Selective mediastinal lymph node dissection: Precision surgery in the era of precision medicine_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

DENG Chaoqiang ^1,2,3,4 , JIANG Chenyu ^1,2,3,4 ,  ZHANG Yang ^1,2,3,4 ,  CHEN Haiquan ^1,2,3,4

1. Department of Thoracic Surgery, Cancer Center, Fudan University, Shanghai, 200032, P. R. China;
2. State Key Laboratory of Genetic Engineering, Cancer Center, Fudan University, Shanghai, 200032, P. R. China;
3. Institute of Thoracic Oncology, Fudan University, Shanghai, 200032, P. R. China;
4. Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, 200032, P. R. China;

Corresponding author：

ZHANG Yang, Email: fduzhangyang1987@hotmail.com; CHEN Haiquan, Email: hqchen1@yahoo.com

Keywords：

Selective lymph node dissection; precision medicine; precision surgery

DOI：

10.7507/1007-4848.202307027

Video：

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Along with the popularity of low-dose computed tomography lung cancer screening, an increasing number of early-stage lung cancers are detected. Radical lobectomy with systematic nodal dissection (SND) remains the standard-of-care for operable lung cancer patients. However, whether SND should be performed on non-metastatic lymph nodes remains controversy. Unnecessary lymph node dissection can increase the difficulty of surgery while also causing additional surgical damage. In addition, non-metastatic lymph nodes have been recently reported to play a key role in immunotherapy. How to reduce the surgical damage of mediastinal lymph node dissection for early-stage lung cancer patients is pivotal for modern concept of "minimally invasive surgery for lung cancer 3.0". The selective mediastinal lymph node dissection strategy aims to dissect lymph nodes with tumor metastasis while preserving normal mediastinal lymph nodes. Previous studies have shown that combination of specific tumor segment site, radiology and intraoperative frozen pathology characteristics can accurately predict the pattern of mediastinal lymph node metastasis. The personalized selective mediastinal lymph node dissection strategy formed from this has been successfully validated in a recent prospective clinical trial, providing an important basis for early-stage lung cancer patients to receive more personalized selective lymph node dissection with "precision surgery" strategies.

Citation： DENG Chaoqiang, JIANG Chenyu, ZHANG Yang, CHEN Haiquan. Selective mediastinal lymph node dissection: Precision surgery in the era of precision medicine. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2023, 30(9): 1224-1227. doi: 10.7507/1007-4848.202307027 Copy

