Expert consensus of thoracic surgeons on guiding surgical decision-making based on intraoperative frozen sections for peripheral pulmonary nodules with diameter≤2 cm_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

 Thoracic Surgery Branch of Shanghai Medical Association, Thoracic Surgeons Branch of Shanghai Medical Doctor Association, The Specialist Alliance of Clinical Skills Promotion and Enhancement for General Thoracic Surgery

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

Corresponding author：

Thoracic Surgery Branch of Shanghai Medical Association, Thoracic Surgeons Branch of Shanghai Medical Doctor Association, The Specialist Alliance of Clinical Skills Promotion and Enhancement for General Thoracic Surgery, Email: chenthoracic@163.com

Keywords：

Pulmonary nodules; non-small cell lung cancer; frozen section; expert consensus

DOI：

10.7507/1007-4848.202204098

Video：

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Surgical resection is the only radical method for the treatment of early-stage non-small cell lung cancer. Intraoperative frozen section (FS) has the advantages of high accuracy, wide applicability, few complications and real-time diagnosis of pulmonary nodules. It is one of the main means to guide surgical strategies for pulmonary nodules. Therefore, we searched PubMed, Web of Science, CNKI, Wanfang and other databases for nearly 30 years of relevant literature and research data, held 3 conferences, and formulated this consensus by using the Delphi method. A total of 6 consensus contents were proposed: (1) Rapid intraoperative FS diagnosis of benign and malignant diseases; (2) Diagnosis of lung cancer types including adenocarcinoma, squamous cell carcinoma, others, etc; (3) Diagnosis of lung adenocarcinoma infiltration degree; (4) Histological subtype diagnosis of invasive adenocarcinoma; (5) The treatment strategy of lung adenocarcinoma with inconsistent diagnosis on degree of invasion between intraoperative FS and postoperative paraffin diagnosis; (6) Intraoperative FS diagnosis of tumor spread through air space, visceral pleural invasion and lymphovascular invasion. Finally, we gave 11 recommendations in the above 6 consensus contents to provide a reference for diagnosis of pulmonary nodules and guiding surgical decision-making for peripheral non-small cell lung cancer using FS, and to further improve the level of individualized and precise diagnosis and treatment of early-stage lung cancer.

Citation： Thoracic Surgery Branch of Shanghai Medical Association, Thoracic Surgeons Branch of Shanghai Medical Doctor Association, The Specialist Alliance of Clinical Skills Promotion and Enhancement for General Thoracic Surgery. Expert consensus of thoracic surgeons on guiding surgical decision-making based on intraoperative frozen sections for peripheral pulmonary nodules with diameter≤2 cm. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(6): 667-675. doi: 10.7507/1007-4848.202204098 Copy

