Prognostic impact of lymph node dissection modality in patients with STAS-positive ≤2 cm stage ⅠA lung adenocarcinoma_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

CHEN Xiao ¹ , ZHOU Hangcheng ² , WU Mingsheng ¹ , XU Meiqing ¹ , LI Tian ¹ , SUN Xiaohui ¹ , ZHANG Zekai ¹ , WANG Yu ¹ ,  XIE Mingran ¹

1. Department of Thoracic Surgery, The First Affiliated Hospital of University of Science and Technology of China, Division of Life Science and Medicine, University of Science and Technology of China, Hefei, 230000, P. R. China;
2. Department of Pathology, The First Affiliated Hospital of University of Science and Technology of China, Division of Life Science and Medicine, University of Science and Technology of China, Hefei, 230000, P. R. China;

Corresponding author：

XIE Mingran, Email: xmr1981@ustc.edu.cn

Keywords：

Lung adenocarcinoma; spread through air space; lymph node dissection modality; prognosis

DOI：

10.7507/1007-4848.202409042

Video：

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Objective To investigate the effect of different lymph node dissection methods on the prognosis of patients with stage ⅠA spread through air space (STAS)-positive lung adenocarcinoma≤ 2 cm. Methods Clinical data of 3148 patients with lung adenocarcinoma who underwent surgery at the Department of Thoracic Surgery, the First Affiliated Hospital of University of Science and Technology of China from 2016 to 2018 were retrospectively analyzed. Patients with stage ⅠA STAS-positive lung adenocarcinoma≤ 2 cm were included and divided into two groups based on lymph node dissection methods: systematic lymph node dissection group and limited lymph node dissection group. Compare the clinical and pathological data of two groups of patients and use Cox proportional hazards regression model for multivariate survival analysis. Results A total of 209 STAS-positive patients were enrolled in the study, including 98 males and 111 females, aged 28-83 (60.42±10.15) years. Univariate analysis showed that the mode of lymph node dissection, past history, micropapillary histological subtype, and papillary histological subtype were risk factors for patient prognosis. Multifactorial analysis showed that lymph node dissection method, past history, and solid-type histological subtype were risk factors for patient prognosis. Meanwhile, among STAS-positive patients, systematic lymph node dissection had a better prognosis than limited lymph node dissection patients. Conclusion STAS plays an important role in patient prognosis as an independent risk factor for prognosis of stage ⅠA ≤2 cm lung adenocarcinoma. When STAS is positive, the choice of systematic lymph node dissection may be more favourable to patients' long-term prognosis.