1.	Cahan WG, Watson WL, Pool JL. Radical pneumonectomy. J Thorac Surg, 1951, 22(5): 449-473.
2.	Cahan WG. Radical lobectomy. J Thorac Cardiovasc Surg, 1960, 39: 555-572.
3.	Goldstraw P. Report on the international workshop on intrathoracic staging. London, October 1996. Lung Cancer, 1997, 18(1): 107-111.
4.	Izbicki JR, Passlick B, Pantel K, et al. Effectiveness of radical systematic mediastinal lymphadenectomy in patients with resectable non-small cell lung cancer: Results of a prospective randomized trial. Ann Surg, 1998, 227(1): 138-144.
5.	Izbicki JR, Thetter O, Habekost M, et al. Radical systematic mediastinal lymphadenectomy in non-small cell lung cancer: A randomized controlled trial. Br J Surg, 1994, 81(2): 229-235.
6.	Chida M, Minowa M, Karube Y, et al. Worsened long-term outcomes and postoperative complications in octogenarians with lung cancer following mediastinal lymph-node dissection. Interact Cardiovasc Thorac, 2009, 8(1): 89-92.
7.	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.
8.	Fransen MF, Schoonderwoerd M, Knopf P, et al. Tumor-draining lymph nodes are pivotal in PD-1/PD-L1 checkpoint therapy. JCI Insight, 2018, 3(23): e124507.
9.	Lane RS, Femel J, Breazeale AP, et al. IFNgamma-activated dermal lymphatic vessels inhibit cytotoxic T cells in melanoma and inflamed skin. J Exp Med, 2018, 215(12): 3057-3074.
10.	Dammeijer F, van Gulijk M, Mulder EE, et al. The PD-1/PD-L1-checkpoint restrains T cell Immunity in tumor-draining lymph nodes. Cancer Cell, 2020, 38(5): 685-700.
11.	Rahim MK, Okholm TLH, Jones KB, et al. Dynamic CD8(+) T cell responses to cancer immunotherapy in human regional lymph nodes are disrupted in metastatic lymph nodes. Cell, 2023, 186(6): 1127-1143.
12.	Lucci A, McCall LM, Beitsch PD, et al. Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol, 2007, 25(24): 3657-3663.
13.	Cheng X, Onaitis MW, D'Amico TA, et al. Minimally invasive thoracic surgery 3.0: Lessons learned from the history of lung cancer surgery. Ann Surg, 2018, 267(1): 37-38.
14.	Allen MS, Darling GE, Pechet TT, et al. Morbidity and mortality of major pulmonary resections in patients with early-stage lung cancer: initial results of the randomized, prospective ACOSOG Z0030 trial. Ann Thorac Surg, 2006, 81(3): 1013-1020.
15.	Darling GE. Current status of mediastinal lymph node dissection versus sampling in non-small cell lung cancer. Thorac Surg Clin, 2013, 23(3): 349-356.
16.	Asamura H, Nakayama H, Kondo H, et al. Lobe-specific extent of systematic lymph node dissection for non-small cell lung carcinomas according to a retrospective study of metastasis and prognosis. J Thorac Cardiovasc Surg, 1999, 117(6): 1102-1111.
17.	Okada M, Tsubota N, Yoshimura M, et al. Proposal for reasonable mediastinal lymphadenectomy in bronchogenic carcinomas: Role of subcarinal nodes in selective dissection. J Thorac Cardiovasc Surg, 1998, 116(6): 949-953.
18.	Hishida T, Miyaoka E, Yokoi K, et al. Lobe-specific nodal dissection for clinical stage Ⅰ and Ⅱ NSCLC: Japanese multi-institutional retrospective study using a propensity score analysis. J Thorac Oncol, 2016, 11(9): 1529-1537.
19.	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.
20.	Gaer JA, Goldstraw P. Intraoperative assessment of nodal staging at thoracotomy for carcinoma of the bronchus. Eur J Cardiothorac Surg, 1990, 4(4): 207-210.
21.	Darling GE, Maziak DE, Inculet RI, et al. Positron emission tomography-computed tomography compared with invasive mediastinal staging in non-small cell lung cancer: results of mediastinal staging in the early lung positron emission tomography trial. J Thorac Oncol, 2011, 6(8): 1367-1372.
22.	Zhang Y, Sun Y, Shen L, et al. Predictive factors of lymph node status in small peripheral non-small cell lung cancers: Tumor histology is more reliable. Ann Surg Oncol, 2013, 20(6): 1949-1954.
23.	Ishida T, Yano T, Maeda K, et al. Strategy for lymphadenectomy in lung cancer three centimeters or less in diameter. Ann Thorac Surg, 1990, 50(5): 708-713.
24.	Flores RM, Nicastri D, Bauer T, et al. Computed tomography screening for lung cancer: Mediastinal lymph node resection in stage ⅠA nonsmall cell lung cancer manifesting as subsolid and solid nodules. Ann Surg 2017, 265(5): 1025-1033.
25.	Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
26.	Kawamoto N, Tsutani Y, Kamigaichi A, et al. Tumour location predicts occult N1 nodal metastasis in clinical stage Ⅰ non-small-cell lung cancer. Eur J Cardiothorac Surg, 2023, 63(2): ezac575.
27.	Roy P, Levesque-Laplante A, Guinde J, et al. Central tumor location and occult lymph node metastasis in cT1N0M0 non-small-cell lung cancer. Ann Am Thorac Soc, 2020, 17(4): 522-525.
28.	Zhang Y, Sun Y, Xiang J, et al. A prediction model for N2 disease in T1 non-small cell lung cancer. J Thorac Cardiovasc Surg, 2012, 144(6): 1360-1364.
29.	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.
30.	Zhang Y, Ma X, Shen X, et al. Surgery for pre- and minimally invasive lung adenocarcinoma. J Thorac Cardiovasc Surg, 2022, 163(2): 456-464.
31.	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, 165(6): 2648-2656.
32.	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.
33.	Zhang Y, Deng C, Fu F, et al. Excellent prognosis of patients with invasive lung adenocarcinomas during surgery misdiagnosed as atypical adenomatous hyperplasia, adenocarcinoma in situ, or minimally invasive adenocarcinoma by frozen section. Chest, 2021, 159(3): 1265-1272.
34.	Zhang Y, Fu F, Wen Z, et al. Segment location and ground glass opacity ratio reliably predict node-negative status in lung cancer. Ann Thorac Surg, 2020, 109(4): 1061-1068.
35.	Zhang Y, Deng C, Zheng Q, et al. Selective mediastinal lymph node dissection strategy for clinical T1N0 invasive lung cancer: A prospective, multicenter, clinical trial. J Thorac Oncol, 2023, 18(7): 931-939.
36.	Kim HK. Selective mediastinal lymph node dissection: Precision surgery in the era of precision medicine. J Thorac Oncol, l 2023, 18(7): 834-837.