1.	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.
2.	Huang KY, Ko PZ, Yao CW, et al. Inaccuracy of lung adenocarcinoma subtyping using preoperative biopsy specimens. J Thorac Cardiovasc Surg, 2017, 154(1): 332-339.
3.	Taffurelli M, Montroni I, Santini D, et al. Effectiveness of sentinel lymph node intraoperative examination in 753 women with breast cancer: Are we overtreating patients? Ann Surg, 2012, 255(5): 976-980.
4.	Hasegawa Y, Tsukahara K, Yoshimoto S, et al. Neck dissections based on sentinel lymph node navigation versus elective neck dissections in early oral cancers: A randomized, multicenter, and noninferiority trial. J Clin Oncol, 2021, 39(18): 2025-2036.
5.	Iyer NG, Kumar A, Nixon IJ, et al. Incidence and significance of Delphian node metastasis in papillary thyroid cancer. Ann Surg, 2011, 253(5): 988-991.
6.	Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
7.	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.
8.	Yotsukura M, Asamura H, Motoi N, et al. Long-term prognosis of patients with resected adenocarcinoma in situ and minimally invasive adenocarcinoma of the lung. J Thorac Oncol, 2021, 16(8): 1312-1320.
9.	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.
10.	Kadota K, Villena-Vargas J, Yoshizawa A, et al. Prognostic significance of adenocarcinoma in situ, minimally invasive adenocarcinoma, and nonmucinous lepidic predominant invasive adenocarcinoma of the lung in patients with stageⅠ disease. Am J Surg Pathol, 2014, 38(4): 448-460.
11.	Tsutani Y, Miyata Y, Nakayama H, et al. Appropriate sublobar resection choice for ground glass opacity-dominant clinical stageⅠA lung adenocarcinoma: Wedge resection or segmentectomy. Chest, 2014, 145(1): 66-71.
12.	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.
13.	Tsutani Y, Nakayama H, Ito H, et al. Long-term outcomes after sublobar resection versus lobectomy in patients with clinical stageⅠa lung adenocarcinoma meeting the node-negative criteria defined by high-resolution computed tomography and [18F]-fluoro-2-deoxy-d-glucose positron emission tomography. Clin Lung Cancer, 2021, 22(3): e431-e437.
14.	Veluswamy RR, Ezer N, Mhango G, et al. Limited resection versus lobectomy for older patients with early-stage lung cancer: Impact of histology. J Clin Oncol, 2015, 33(30): 3447-3453.
15.	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.
16.	Nitadori J, Bograd AJ, Kadota K, et al. Impact of micropapillary histologic subtype in selecting limited resection vs. lobectomy for lung adenocarcinoma of 2 cm or smaller. J Natl Cancer Inst, 2013, 105(16): 1212-1220.
17.	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 stageⅠ lung adenocarcinomas. J Thorac Oncol, 2015, 10(5): 806-814.
18.	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.
19.	Huang W, Deng HY, Lin MY, et al. Treatment modality for stageⅠb peripheral non-small cell lung cancer with visceral pleural invasion and ≤3 cm in size. Front Oncol, 2022, 12: 830470.
20.	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.
21.	WHO Classification of Tumours, 5th Edition, Volume 5: Thoracic Tumour. 2021. 60-149.
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23.	李媛, 谢惠康, 武春燕. WHO胸部肿瘤分类(第5版)中肺肿瘤部分解读. 中国癌症杂志, 2021, 31(7): 574-580.
24.	Xu Y, Bai L, Zhang L, et al. Analysis of the choice of operation mode and prognosis factors of patients with tumors of the lung metastasis. Zhongguo Fei Ai Za Zhi, 2015, 18(4): 206-211.
25.	徐丽伟, 刘金石, 李德川. 可手术切除直肠癌肺转移患者临床病理特征及异时性肺转移发生率分析. 结直肠肛门外科, 2020, 26(2): 158-161.
26.	徐璐茜, 祁雪玲, 王娟, 等. 宫颈癌肺转移患者预后分析及列线图的构建. 医学理论与实践, 2021, 34(21): 3699-3703.
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28.	谢惠康, 陈岗. 肺腺癌的最早期: 原位腺癌的病理诊断和临床意义. 中国肺癌杂志, 2021, 24(11): 753-755.
29.	Hu B, Li Q. Strategies of individual surgical treatment for early stage non-small cell lung cancer and the guidance of intraoperative frozen pathology. Zhongguo Fei Ai Za Zhi, 2016, 19(6): 364-367.
30.	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.
