Skip to main content
Top
Published in: Annals of Surgical Oncology 13/2022

18-08-2022 | Lung Cancer | Thoracic Oncology

A Comprehensive Comparison of Different Nodal Subclassification Methods in Surgically Resected Non-Small-Cell Lung Cancer Patients

Authors: Zihuai Wang, MD, Zhenyu Yang, MD, Sijia Li, MD, Junqi Zhang, MD, Liang Xia, MD, Jian Zhou, MD, Nan Chen, MD, Chenglin Guo, MD, Lunxu Liu, MD, PhD, FRCS

Published in: Annals of Surgical Oncology | Issue 13/2022

Login to get access

Abstract

Introduction

The revision of the N descriptor in non-small-cell lung cancer has been widely discussed in the past few years. Many different subclassification methods based on number or location of lymph nodes have been proposed for better distinguishing different N patients. This study aimed to systematically collect them and provide a comprehensive comparison among different subclassification methods in a large cohort.

Method

Pathological N1 or N2 non-small-cell lung cancer patients undergoing surgical resection between 2005 and 2016 in the Western China Lung Cancer Database were retrospectively reviewed. A literature review was conducted to collect previous subclassification methods. Kaplan-Meier and multivariable Cox analyses were used to examine the prognostic performance of subclassification methods. Decision curve analysis, Akaike’s information criterion, and area under the receiver operating curve concordance were also performed to evaluate the standardized net benefit of the subclassification methods.

Results

A total of 1625 patients were identified in our cohort. Eight subclassification methods were collected from previous articles and further grouped into subclassification based on number categories (node number or station number), location categories (lymph node zone or chain) or combination of number and location categories. Subclassification based on combination of lymph node location and number tended to have better discrimination ability in multivariable Cox analysis. No significant superiority among the different subclassification methods was observed in the three statistical models.