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.	Yun JK, Lee GD, Choi S, et al. Comparison of prognostic impact of lymphovascular invasion in stage ⅠA non-small cell lung cancer after lobectomy versus sublobar resection: A propensity score-matched analysis. Lung Cancer, 2020, 146: 105-111.
3.	Kadota K, Nitadori JI, Sima CS, et al. Tumor spread through air spaces is an important pattern of invasion and impacts the frequency and location of recurrences after limited resection for small stage Ⅰ lung adenocarcinomas. J Thorac Oncol, 2015, 10(5): 806-814.
4.	Toyokawa G, Yamada Y, Tagawa T, et al. Significance of spread through air spaces in early-stage lung adenocarcinomas undergoing limited resection. Thorac Cancer, 2018, 9(10): 1255-1261.
5.	Travis WD, Brambilla E, Nicholson AG, et al. The 2015 World Health Organization classification of lung tumors: Impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol, 2015, 10(9): 1243-1260.
6.	Vaghjiani RG, Takahashi Y, Eguchi T, et al. Tumor spread through air spaces is a predictor of occult lymph node metastasis in clinical stage ⅠA lung adenocarcinoma. J Thorac Oncol, 2020, 15(5): 792-802.
7.	Toyokawa G, Yamada Y, Tagawa T, et al. Significance of spread through air spaces in resected pathological stage Ⅰ lung adenocarcinoma. Ann Thorac Surg, 2018, 105(6): 1655-1663.
8.	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.
9.	Shimomura M, Miyagawa-Hayashino A, Omatsu I, et al. Spread through air spaces is a powerful prognostic predictor in patients with completely resected pathological stage Ⅰlung adenocarcinoma. Lung Cancer, 2022, 174: 165-171.
10.	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.
11.	Sun W, Su H, Liu J, et al. Impact of histological components on selecting limited lymphadenectomy for lung adenocarcinoma ≤ 2 cm. Lung Cancer, 2020, 150: 36-43.
12.	Hung JJ, Yeh YC, Jeng WJ, et al. Predictive value of the international association for the study of lung cancer/American Thoracic Society/European Respiratory Society classification of lung adenocarcinoma in tumor recurrence and patient survival. J Clin Oncol, 2014, 32(22): 2357-2364.
13.	Chen X, Zhou H, Wu M, et al. Prognostic impact of spread through air spaces in patients with ≤2 cm stage ⅠA lung adenocarcinoma. J Thorac Dis, 2024, 16(4): 2432-2442.
14.	Kagimoto A, Tsutani Y, Kushitani K, et al. Segmentectomy vs lobectomy for clinical stage ⅠA lung adenocarcinoma with spread through air spaces. Ann Thorac Surg, 2021, 112(3): 935-943.
15.	Gross DJ, Hsieh MS, Li Y, et al. Spread through air spaces (STAS) in non-small cell lung carcinoma: Evidence supportive of an in vivo phenomenon. Am J Surg Pathol, 2021, 45(11): 1509-1515.
16.	Ren Y, Xie H, Dai C, et al. Prognostic impact of tumor spread through air spaces in sublobar resection for 1A lung adenocarcinoma patients. Ann Surg Oncol, 2019, 26(6): 1901-1908.
17.	Jung W, Chung JH, Yum S, et al. The differential prognostic impact of spread through air spaces in early-stage lung adenocarcinoma after lobectomy according to the pT descriptor. J Thorac Cardiovasc Surg, 2022, 163(1): 277-284.
18.	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.
19.	Yoshida C, Kadota K, Ikeda T, et al. Tumor-associated macrophage infiltration is associated with a higher rate of tumor spread through air spaces in resected lung adenocarcinomas. Lung Cancer, 2021, 158: 91-96.
20.	Yagi Y, Aly RG, Tabata K, et al. Three-Dimensional histologic, immunohistochemical, and multiplex immunofluorescence analyses of dynamic vessel co-option of spread through air spaces in lung adenocarcinoma. J Thorac Oncol, 2020, 15(4): 589-600.
21.	Shiono S, Endo M, Suzuki K, et al. Spread through air spaces is a prognostic factor in sublobar resection of non-small cell lung cancer. Ann Thorac Surg, 2018, 106(2): 354-360.
22.	Ding Y, Chen Y, Wen H, et al. Pretreatment prediction of tumour spread through air spaces in clinical stage Ⅰ non-small-cell lung cancer. Eur J Cardiothorac Surg, 2022, 62(3): ezac248.
23.	Uruga H, Fujii T, Fujimori S, et al. Semiquantitative assessment of tumor spread through air spaces (STAS) in early-stage lung adenocarcinomas. J Thorac Oncol, 2017, 12(7): 1046-1051.
24.	Chen Z, Wu X, Fang T, et al. Prognostic impact of tumor spread through air spaces for T2aN0 stage ⅠB non-small cell lung cancer. Cancer Med, 2023, 12(14): 15246-15255.
25.	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.
26.	Zhou F, Villalba JA, Sayo TMS, et al. Assessment of the feasibility of frozen sections for the detection of spread through air spaces (STAS) in pulmonary adenocarcinoma. Mod Pathol, 2022, 35(2): 210-217.
27.	Gao Z, An P, Li R, et al. Development and validation of a clinic-radiological model to predict tumor spread through air spaces in stageⅠ lung adenocarcinoma. Cancer Imaging, 2024, 24(1): 25.
28.	Jin W, Shen L, Tian Y, et al. Improving the prediction of spreading through air spaces (STAS) in primary lung cancer with a dynamic dual-delta hybrid machine learning model: A multicenter cohort study. Biomark Res, 2023, 11(1): 102.

