Impact of tumor spread through air spaces on surgical decision-making and accuracy of identifying spread through air spaces on frozen sections: A systematic review and meta-analysis_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

XU Yi ¹ , CHEN Donglai ² , XU Xuejun ¹ , ZHANG Yongsheng ³ , DUAN Shanzhou ¹ ,  CHEN Yongbing ¹ , TAN Lijie ²

1. Department of Thoracic and Cardiac Surgery, The Second Affiliated Hospital of Soochow University, Suzhou, 215004, Jiangsu, P. R. China;
2. Department of Thoracic Surgery, Zhongshan Hospital, Fudan University, Shanghai, 200032, P. R. China;
3. Department of Pathology, The Second Affiliated Hospital of Soochow University, Suzhou, 215004, Jiangsu, P. R. China;

Corresponding author：

CHEN Yongbing, Email: chentongt@sina.com

Keywords：

Non-small cell lung cancer; spread through air spaces; sublobar resection; lobectomy; prognosis; frozen sections; systematic review/meta-analysis

DOI：

10.7507/1007-4848.202211048

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Objective To investigate the significance of spread through air spaces (STAS) in early-stage non-small cell lung cancer (NSCLC) patients undergoing either sublobar resection or lobectomy by pooling evidence available, and to assess the accuracy of frozen sections in determining types of resection among patients with suspected presence of STAS. Methods Studies were identified by searching databases including PubMed, EMbase, Web of Science, and The Cochrane Library from inception to July 2022. Two researchers independently searched, screened, evaluated literature, and extracted data. Statistical analysis was conducted using RevMan 5.4 and STATA 15.0. The Newcastle-Ottawa Scale (NOS) was used to evaluate the quality of the study. Results A total of 26 studies involving 23 surgical related studies (12 266 patients) were included, among which, 11 compared the outcomes of lobectomy with sublobar resection in the STAS-positive patients. NOS score≥6 points. Meta-analysis indicated that presence of STAS shortened patients' survival in both lobectomy group and sublobar resection group (RFS: HR=2.27, 95%CI 1.96-2.63, P＜0.01; OS: HR=2.08, 95%CI 1.74-2.49, P＜0.01). Moreover, lobectomy brought additional survival benefits to STAS-positive patients compared with sublobar resection (RFS: HR=1.97, 95%CI 1.59-2.44, P＜0.01; OS: HR=1.91, 95%CI 1.47-2.48, P＜0.01). Four studies were included to assess the accuracy of identifying presence of STAS on intraoperative frozen sections, of which the pooled sensitivity reached 55% (95%CI 45%-64%), the pooled specificity reached 92% (95%CI 77%-97%), and the pooled area under the curve was 0.68 (95%CI 0.64-0.72) based on the data available. Conclusion This study confirms that presence of STAS is a critical risk factor for patients with early-stage NSCLC. Lobectomy should be recommended as the first choice when presence of STAS is identified on frozen sections, as lobectomy can prolong patients' survival compared with sublobar resection in STAS-positive disease. The specificity of identifying STAS on frozen sections seems to be satisfactory, which may be helpful in determining types of resection. However, more robust methods are urgently in need to make up for the limited sensitivity and accuracy of frozen sections.

Citation： XU Yi, CHEN Donglai, XU Xuejun, ZHANG Yongsheng, DUAN Shanzhou, CHEN Yongbing, TAN Lijie. Impact of tumor spread through air spaces on surgical decision-making and accuracy of identifying spread through air spaces on frozen sections: A systematic review and meta-analysis. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(6): 900-909. doi: 10.7507/1007-4848.202211048 Copy