Conclusion

Subclassification based on the combination of location and number could be used to provide a more accurate prognostic stratification in surgically resected NSCLC and is worth further validation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Goldstraw P, Chansky K, Crowley J, et al. The IASLC lung cancer staging project: proposals for revision of the TNM stage groupings in the forthcoming (Eighth) edition of the TNM classification for lung cancer. J Thorac Oncol. 2016;11(1):39–51.CrossRefPubMed Goldstraw P, Chansky K, Crowley J, et al. The IASLC lung cancer staging project: proposals for revision of the TNM stage groupings in the forthcoming (Eighth) edition of the TNM classification for lung cancer. J Thorac Oncol. 2016;11(1):39–51.CrossRefPubMed
2.
go back to reference Rusch VW, Crowley J, Giroux DJ, et al. The IASLC lung cancer staging project: proposals for the Revision of the N descriptors in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol. 2007;2(7):603–12.CrossRefPubMed Rusch VW, Crowley J, Giroux DJ, et al. The IASLC lung cancer staging project: proposals for the Revision of the N descriptors in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol. 2007;2(7):603–12.CrossRefPubMed
3.
go back to reference Asamura H, Chansky K, Crowley J, et al. The international association for the study of lung cancer lung cancer staging project. J Thorac Oncol. 2015;10(12):1675–84.CrossRefPubMed Asamura H, Chansky K, Crowley J, et al. The international association for the study of lung cancer lung cancer staging project. J Thorac Oncol. 2015;10(12):1675–84.CrossRefPubMed
4.
go back to reference Park BJ, Kim TH, Shin S, et al. Recommended change in the N descriptor proposed by the international association for the study of lung cancer: a validation study. J Thorac Oncol. 2019;14(11):1962–9.CrossRefPubMed Park BJ, Kim TH, Shin S, et al. Recommended change in the N descriptor proposed by the international association for the study of lung cancer: a validation study. J Thorac Oncol. 2019;14(11):1962–9.CrossRefPubMed
5.
go back to reference Chiappetta M, Lococo F, Leuzzi G, et al. External validation of the N descriptor in the proposed tumour-node-metastasis subclassification for lung cancer: the crucial role of histological type, number of resected nodes and adjuvant therapy. Eur J Cardiothorac Surg. 2020;58(6):1236–44.CrossRefPubMed Chiappetta M, Lococo F, Leuzzi G, et al. External validation of the N descriptor in the proposed tumour-node-metastasis subclassification for lung cancer: the crucial role of histological type, number of resected nodes and adjuvant therapy. Eur J Cardiothorac Surg. 2020;58(6):1236–44.CrossRefPubMed
6.
go back to reference Chen W, Zhang C, Wang G, Yu Z, Liu H. Feasibility of nodal classification for non-small cell lung cancer by merging current N categories with the number of involved lymph node stations. Thorac Cancer. 2019;10(7):1533–43.CrossRefPubMedPubMedCentral Chen W, Zhang C, Wang G, Yu Z, Liu H. Feasibility of nodal classification for non-small cell lung cancer by merging current N categories with the number of involved lymph node stations. Thorac Cancer. 2019;10(7):1533–43.CrossRefPubMedPubMedCentral
7.
go back to reference Yun JK, Lee GD, Choi S, et al. Comparison between lymph node station- and zone-based classification for the future revision of node descriptors proposed by the international association for the study of lung cancer in surgically resected patients with non-small-cell lung cancer. Eur J Cardiothorac Surg. 2019;56(5):849–57.CrossRefPubMed Yun JK, Lee GD, Choi S, et al. Comparison between lymph node station- and zone-based classification for the future revision of node descriptors proposed by the international association for the study of lung cancer in surgically resected patients with non-small-cell lung cancer. Eur J Cardiothorac Surg. 2019;56(5):849–57.CrossRefPubMed
8.
go back to reference Yu Y, Zhang P, Yao R, et al. Prognostic value of log odds of positive lymph nodes in node-positive lung squamous cell carcinoma patients after surgery: a SEER population-based study. Transl Lung Cancer Res. 2020;9(4):1285–301.CrossRefPubMedPubMedCentral Yu Y, Zhang P, Yao R, et al. Prognostic value of log odds of positive lymph nodes in node-positive lung squamous cell carcinoma patients after surgery: a SEER population-based study. Transl Lung Cancer Res. 2020;9(4):1285–301.CrossRefPubMedPubMedCentral