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. Yun JK, Lee GD, Choi S, et al. Comparison of prognostic impact of lymphovascular invasion in stage ⅠA non-small cell lung cancer after lobectomy versus sublobar resection: A propensity score-matched analysis. Lung Cancer, 2020, 146: 105-111.
3. Kadota K, Nitadori JI, Sima CS, et al. Tumor spread through air spaces is an important pattern of invasion and impacts the frequency and location of recurrences after limited resection for small stage Ⅰ lung adenocarcinomas. J Thorac Oncol, 2015, 10(5): 806-814.
4. Toyokawa G, Yamada Y, Tagawa T, et al. Significance of spread through air spaces in early-stage lung adenocarcinomas undergoing limited resection. Thorac Cancer, 2018, 9(10): 1255-1261.
5. Travis WD, Brambilla E, Nicholson AG, et al. The 2015 World Health Organization classification of lung tumors: Impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol, 2015, 10(9): 1243-1260.
6. Vaghjiani RG, Takahashi Y, Eguchi T, et al. Tumor spread through air spaces is a predictor of occult lymph node metastasis in clinical stage ⅠA lung adenocarcinoma. J Thorac Oncol, 2020, 15(5): 792-802.
7. Toyokawa G, Yamada Y, Tagawa T, et al. Significance of spread through air spaces in resected pathological stage Ⅰ lung adenocarcinoma. Ann Thorac Surg, 2018, 105(6): 1655-1663.
8. 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.
9. Shimomura M, Miyagawa-Hayashino A, Omatsu I, et al. Spread through air spaces is a powerful prognostic predictor in patients with completely resected pathological stage Ⅰlung adenocarcinoma. Lung Cancer, 2022, 174: 165-171.
10. 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.
11. Sun W, Su H, Liu J, et al. Impact of histological components on selecting limited lymphadenectomy for lung adenocarcinoma ≤ 2 cm. Lung Cancer, 2020, 150: 36-43.
12. Hung JJ, Yeh YC, Jeng WJ, et al. Predictive value of the international association for the study of lung cancer/American Thoracic Society/European Respiratory Society classification of lung adenocarcinoma in tumor recurrence and patient survival. J Clin Oncol, 2014, 32(22): 2357-2364.
13. Chen X, Zhou H, Wu M, et al. Prognostic impact of spread through air spaces in patients with ≤2 cm stage ⅠA lung adenocarcinoma. J Thorac Dis, 2024, 16(4): 2432-2442.
14. Kagimoto A, Tsutani Y, Kushitani K, et al. Segmentectomy vs lobectomy for clinical stage ⅠA lung adenocarcinoma with spread through air spaces. Ann Thorac Surg, 2021, 112(3): 935-943.
15. Gross DJ, Hsieh MS, Li Y, et al. Spread through air spaces (STAS) in non-small cell lung carcinoma: Evidence supportive of an in vivo phenomenon. Am J Surg Pathol, 2021, 45(11): 1509-1515.
16. Ren Y, Xie H, Dai C, et al. Prognostic impact of tumor spread through air spaces in sublobar resection for 1A lung adenocarcinoma patients. Ann Surg Oncol, 2019, 26(6): 1901-1908.
17. Jung W, Chung JH, Yum S, et al. The differential prognostic impact of spread through air spaces in early-stage lung adenocarcinoma after lobectomy according to the pT descriptor. J Thorac Cardiovasc Surg, 2022, 163(1): 277-284.
18. 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.
19. Yoshida C, Kadota K, Ikeda T, et al. Tumor-associated macrophage infiltration is associated with a higher rate of tumor spread through air spaces in resected lung adenocarcinomas. Lung Cancer, 2021, 158: 91-96.
20. Yagi Y, Aly RG, Tabata K, et al. Three-Dimensional histologic, immunohistochemical, and multiplex immunofluorescence analyses of dynamic vessel co-option of spread through air spaces in lung adenocarcinoma. J Thorac Oncol, 2020, 15(4): 589-600.
21. Shiono S, Endo M, Suzuki K, et al. Spread through air spaces is a prognostic factor in sublobar resection of non-small cell lung cancer. Ann Thorac Surg, 2018, 106(2): 354-360.
22. Ding Y, Chen Y, Wen H, et al. Pretreatment prediction of tumour spread through air spaces in clinical stage Ⅰ non-small-cell lung cancer. Eur J Cardiothorac Surg, 2022, 62(3): ezac248.
23. Uruga H, Fujii T, Fujimori S, et al. Semiquantitative assessment of tumor spread through air spaces (STAS) in early-stage lung adenocarcinomas. J Thorac Oncol, 2017, 12(7): 1046-1051.
24. Chen Z, Wu X, Fang T, et al. Prognostic impact of tumor spread through air spaces for T2aN0 stage ⅠB non-small cell lung cancer. Cancer Med, 2023, 12(14): 15246-15255.
25. 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.
26. Zhou F, Villalba JA, Sayo TMS, et al. Assessment of the feasibility of frozen sections for the detection of spread through air spaces (STAS) in pulmonary adenocarcinoma. Mod Pathol, 2022, 35(2): 210-217.
27. Gao Z, An P, Li R, et al. Development and validation of a clinic-radiological model to predict tumor spread through air spaces in stageⅠ lung adenocarcinoma. Cancer Imaging, 2024, 24(1): 25.
28. Jin W, Shen L, Tian Y, et al. Improving the prediction of spreading through air spaces (STAS) in primary lung cancer with a dynamic dual-delta hybrid machine learning model: A multicenter cohort study. Biomark Res, 2023, 11(1): 102.

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