1.	Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Abate D, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: A systematic analysis for the global burden of disease study. JAMA Oncol, 2019, 5(12): 1749-1768.
2.	Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin, 2021, 71(1): 7-33.
3.	Hartwig MG, D'Amico TA. Thoracoscopic lobectomy: The gold standard for early-stage lung cancer? Ann Thorac Surg, 2010, 89(6): S2098-S2101.
4.	Howington JA, Blum MG, Chang AC, et al. Treatment of stage Ⅰ and Ⅱnon-small cell 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): e278S-e313S.
5.	Altorki NK, Wang X, Kozono D. PL03.06 Lobar or sub-lobar resection for peripheral clinical stageⅠA = 2 cm non-small cell lung cancer (NSCLC): Results from an international randomized phaseⅢ trial (CALGB 140503 [Alliance]). J Thorac Oncol, 2022, 17(9): S1-S2.
6.	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.
7.	Kadota K, Kushida Y, Kagawa S, et al. Limited resection is associated with a higher risk of locoregional recurrence than lobectomy in stage Ⅰ lung adenocarcinoma with tumor spread through air spaces. Am J Surg Pathol, 2019, 43(8): 1033-1041.
8.	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.
9.	Warth A. Spread through air spaces (STAS): A comprehensive update. Transl Lung Cancer Res, 2017, 6(5): 501-507.
10.	Weiss K, Rochefort MM. Spread through air spaces-positive T1 lung adenocarcinoma: Is lobectomy associated with better outcomes than sublobar resection? Ann Transl Med, 2019, 7(Suppl 3): S126.
11.	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.
12.	Kadota K, Kushida Y, Katsuki N, et al. Tumor spread through air spaces is an independent predictor of recurrence-free survival in patients with resected lung squamous cell carcinoma. Am J Surg Pathol, 2017, 41(8): 1077-1086.
13.	Bains S, Eguchi T, Warth A, et al. Procedure-specific risk prediction for recurrence in patients undergoing lobectomy or sublobar resection for small (≤2 cm) lung adenocarcinoma: An international cohort analysis. J Thorac Oncol, 2019, 14(1): 72-86.
14.	Warth A, Beasley MB, Mino-Kenudson M. Breaking new ground: The evolving concept of spread through air spaces (STAS). J Thorac Oncol, 2017, 12(2): 176-178.
15.	陈东来, 戴晨阳, 西尔买买提·卡德尔, 等. 肺癌气腔扩散的研究进展. 中华胸心血管外科杂志, 2017, 33(11): 697-700.
16.	Chen D, She Y, Wang T, et al. Radiomics-based prediction for tumour spread through air spaces in stage Ⅰ lung adenocarcinoma using machine learning. Eur J Cardiothorac Surg, 2020, 58(1): 51-58.
17.	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.
18.	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.
19.	Li J, Wang Y, Li J, et al. Meta-analysis of lobectomy and sublobar resection for stage Ⅰ non-small cell lung cancer with spread through air spaces. Clin Lung Cancer, 2022, 23(3): 208-213.
20.	Toyokawa G, Yamada Y, Tagawa T, et al. Computed tomography features of resected lung adenocarcinomas with spread through air spaces. J Thorac Cardiovasc Surg, 2018, 156(4): 1670-1676.
21.	Kim SK, Kim TJ, Chung MJ, et al. Lung adenocarcinoma: CT features associated with spread through air spaces. Radiology, 2018, 289(3): 831-840.
22.	de Margerie-Mellon C, Onken A, Heidinger BH, et al. CT manifestations of tumor spread through airspaces in pulmonary adenocarcinomas presenting as subsolid nodules. J Thorac Imaging, 2018, 33(6): 402-408.
23.	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.
24.	Zhu E, Xie H, Dai C, et al. Intraoperatively measured tumor size and frozen section results should be considered jointly to predict the final pathology for lung adenocarcinoma. Mod Pathol, 2018, 31(9): 1391-1399.
25.	Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
26.	Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
27.	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.
28.	Yanagawa N, Shiono S, Endo M, et al. Tumor spread through air spaces is a useful predictor of recurrence and prognosis in stageⅠ lung squamous cell carcinoma, but not in stage Ⅱand Ⅲ. Lung Cancer, 2018, 120: 14-21.
29.	Dai C, Xie H, Su H, et al. Tumor spread through air spaces affects the recurrence and overall survival in patients with lung adenocarcinoma >2 to 3 cm. J Thorac Oncol, 2017, 12(7): 1052-1060.
30.	Han YB, Kim H, Mino-Kenudson M, et al. Tumor spread through air spaces (STAS): Prognostic significance of grading in non-small cell lung cancer. Mod Pathol, 2021, 34(3): 549-561.