9.
go back to reference Tsitsias T, Okiror L, Veres L, et al. New N1/N2 classification and lobe specific lymphatic drainage: Impact on survival in patients with non-small cell lung cancer treated with surgery. Lung Cancer. 2021;151:84–90.CrossRefPubMed Tsitsias T, Okiror L, Veres L, et al. New N1/N2 classification and lobe specific lymphatic drainage: Impact on survival in patients with non-small cell lung cancer treated with surgery. Lung Cancer. 2021;151:84–90.CrossRefPubMed
10.
go back to reference Xu L, Su H, She Y, et al. Which N descriptor is more predictive of prognosis in resected non-small cell lung cancer: the number of involved nodal stations or the location-based pathological N stage? Chest. 2021;159(6):2458–69.CrossRefPubMed Xu L, Su H, She Y, et al. Which N descriptor is more predictive of prognosis in resected non-small cell lung cancer: the number of involved nodal stations or the location-based pathological N stage? Chest. 2021;159(6):2458–69.CrossRefPubMed
11.
go back to reference Rusch VW, Asamura H, Watanabe H, Giroux DJ, Rami-Porta R, Goldstraw P. The IASLC lung cancer staging project: a proposal for a new international lymph node map in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol. 2009;4(5):568–77.CrossRefPubMed Rusch VW, Asamura H, Watanabe H, Giroux DJ, Rami-Porta R, Goldstraw P. The IASLC lung cancer staging project: a proposal for a new international lymph node map in the forthcoming seventh edition of the TNM classification for lung cancer. J Thorac Oncol. 2009;4(5):568–77.CrossRefPubMed
12.
go back to reference Liu C, Wei S, Guo C, Mei J, Pu Q, Liu L. Clinical significance of station 3A lymph node dissection in patients with right-side non-small-cell lung cancer: a retrospective propensity-matched analysis. Annal Surg Oncol. 2021;28(1):194–202.CrossRef Liu C, Wei S, Guo C, Mei J, Pu Q, Liu L. Clinical significance of station 3A lymph node dissection in patients with right-side non-small-cell lung cancer: a retrospective propensity-matched analysis. Annal Surg Oncol. 2021;28(1):194–202.CrossRef
13.
go back to reference Aksoy Y, Çıtak N, Obuz Ç, Metin M, Sayar A. Does anatomical location-based metastatic lymph node density affect prognosis in lung cancer patients? Interact Cardiovasc Thorac Surg. 2021;33(4):541–9.CrossRefPubMedPubMedCentral Aksoy Y, Çıtak N, Obuz Ç, Metin M, Sayar A. Does anatomical location-based metastatic lymph node density affect prognosis in lung cancer patients? Interact Cardiovasc Thorac Surg. 2021;33(4):541–9.CrossRefPubMedPubMedCentral
14.
go back to reference Bertoglio P, Ricciardi S, Alì G, et al. N2 lung cancer is not all the same: an analysis of different prognostic groups. Interact CardioVascular Thorac Surg. 2018;27(5):720–6.CrossRef Bertoglio P, Ricciardi S, Alì G, et al. N2 lung cancer is not all the same: an analysis of different prognostic groups. Interact CardioVascular Thorac Surg. 2018;27(5):720–6.CrossRef
15.
go back to reference Kojima H, Terada Y, Yasuura Y, et al. Prognostic impact of the number of involved lymph node stations in patients with completely resected non-small cell lung cancer: a proposal for future revisions of the N classification. Gen Thorac Cardiovasc Surg. 2020;68(11):1298–304.CrossRefPubMed Kojima H, Terada Y, Yasuura Y, et al. Prognostic impact of the number of involved lymph node stations in patients with completely resected non-small cell lung cancer: a proposal for future revisions of the N classification. Gen Thorac Cardiovasc Surg. 2020;68(11):1298–304.CrossRefPubMed
16.
go back to reference Baba T, Uramoto H, Kuwata T, et al. Survival impact of node zone classification in resected pathological N2 non-small cell lung cancer. Interact Cardiovasc Thorac Surg. 2012;14(6):760–4.CrossRefPubMedPubMedCentral Baba T, Uramoto H, Kuwata T, et al. Survival impact of node zone classification in resected pathological N2 non-small cell lung cancer. Interact Cardiovasc Thorac Surg. 2012;14(6):760–4.CrossRefPubMedPubMedCentral
17.
