and survival after R0 resection for non-small cell lung cancer. Ann Thorac Surg, 2013, 96(4): 1163-1170.
41.	Zhong WZ, Liu SY, Wu YL. Numbers or stations: from systematic sampling to individualized lymph node dissection in non-small-cell lung cancer. J Clin Oncol, 2017, 35(11): 1143-1145.
42.	Cheng X, Zheng D, Li Y, et al. Tumor histology predicts mediastinal nodal status and may be used to guide limited lymphadenectomy in patients with clinical stage I non-small cell lung cancer. J Thorac Cardiovasc Surg, 2018, 155(6): 2648-2656.

1. Gould MK, Donington J, Lynch WR, et al. Evaluation of individuals with pulmonary nodules: when is it 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): e93S-e120S.
2. Kataoka Y, Hirano K, Narabayashi T, et al. Concordance between the response evaluation criteria in solid tumors version 1.1 and the immune-related response criteria in patients with non-small cell lung cancer treated with nivolumab: a multicenter retrospective cohort study. Cancer Chemother Pharmacol, 2018, 81(2): 333-337.
3. De Leyn P, Dooms C, Kuzdzal J, et al. Revised ESTS guidelines for preoperative mediastinal lymph node staging for non-small-cell lung cancer. Eur J Cardiothorac Surg, 2014, 45(5): 787-798.
4. Erickson CJ, Fernandez FG, Reddy RM. Minimally invasive and open approaches to mediastinal nodal assessment. Ann Surg Oncol, 2018, 25(1): 64-67.
5. Meng D, Zhou Z, Wang Y, et al. Lymphadenectomy for clinical early-stage non-small-cell lung cancer: a systematic review and meta-analysis. Eur J Cardiothorac Surg, 2016, 50(4): 597-604.
6. Mokhles S, Macbeth F, Treasure T, et al. Systematic lymphadenectomy versus sampling of ipsilateral mediastinal lymph-nodes during lobectomy for non-small-cell lung cancer: a systematic review of randomized trials and a meta-analysis. Eur J Cardiothorac Surg, 2017, 51(6): 1149-1156.
7. Flores RM, Nicastri D, Bauer T, et al. Computed tomography screening for lung cancer: mediastinal lymph node resection in stage ⅠA non-small cell lung cancer manifesting as subsolid and solid nodules. Ann Surg, 2017, 265(5): 1025-1033.
8. Riquet M, Rivera C, Pricopi C, et al. Is the lymphatic drainage of lung cancer lobe-specific? A surgical appraisal. Eur J Cardiothorac Surg, 2015, 47(3): 543-549.
9. Detterbeck FC, Boffa DJ, Kim AW, et al. The eighth edition lung cancer stage classification. Chest, 2017, 151(1): 193-203.
10. Watanabe Y, Shimizu J, Tsubota M, et al. Mediastinal spread of metastatic lymph nodes in bronchogenic carcinoma. Mediastinal nodal metastases in lung cancer. Chest, 1990, 97(5): 1059-1065.
11. 陈建, 申屠阳. 早期肺癌肺叶特异性淋巴结清扫的研究进展. 中国肺癌杂志, 2011, 14(1): 63-68.
12. Riquet M, Assouad J, Bagan P, et al. Skip mediastinal lymph node metastasis and lung cancer: a particular N2 subgroup with a better prognosis. Ann Thorac Surg, 2005, 79(1): 225-233.
13. Dai C, Xie H, Kadeer X, et al. Relationship of lymph node micrometastasis and micropapillary component and their joint influence on prognosis of patients with stage i lung adenocarcinoma. Am J Surg Pathol, 2017, 41(9): 1212-1220.
14. Guerrera F, Renaud S, Tabbó F, et al. Epidermal growth factor receptor mutations are linked to skip N2 lymph node metastasis in resected non-small-cell lung cancer adenocarcinomas. Eur J Cardiothorac Surg, 2017, 51(4): 680-688.
15. Li H, Hu H, Wang R, et al. Lung adenocarcinoma: Are skip N2 metastases different from non-skip? J Thorac Cardiovasc Surg, 2015, 150(4): 790-795.
16. He Z, Xia Y, Tang S, et al. Detection of occult tumor cells in regional lymph nodes is associated with poor survival in pN0 non-small cell lung cancer: a meta-analysis. J Thorac Dis, 2016, 8(3): 375-385.
17. Martin LW, D'Cunha J, Wang X, et al. Detection of occult micrometastases in patients with clinical stage i non-small-cell lung cancer: a prospective analysis of mature results of CALGB 9761(Alliance). J Clin Oncol, 2016, 34(13): 1484-1491.
18. Koike T, Koike T, Yamato Y, et al. Predictive risk factors for mediastinal lymph node metastasis in clinical stage ⅠA non-small-cell lung cancer patients. J Thorac Oncol, 2012, 7(8): 1246-1251.
19. Bao F, Yuan P, Yuan X, et al. Predictive risk factors for lymph node metastasis in patients with small size non-small cell lung cancer. J Thorac Dis, 2014, 6(12): 1697-1703.
20. Tsutani Y, Miyata Y, Nakayama H, et al. Prediction of pathologic node-negative clinical stage ⅠA lung adenocarcinoma for optimal candidates undergoing sublobar resection. J Thorac Cardiovasc Surg, 2012, 144(6): 1365-1371.