1. Cahan WG, Watson WL, Pool JL. Radical pneumonectomy. J Thorac Surg, 1951, 22(5): 449-473.
2. Cahan WG. Radical lobectomy. J Thorac Cardiovasc Surg, 1960, 39: 555-572.
3. Goldstraw P. Report on the international workshop on intrathoracic staging. London, October 1996. Lung Cancer, 1997, 18(1): 107-111.
4. Izbicki JR, Passlick B, Pantel K, et al. Effectiveness of radical systematic mediastinal lymphadenectomy in patients with resectable non-small cell lung cancer: Results of a prospective randomized trial. Ann Surg, 1998, 227(1): 138-144.
5. Izbicki JR, Thetter O, Habekost M, et al. Radical systematic mediastinal lymphadenectomy in non-small cell lung cancer: A randomized controlled trial. Br J Surg, 1994, 81(2): 229-235.
6. Chida M, Minowa M, Karube Y, et al. Worsened long-term outcomes and postoperative complications in octogenarians with lung cancer following mediastinal lymph-node dissection. Interact Cardiovasc Thorac, 2009, 8(1): 89-92.
7. 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.
8. Fransen MF, Schoonderwoerd M, Knopf P, et al. Tumor-draining lymph nodes are pivotal in PD-1/PD-L1 checkpoint therapy. JCI Insight, 2018, 3(23): e124507.
9. Lane RS, Femel J, Breazeale AP, et al. IFNgamma-activated dermal lymphatic vessels inhibit cytotoxic T cells in melanoma and inflamed skin. J Exp Med, 2018, 215(12): 3057-3074.
10. Dammeijer F, van Gulijk M, Mulder EE, et al. The PD-1/PD-L1-checkpoint restrains T cell Immunity in tumor-draining lymph nodes. Cancer Cell, 2020, 38(5): 685-700.
11. Rahim MK, Okholm TLH, Jones KB, et al. Dynamic CD8(+) T cell responses to cancer immunotherapy in human regional lymph nodes are disrupted in metastatic lymph nodes. Cell, 2023, 186(6): 1127-1143.
12. Lucci A, McCall LM, Beitsch PD, et al. Surgical complications associated with sentinel lymph node dissection (SLND) plus axillary lymph node dissection compared with SLND alone in the American College of Surgeons Oncology Group Trial Z0011. J Clin Oncol, 2007, 25(24): 3657-3663.
13. Cheng X, Onaitis MW, D'Amico TA, et al. Minimally invasive thoracic surgery 3.0: Lessons learned from the history of lung cancer surgery. Ann Surg, 2018, 267(1): 37-38.
14. Allen MS, Darling GE, Pechet TT, et al. Morbidity and mortality of major pulmonary resections in patients with early-stage lung cancer: initial results of the randomized, prospective ACOSOG Z0030 trial. Ann Thorac Surg, 2006, 81(3): 1013-1020.
15. Darling GE. Current status of mediastinal lymph node dissection versus sampling in non-small cell lung cancer. Thorac Surg Clin, 2013, 23(3): 349-356.
16. Asamura H, Nakayama H, Kondo H, et al. Lobe-specific extent of systematic lymph node dissection for non-small cell lung carcinomas according to a retrospective study of metastasis and prognosis. J Thorac Cardiovasc Surg, 1999, 117(6): 1102-1111.
17. Okada M, Tsubota N, Yoshimura M, et al. Proposal for reasonable mediastinal lymphadenectomy in bronchogenic carcinomas: Role of subcarinal nodes in selective dissection. J Thorac Cardiovasc Surg, 1998, 116(6): 949-953.