go back to reference Demir A, Turna A, Kocaturk C, et al. Prognostic significance of surgical-pathologic N1 lymph node involvement in non-small cell lung cancer. Ann Thorac Surg. 2009;87(4):1014–22.CrossRefPubMed Demir A, Turna A, Kocaturk C, et al. Prognostic significance of surgical-pathologic N1 lymph node involvement in non-small cell lung cancer. Ann Thorac Surg. 2009;87(4):1014–22.CrossRefPubMed
18.
go back to reference Eichhorn F, Klotz LV, Muley T, Kobinger S, Winter H, Eichhorn ME. Prognostic relevance of regional lymph-node distribution in patients with N1-positive non-small cell lung cancer: A retrospective single-center analysis. Lung Cancer. 2019;138:95–101.CrossRefPubMed Eichhorn F, Klotz LV, Muley T, Kobinger S, Winter H, Eichhorn ME. Prognostic relevance of regional lymph-node distribution in patients with N1-positive non-small cell lung cancer: A retrospective single-center analysis. Lung Cancer. 2019;138:95–101.CrossRefPubMed
19.
go back to reference Zheng H, Wang LM, Bao F, et al. Re-appraisal of N2 disease by lymphatic drainage pattern for non-small-cell lung cancers: by terms of nodal stations, zones, chains, and a composite. Lung Cancer. 2011;74(3):497–503.CrossRefPubMed Zheng H, Wang LM, Bao F, et al. Re-appraisal of N2 disease by lymphatic drainage pattern for non-small-cell lung cancers: by terms of nodal stations, zones, chains, and a composite. Lung Cancer. 2011;74(3):497–503.CrossRefPubMed
20.
go back to reference Li S, Yan S, Lu F, et al. Validation of the 8th edition nodal staging and proposal of new nodal categories for future edition of the TNM classification of non-small cell lung cancer. Ann Surg Oncol. 2021;28(8):4510–6.CrossRefPubMed Li S, Yan S, Lu F, et al. Validation of the 8th edition nodal staging and proposal of new nodal categories for future edition of the TNM classification of non-small cell lung cancer. Ann Surg Oncol. 2021;28(8):4510–6.CrossRefPubMed
21.
go back to reference Ding X, Hui Z, Dai H, et al. A proposal for combination of lymph node ratio and anatomic location of involved lymph nodes for nodal classification in non-small cell lung cancer. J Thorac Oncol. 2016;11(9):1565–73.CrossRefPubMed Ding X, Hui Z, Dai H, et al. A proposal for combination of lymph node ratio and anatomic location of involved lymph nodes for nodal classification in non-small cell lung cancer. J Thorac Oncol. 2016;11(9):1565–73.CrossRefPubMed
22.
go back to reference Jonnalagadda S, Smith C, Mhango G, Wisnivesky JP. The number of lymph node metastases as a prognostic factor in patients with N1 non-small cell lung cancer. Chest. 2011;140(2):433–40.CrossRefPubMedPubMedCentral Jonnalagadda S, Smith C, Mhango G, Wisnivesky JP. The number of lymph node metastases as a prognostic factor in patients with N1 non-small cell lung cancer. Chest. 2011;140(2):433–40.CrossRefPubMedPubMedCentral
23.
go back to reference Lee JG, Lee CY, Park IK, et al. Number of metastatic lymph nodes in resected non-small cell lung cancer predicts patient survival. Ann Thorac Surg. 2008;85(1):211–5.CrossRefPubMed Lee JG, Lee CY, Park IK, et al. Number of metastatic lymph nodes in resected non-small cell lung cancer predicts patient survival. Ann Thorac Surg. 2008;85(1):211–5.CrossRefPubMed
24.
go back to reference Li F, Yuan L, Zhao Y, Wang S, Lv Z, Mao Y. Comparison of two proposed changes to the current nodal classification for non-small cell lung cancer based on the number and ratio of metastatic lymph nodes. Chest. 2021;160(4):1520–33.CrossRefPubMed Li F, Yuan L, Zhao Y, Wang S, Lv Z, Mao Y. Comparison of two proposed changes to the current nodal classification for non-small cell lung cancer based on the number and ratio of metastatic lymph nodes. Chest. 2021;160(4):1520–33.CrossRefPubMed
25.
go back to reference Maniwa T, Ohmura A, Hiroshima T, et al. Number of metastatic lymph nodes and zones as prognostic factors in non-small-cell lung cancer. Interact Cardiovasc Thorac Surg. 2020;31(3):305–14.CrossRefPubMed Maniwa T, Ohmura A, Hiroshima T, et al. Number of metastatic lymph nodes and zones as prognostic factors in non-small-cell lung cancer. Interact Cardiovasc Thorac Surg. 2020;31(3):305–14.CrossRefPubMed
26.
go back to reference Saji H, Tsuboi M, Shimada Y, et al. A proposal for combination of total number and anatomical location of involved lymph nodes for nodal classification in non-small cell lung cancer. Chest. 2013;143(6):1618–25.CrossRefPubMed Saji H, Tsuboi M, Shimada Y, et al. A proposal for combination of total number and anatomical location of involved lymph nodes for nodal classification in non-small cell lung cancer. Chest. 2013;143(6):1618–25.CrossRefPubMed