31.	Koezuka S, Mikami T, Tochigi N, et al. Toward improving prognosis prediction in patients undergoing small lung adenocarcinoma resection: Radiological and pathological assessment of diversity and intratumor heterogeneity. Lung Cancer, 2019, 135: 40-46.
32.	Yang L, Yang Y, Ma P, et al. Spread through air spaces predicts a worse survival in patients with stage Ⅰadenocarcinomas >2 cm after radical lobectomy. J Thorac Dis, 2018, 10(9): 5308-5317.
33.	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.
34.	Shiono S, Endo M, Suzuki K, et al. Spread through air spaces affects survival and recurrence of patients with clinical stage ⅠA non-small cell lung cancer after wedge resection. J Thorac Dis, 2020, 12(5): 2247-2260.
35.	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.
36.	Ikeda T, Kadota K, Go T, et al. Segmentectomy provides comparable outcomes to lobectomy for stage ⅠA non-small cell lung cancer with spread through air spaces. Semin Thorac Cardiovasc Surg, 2023, 35(1): 156-163.
37.	Onozato Y, Nakajima T, Yokota H, et al. Radiomics is feasible for prediction of spread through air spaces in patients with nonsmall cell lung cancer. Sci Rep, 2021, 11(1): 13526.
38.	Chae M, Jeon JH, Chung JH, et al. Prognostic significance of tumor spread through air spaces in patients with stage ⅠA part-solid lung adenocarcinoma after sublobar resection. Lung Cancer, 2021, 152: 21-26.
39.	Chen S, Ye T, Yang S, et al. Prognostic implication of tumor spread through air spaces in patients with pathologic N0 lung adenocarcinoma. Lung Cancer, 2022, 164: 33-38.
40.	Mantovani S, Pernazza A, Bassi M, et al. Prognostic impact of spread through air spaces in lung adenocarcinoma. Interact Cardiovasc Thorac Surg, 2022, 34(6): 1011-1015.
41.	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.
42.	Hara K, Mizuguchi S, Okada S, et al. Intensity of SLX predicts distance of tumor spread through alveolar spaces in stageⅠlung adenocarcinoma. Thorac Cancer, 2019, 10(4): 832-838.
43.	Chen D, Wang X, Zhang F, et al. Could tumor spread through air spaces benefit from adjuvant chemotherapy in stageⅠ lung adenocarcinoma? A multi-institutional study. Ther Adv Med Oncol, 2020, 12: 1758835920978147.
44.	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.
45.	Walts AE, Marchevsky AM. Current evidence does not warrant frozen section evaluation for the presence of tumor spread through alveolar spaces. Arch Pathol Lab Med, 2018, 142(1): 59-63.
46.	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.
47.	Chen D, Mao Y, Wen J, et al. Tumor spread through air spaces in non-small cell lung cancer: A systematic review and meta-analysis. Ann Thorac Surg, 2019, 108(3): 945-954.
48.	Liu H, Yin Q, Yang G, et al. Prognostic impact of tumor spread through air spaces in non-small cell lung cancers: A meta-analysis including 3564 patients. Pathol Oncol Res, 2019, 25(4): 1303-1310.
49.	Wang S, Hao J, Qian C, et al. Tumor spread through air spaces is a survival predictor in non-small-cell lung cancer. Clin Lung Cancer, 2019, 20(5): e584-e591.
50.	Matsuoka S, Eguchi T, Iwaya M, et al. P2.12-02 Immune-cell distribution between tumor edge and center affects lung cancer aggressiveness—Multiplex immunofluorescence. J Thorac Oncol, 2022, 17(9): S150-S151.
51.	Eguchi T, Matsuoka S, Iwaya M, et al. MA03.07 Accurate intraoperative diagnosis of spread through air spaces (STAS) using a cryo embedding medium inflation method. J Thorac Oncol, 2022, 17(9): S52.
52.	Blaauwgeers H, Flieder D, Warth A, et al. A prospective study of loose tissue fragments in non-small cell lung cancer resection specimens: An alternative view to "spread through air spaces". Am J Surg Pathol, 2017, 41(9): 1226-1230.
53.	Blaauwgeers H, Russell PA, Jones KD, et al. Pulmonary loose tumor tissue fragments and spread through air spaces (STAS): Invasive pattern or artifact? A critical review. Lung Cancer, 2018, 123: 107-111.
54.	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.
55.	Wang X, Chen D, Wen J, et al. Benefit of adjuvant chemotherapy for patients with stage ⅠB non-small cell lung cancer: A systematic review and meta-analysis. Ann Transl Med, 2021, 9(18): 1430.
56.	Qian F, Yang W, Wang R, et al. Prognostic significance and adjuvant chemotherapy survival benefits of a solid or micropapillary pattern in patients with resected stage ⅠB lung adenocarcinoma. J Thorac Cardiovasc Surg, 2018, 155(3): 1227-1235.