18. Hishida T, Miyaoka E, Yokoi K, et al. Lobe-specific nodal dissection for clinical stage Ⅰ and Ⅱ NSCLC: Japanese multi-institutional retrospective study using a propensity score analysis. J Thorac Oncol, 2016, 11(9): 1529-1537.
19. 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.
20. Gaer JA, Goldstraw P. Intraoperative assessment of nodal staging at thoracotomy for carcinoma of the bronchus. Eur J Cardiothorac Surg, 1990, 4(4): 207-210.
21. Darling GE, Maziak DE, Inculet RI, et al. Positron emission tomography-computed tomography compared with invasive mediastinal staging in non-small cell lung cancer: results of mediastinal staging in the early lung positron emission tomography trial. J Thorac Oncol, 2011, 6(8): 1367-1372.
22. Zhang Y, Sun Y, Shen L, et al. Predictive factors of lymph node status in small peripheral non-small cell lung cancers: Tumor histology is more reliable. Ann Surg Oncol, 2013, 20(6): 1949-1954.
23. Ishida T, Yano T, Maeda K, et al. Strategy for lymphadenectomy in lung cancer three centimeters or less in diameter. Ann Thorac Surg, 1990, 50(5): 708-713.
24. Flores RM, Nicastri D, Bauer T, et al. Computed tomography screening for lung cancer: Mediastinal lymph node resection in stage ⅠA nonsmall cell lung cancer manifesting as subsolid and solid nodules. Ann Surg 2017, 265(5): 1025-1033.
25. Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
26. Kawamoto N, Tsutani Y, Kamigaichi A, et al. Tumour location predicts occult N1 nodal metastasis in clinical stage Ⅰ non-small-cell lung cancer. Eur J Cardiothorac Surg, 2023, 63(2): ezac575.
27. Roy P, Levesque-Laplante A, Guinde J, et al. Central tumor location and occult lymph node metastasis in cT1N0M0 non-small-cell lung cancer. Ann Am Thorac Soc, 2020, 17(4): 522-525.
28. Zhang Y, Sun Y, Xiang J, et al. A prediction model for N2 disease in T1 non-small cell lung cancer. J Thorac Cardiovasc Surg, 2012, 144(6): 1360-1364.
29. 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.
30. Zhang Y, Ma X, Shen X, et al. Surgery for pre- and minimally invasive lung adenocarcinoma. J Thorac Cardiovasc Surg, 2022, 163(2): 456-464.
31. 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, 165(6): 2648-2656.
32. 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.
33. Zhang Y, Deng C, Fu F, et al. Excellent prognosis of patients with invasive lung adenocarcinomas during surgery misdiagnosed as atypical adenomatous hyperplasia, adenocarcinoma in situ, or minimally invasive adenocarcinoma by frozen section. Chest, 2021, 159(3): 1265-1272.
34. Zhang Y, Fu F, Wen Z, et al. Segment location and ground glass opacity ratio reliably predict node-negative status in lung cancer. Ann Thorac Surg, 2020, 109(4): 1061-1068.
35. Zhang Y, Deng C, Zheng Q, et al. Selective mediastinal lymph node dissection strategy for clinical T1N0 invasive lung cancer: A prospective, multicenter, clinical trial. J Thorac Oncol, 2023, 18(7): 931-939.
36. Kim HK. Selective mediastinal lymph node dissection: Precision surgery in the era of precision medicine. J Thorac Oncol, l 2023, 18(7): 834-837.

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