21. Hattori A, Suzuki K, Maeyashiki T, et al. The presence of air bronchogram is a novel predictor of negative nodal involvement in radiologically pure-solid lung cancer. Eur J Cardiothorac Surg, 2014, 45(4): 699-702.
22. Kudo Y, Matsubayashi J, Saji H, et al. Association between high-resolution computed tomography findings and the IASLC/ATS/ERS classification of small lung adenocarcinomas in Japanese patients. Lung Cancer, 2015, 90(1): 47-54.
23. Ma K, Chang D, He B, et al. Radical systematic mediastinal lymphadenectomy versus mediastinal lymph node sampling in patients with clinical stage ⅠA and pathological stage T1 non-small cell lung cancer. J Cancer Res Clin Oncol, 2008, 134(12): 1289-1295.
24. Darling GE, Allen MS, Decker PA, et al. Number of lymph nodes harvested from a mediastinal lymphadenectomy: results of the randomized, prospective American College of Surgeons Oncology Group Z0030 trial. Chest, 2011, 139(5): 1124-1129.
25. Darling GE, Allen MS, Decker PA, et al. Randomized trial of mediastinal lymph node sampling versus complete lymphadenectomy during pulmonary resection in the patient with N0 or N1(less than hilar) non-small cell carcinoma: results of the American College of Surgery Oncology Group Z0030 Trial. J Thorac Cardiovasc Surg, 2011, 141(3): 662-670.
26. Maniwa T, Okumura T, Isaka M, et al. Recurrence of mediastinal node cancer after lobe-specific systematic nodal dissection for non-small-cell lung cancer. Eur J Cardiothorac Surg, 2013, 44(1): e59-e64.
27. Adachi H, Sakamaki K, Nishii T, et al. Lobe-specific lymph node dissection as a standard procedure in surgery for non-small cell lung cancer: a propensity score matching study. J Thorac Oncol, 2017, 12(1): 85-93.
28. Hishida T, Saji H, Watanabe SI, et al. A randomized Phase Ⅲ trial of lobe-specific vs. systematic nodal dissection for clinical Stage I-II non-small cell lung cancer (JCOG1413). Jpn J Clin Oncol, 2018, 48(2): 190-194.
29. Shapiro M, Kadakia S, Lim J, et al. Lobe-specific mediastinal nodal dissection is sufficient during lobectomy by video-assisted thoracic surgery or thoracotomy for early-stage lung cancer. Chest, 2013, 144(5): 1615-1621.
30. Funatsu T, Matsubara Y, Ikeda S, et al. Preoperative mediastinoscopic assessment of N factors and the need for mediastinal lymph node dissection in T1 lung cancer. J Thorac Cardiovasc Surg, 1994, 108(2): 321-328.
31. Baisi A, Raveglia F, De Simone M, et al. Micrometastasis and skip metastasis as predictive factors in non-small-cell lung cancer staging. Eur J Cardiothorac Surg, 2013, 43(5): 1075.
32. Wu Yl, Huang ZF, Wang SY, et al. A randomized trial of systematic nodal dissection in resectable non-small cell lung cancer. Lung Cancer, 2002, 36(1): 1-6.
33. Sugi K, Nawata K, Fujita N, et al. Systematic lymph node dissection for clinically diagnosed peripheral non-small-cell lung cancer less than 2 cm in diameter. World J Surg, 1998, 22(3): 290-295.
34. Dong S, Du J, Li W, et al. Systematic mediastinal lymphadenectomy or mediastinal lymph node sampling in patients with pathological stage Ⅰ NSCLC: a meta-analysis. World J Surg, 2015, 39(2): 410-416.
35. Zhang J, Mao T, Gu Z, et al. Comparison of complete and minimal mediastinal lymph node dissection for non-small cell lung cancer: Results of a prospective randomized trial. Thorac Cancer, 2013, 4(4): 416-421.
36. Huang X, Wang J, Chen Q, et al. Mediastinal lymph node dissection versus mediastinal lymph node sampling for early stage non-small cell lung cancer: a systematic review and meta-analysis. PLoS One, 2014, 9(10): e109979.
37. David EA, Cooke DT, Chen Y, et al. Does lymph node count influence survival in surgically resected non-small cell lung cancer? Ann Thorac Surg, 2017, 103(1): 226-235.
38. Liang W, He J, Shen Y, et al. Impact of examined lymph node count on precise staging and long-term survival of resected non-small-cell lung cancer: a population study of the US SEER database and a Chinese multi-institutional registry. J Clin Oncol, 2017, 35(11): 1162-1170.
39. Liu R, Chen J, Xu S. Examined lymph node count in non-small-cell lung cancer: will it be a decision making approach in treatment of NSCLC? J Thorac Dis, 2017, 9(5): E480-E482.
40. Taylor MD, Lapar DJ, Thomas CJ, et al. Lymph node ratio predicts recurrence and survival after R0 resection for non-small cell lung cancer. Ann Thorac Surg, 2013, 96(4): 1163-1170.
41. Zhong WZ, Liu SY, Wu YL. Numbers or stations: from systematic sampling to individualized lymph node dissection in non-small-cell lung cancer. J Clin Oncol, 2017, 35(11): 1143-1145.
42. Cheng X, Zheng D, Li Y, et al. Tumor histology predicts mediastinal nodal status and may be used to guide limited lymphadenectomy in patients with clinical stage I non-small cell lung cancer. J Thorac Cardiovasc Surg, 2018, 155(6): 2648-2656.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Recent progress of lymph nodes management of clinical stage ⅠA lung cancer

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