1. Global Burden of Disease Cancer Collaboration, Fitzmaurice C, Abate D, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life-years for 29 cancer groups, 1990 to 2017: A systematic analysis for the global burden of disease study. JAMA Oncol, 2019, 5(12): 1749-1768.
2. Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2021. CA Cancer J Clin, 2021, 71(1): 7-33.
3. Hartwig MG, D'Amico TA. Thoracoscopic lobectomy: The gold standard for early-stage lung cancer? Ann Thorac Surg, 2010, 89(6): S2098-S2101.
4. Howington JA, Blum MG, Chang AC, et al. Treatment of stage Ⅰ and Ⅱnon-small cell 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): e278S-e313S.
5. Altorki NK, Wang X, Kozono D. PL03.06 Lobar or sub-lobar resection for peripheral clinical stageⅠA = 2 cm non-small cell lung cancer (NSCLC): Results from an international randomized phaseⅢ trial (CALGB 140503 [Alliance]). J Thorac Oncol, 2022, 17(9): S1-S2.
6. 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.
7. Kadota K, Kushida Y, Kagawa S, et al. Limited resection is associated with a higher risk of locoregional recurrence than lobectomy in stage Ⅰ lung adenocarcinoma with tumor spread through air spaces. Am J Surg Pathol, 2019, 43(8): 1033-1041.
8. 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.
9. Warth A. Spread through air spaces (STAS): A comprehensive update. Transl Lung Cancer Res, 2017, 6(5): 501-507.
10. Weiss K, Rochefort MM. Spread through air spaces-positive T1 lung adenocarcinoma: Is lobectomy associated with better outcomes than sublobar resection? Ann Transl Med, 2019, 7(Suppl 3): S126.
11. 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.
12. Kadota K, Kushida Y, Katsuki N, et al. Tumor spread through air spaces is an independent predictor of recurrence-free survival in patients with resected lung squamous cell carcinoma. Am J Surg Pathol, 2017, 41(8): 1077-1086.
13. Bains S, Eguchi T, Warth A, et al. Procedure-specific risk prediction for recurrence in patients undergoing lobectomy or sublobar resection for small (≤2 cm) lung adenocarcinoma: An international cohort analysis. J Thorac Oncol, 2019, 14(1): 72-86.
14. Warth A, Beasley MB, Mino-Kenudson M. Breaking new ground: The evolving concept of spread through air spaces (STAS). J Thorac Oncol, 2017, 12(2): 176-178.
15. 陈东来, 戴晨阳, 西尔买买提·卡德尔, 等. 肺癌气腔扩散的研究进展. 中华胸心血管外科杂志, 2017, 33(11): 697-700.
16. Chen D, She Y, Wang T, et al. Radiomics-based prediction for tumour spread through air spaces in stage Ⅰ lung adenocarcinoma using machine learning. Eur J Cardiothorac Surg, 2020, 58(1): 51-58.
17. 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.
18. 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.
19. Li J, Wang Y, Li J, et al. Meta-analysis of lobectomy and sublobar resection for stage Ⅰ non-small cell lung cancer with spread through air spaces. Clin Lung Cancer, 2022, 23(3): 208-213.
20. Toyokawa G, Yamada Y, Tagawa T, et al. Computed tomography features of resected lung adenocarcinomas with spread through air spaces. J Thorac Cardiovasc Surg, 2018, 156(4): 1670-1676.
21. Kim SK, Kim TJ, Chung MJ, et al. Lung adenocarcinoma: CT features associated with spread through air spaces. Radiology, 2018, 289(3): 831-840.
22. de Margerie-Mellon C, Onken A, Heidinger BH, et al. CT manifestations of tumor spread through airspaces in pulmonary adenocarcinomas presenting as subsolid nodules. J Thorac Imaging, 2018, 33(6): 402-408.
23. 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.
24. Zhu E, Xie H, Dai C, et al. Intraoperatively measured tumor size and frozen section results should be considered jointly to predict the final pathology for lung adenocarcinoma. Mod Pathol, 2018, 31(9): 1391-1399.
25. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol, 2010, 25(9): 603-605.
26. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414): 557-560.
27. 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.
28. Yanagawa N, Shiono S, Endo M, et al. Tumor spread through air spaces is a useful predictor of recurrence and prognosis in stageⅠ lung squamous cell carcinoma, but not in stage Ⅱand Ⅲ. Lung Cancer, 2018, 120: 14-21.
29. Dai C, Xie H, Su H, et al. Tumor spread through air spaces affects the recurrence and overall survival in patients with lung adenocarcinoma >2 to 3 cm. J Thorac Oncol, 2017, 12(7): 1052-1060.
30. Han YB, Kim H, Mino-Kenudson M, et al. Tumor spread through air spaces (STAS): Prognostic significance of grading in non-small cell lung cancer. Mod Pathol, 2021, 34(3): 549-561.