27.
go back to reference Lee GD, Kim DK, Moon DH, et al. A comparison of the proposed classifications for the revision of N descriptors for non-small-cell lung cancer. Eur J Cardiothorac Surg. 2016;49(2):580–8.CrossRefPubMed Lee GD, Kim DK, Moon DH, et al. A comparison of the proposed classifications for the revision of N descriptors for non-small-cell lung cancer. Eur J Cardiothorac Surg. 2016;49(2):580–8.CrossRefPubMed
28.
go back to reference Pawełczyk K, Marciniak M, Błasiak P. Evaluation of new classifications of N descriptor in non-small cell lung cancer (NSCLC) based on the number and the ratio of metastatic lymph nodes. J Cardiothorac Surg. 2016;11(1):68.CrossRefPubMedPubMedCentral Pawełczyk K, Marciniak M, Błasiak P. Evaluation of new classifications of N descriptor in non-small cell lung cancer (NSCLC) based on the number and the ratio of metastatic lymph nodes. J Cardiothorac Surg. 2016;11(1):68.CrossRefPubMedPubMedCentral
29.
go back to reference Deng W, Xu T, Wang Y, et al. Log odds of positive lymph nodes may predict survival benefit in patients with node-positive non-small cell lung cancer. Lung Cancer. 2018;122:60–6.CrossRefPubMed Deng W, Xu T, Wang Y, et al. Log odds of positive lymph nodes may predict survival benefit in patients with node-positive non-small cell lung cancer. Lung Cancer. 2018;122:60–6.CrossRefPubMed
30.
go back to reference Dziedzic D, Piotr R, Langfort R, Orlowski T. Log odds of positive lymph nodes as a novel prognostic indicator in NSCLC staging. Surg Oncol. 2017;26(1):80–5.CrossRefPubMed Dziedzic D, Piotr R, Langfort R, Orlowski T. Log odds of positive lymph nodes as a novel prognostic indicator in NSCLC staging. Surg Oncol. 2017;26(1):80–5.CrossRefPubMed
31.
go back to reference Smeltzer MP, Faris NR, Ray MA, Osarogiagbon RU. Association of pathologic nodal staging quality with survival among patients with non-small cell lung cancer after resection with curative intent. JAMA Oncol. 2018;4(1):80.CrossRefPubMed Smeltzer MP, Faris NR, Ray MA, Osarogiagbon RU. Association of pathologic nodal staging quality with survival among patients with non-small cell lung cancer after resection with curative intent. JAMA Oncol. 2018;4(1):80.CrossRefPubMed
32.
go back to reference Smeltzer MP, Faris N, Yu X, et al. Missed intrapulmonary lymph node metastasis and survival after resection of non-small cell lung cancer. Ann Thorac Surg. 2016;102(2):448–53.CrossRefPubMedPubMedCentral Smeltzer MP, Faris N, Yu X, et al. Missed intrapulmonary lymph node metastasis and survival after resection of non-small cell lung cancer. Ann Thorac Surg. 2016;102(2):448–53.CrossRefPubMedPubMedCentral
33.
go back to reference Ramirez RA, Wang CG, Miller LE, et al. Incomplete intrapulmonary lymph node retrieval after routine pathologic examination of resected lung cancer. J Clin Oncol. 2012;30(23):2823–8.CrossRefPubMed Ramirez RA, Wang CG, Miller LE, et al. Incomplete intrapulmonary lymph node retrieval after routine pathologic examination of resected lung cancer. J Clin Oncol. 2012;30(23):2823–8.CrossRefPubMed
34.
go back to reference Ray MA, Fehnel C, Akinbobola O, et al. Comparative effectiveness of a lymph node collection kit versus heightened awareness on lung cancer surgery quality and outcomes. J Thorac Oncol. 2021;16(5):774–83.CrossRefPubMedPubMedCentral Ray MA, Fehnel C, Akinbobola O, et al. Comparative effectiveness of a lymph node collection kit versus heightened awareness on lung cancer surgery quality and outcomes. J Thorac Oncol. 2021;16(5):774–83.CrossRefPubMedPubMedCentral
Metadata
Title
A Comprehensive Comparison of Different Nodal Subclassification Methods in Surgically Resected Non-Small-Cell Lung Cancer Patients
Authors
Zihuai Wang, MD
Zhenyu Yang, MD
Sijia Li, MD
Junqi Zhang, MD
Liang Xia, MD
Jian Zhou, MD
Nan Chen, MD
Chenglin Guo, MD
Lunxu Liu, MD, PhD, FRCS
Publication date
18-08-2022
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 13/2022
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-022-12363-w

Other articles of this Issue 13/2022

Annals of Surgical Oncology 13/2022 Go to the issue