31. Koezuka S, Mikami T, Tochigi N, et al. Toward improving prognosis prediction in patients undergoing small lung adenocarcinoma resection: Radiological and pathological assessment of diversity and intratumor heterogeneity. Lung Cancer, 2019, 135: 40-46.
32. Yang L, Yang Y, Ma P, et al. Spread through air spaces predicts a worse survival in patients with stage Ⅰadenocarcinomas >2 cm after radical lobectomy. J Thorac Dis, 2018, 10(9): 5308-5317.
33. 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.
34. Shiono S, Endo M, Suzuki K, et al. Spread through air spaces affects survival and recurrence of patients with clinical stage ⅠA non-small cell lung cancer after wedge resection. J Thorac Dis, 2020, 12(5): 2247-2260.
35. 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.
36. Ikeda T, Kadota K, Go T, et al. Segmentectomy provides comparable outcomes to lobectomy for stage ⅠA non-small cell lung cancer with spread through air spaces. Semin Thorac Cardiovasc Surg, 2023, 35(1): 156-163.
37. Onozato Y, Nakajima T, Yokota H, et al. Radiomics is feasible for prediction of spread through air spaces in patients with nonsmall cell lung cancer. Sci Rep, 2021, 11(1): 13526.
38. Chae M, Jeon JH, Chung JH, et al. Prognostic significance of tumor spread through air spaces in patients with stage ⅠA part-solid lung adenocarcinoma after sublobar resection. Lung Cancer, 2021, 152: 21-26.
39. Chen S, Ye T, Yang S, et al. Prognostic implication of tumor spread through air spaces in patients with pathologic N0 lung adenocarcinoma. Lung Cancer, 2022, 164: 33-38.
40. Mantovani S, Pernazza A, Bassi M, et al. Prognostic impact of spread through air spaces in lung adenocarcinoma. Interact Cardiovasc Thorac Surg, 2022, 34(6): 1011-1015.
41. 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.
42. Hara K, Mizuguchi S, Okada S, et al. Intensity of SLX predicts distance of tumor spread through alveolar spaces in stageⅠlung adenocarcinoma. Thorac Cancer, 2019, 10(4): 832-838.
43. Chen D, Wang X, Zhang F, et al. Could tumor spread through air spaces benefit from adjuvant chemotherapy in stageⅠ lung adenocarcinoma? A multi-institutional study. Ther Adv Med Oncol, 2020, 12: 1758835920978147.
44. 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.
45. Walts AE, Marchevsky AM. Current evidence does not warrant frozen section evaluation for the presence of tumor spread through alveolar spaces. Arch Pathol Lab Med, 2018, 142(1): 59-63.
46. 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.
47. Chen D, Mao Y, Wen J, et al. Tumor spread through air spaces in non-small cell lung cancer: A systematic review and meta-analysis. Ann Thorac Surg, 2019, 108(3): 945-954.
48. Liu H, Yin Q, Yang G, et al. Prognostic impact of tumor spread through air spaces in non-small cell lung cancers: A meta-analysis including 3564 patients. Pathol Oncol Res, 2019, 25(4): 1303-1310.
49. Wang S, Hao J, Qian C, et al. Tumor spread through air spaces is a survival predictor in non-small-cell lung cancer. Clin Lung Cancer, 2019, 20(5): e584-e591.
50. Matsuoka S, Eguchi T, Iwaya M, et al. P2.12-02 Immune-cell distribution between tumor edge and center affects lung cancer aggressiveness—Multiplex immunofluorescence. J Thorac Oncol, 2022, 17(9): S150-S151.
51. Eguchi T, Matsuoka S, Iwaya M, et al. MA03.07 Accurate intraoperative diagnosis of spread through air spaces (STAS) using a cryo embedding medium inflation method. J Thorac Oncol, 2022, 17(9): S52.
52. Blaauwgeers H, Flieder D, Warth A, et al. A prospective study of loose tissue fragments in non-small cell lung cancer resection specimens: An alternative view to "spread through air spaces". Am J Surg Pathol, 2017, 41(9): 1226-1230.
53. Blaauwgeers H, Russell PA, Jones KD, et al. Pulmonary loose tumor tissue fragments and spread through air spaces (STAS): Invasive pattern or artifact? A critical review. Lung Cancer, 2018, 123: 107-111.
54. 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.
55. Wang X, Chen D, Wen J, et al. Benefit of adjuvant chemotherapy for patients with stage ⅠB non-small cell lung cancer: A systematic review and meta-analysis. Ann Transl Med, 2021, 9(18): 1430.
56. Qian F, Yang W, Wang R, et al. Prognostic significance and adjuvant chemotherapy survival benefits of a solid or micropapillary pattern in patients with resected stage ⅠB lung adenocarcinoma. J Thorac Cardiovasc Surg, 2018, 155(3): 1227-1235.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Impact of tumor spread through air spaces on surgical decision-making and accuracy of identifying spread through air spaces on frozen sections: A systematic review and meta-analysis

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