31.	Song J, Xu Y, Yang Z, et al. Coexistence of atypical adenomatous hyperplasia, minimally invasive adenocarcinoma and invasive adenocarcinoma: Gene mutation analysis. Thorac Cancer, 2021, 12(5): 693-698.
32.	He P, Yao G, Guan Y, et al. Diagnosis of lung adenocarcinoma in situ and minimally invasive adenocarcinoma from intraoperative frozen sections: An analysis of 136 cases. J Clin Pathol, 2016, 69(12): 1076-1080.
33.	Su H, Gu C, She Y, et al. Predictors of upstage and treatment strategies for stageⅠA lung cancers after sublobar resection for adenocarcinoma in situ and minimally invasive adenocarcinoma. Transl Lung Cancer Res, 2021, 10(1): 32-44.
34.	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.
35.	中华医学会病理学分会胸部疾病学组. 早期(非黏液型附壁生长方式)肺腺癌冷冻切片病理诊断专家共识. 中华病理学杂志, 2019, 48(1): 3-10.
36.	Kameda K, Eguchi T, Lu S, et al. Implications of the eighth edition of the TNM proposal: Invasive versus total tumor size for the T descriptor in pathologic stageⅠ-ⅡA lung adenocarcinoma. J Thorac Oncol, 2018, 13(12): 1919-1929.
37.	Travis WD, Asamura H, Bankier AA, et al. The IASLC lung cancer staging project: Proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol, 2016, 11(8): 1204-1223.
38.	Warth A, Muley T, Meister M, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol, 2012, 30(13): 1438-1446.
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41.	Yoshizawa A, Sumiyoshi S, Sonobe M, et al. Validation of the IASLC/ATS/ERS lung adenocarcinoma classification for prognosis and association with EGFR and KRAS gene mutations: Analysis of 440 Japanese patients. J Thorac Oncol, 2013, 8(1): 52-61.
42.	Cox ML, Yang CJ, Speicher PJ, et al. The role of extent of surgical resection and lymph node assessment for clinical stageⅠ pulmonary lepidic adenocarcinoma: An analysis of 1991 patients. J Thorac Oncol, 2017, 12(4): 689-696.
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47.	Moreira AL, Joubert P, Downey RJ, et al. Cribriform and fused glands are patterns of high-grade pulmonary adenocarcinoma. Hum Pathol, 2014, 45(2): 213-220.
48.	Moreira AL, Ocampo PSS, Xia Y, et al. A grading system for invasive pulmonary adenocarcinoma: A proposal from the International Association for the Study of Lung Cancer Pathology Committee. J Thorac Oncol, 2020, 15(10): 1599-1610.
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1. 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.
2. Huang KY, Ko PZ, Yao CW, et al. Inaccuracy of lung adenocarcinoma subtyping using preoperative biopsy specimens. J Thorac Cardiovasc Surg, 2017, 154(1): 332-339.
3. Taffurelli M, Montroni I, Santini D, et al. Effectiveness of sentinel lymph node intraoperative examination in 753 women with breast cancer: Are we overtreating patients? Ann Surg, 2012, 255(5): 976-980.
4. Hasegawa Y, Tsukahara K, Yoshimoto S, et al. Neck dissections based on sentinel lymph node navigation versus elective neck dissections in early oral cancers: A randomized, multicenter, and noninferiority trial. J Clin Oncol, 2021, 39(18): 2025-2036.
5. Iyer NG, Kumar A, Nixon IJ, et al. Incidence and significance of Delphian node metastasis in papillary thyroid cancer. Ann Surg, 2011, 253(5): 988-991.
6. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
7. 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.
8. Yotsukura M, Asamura H, Motoi N, et al. Long-term prognosis of patients with resected adenocarcinoma in situ and minimally invasive adenocarcinoma of the lung. J Thorac Oncol, 2021, 16(8): 1312-1320.
9. 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.
10. Kadota K, Villena-Vargas J, Yoshizawa A, et al. Prognostic significance of adenocarcinoma in situ, minimally invasive adenocarcinoma, and nonmucinous lepidic predominant invasive adenocarcinoma of the lung in patients with stageⅠ disease. Am J Surg Pathol, 2014, 38(4): 448-460.
11. Tsutani Y, Miyata Y, Nakayama H, et al. Appropriate sublobar resection choice for ground glass opacity-dominant clinical stageⅠA lung adenocarcinoma: Wedge resection or segmentectomy. Chest, 2014, 145(1): 66-71.
12. 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.
13. Tsutani Y, Nakayama H, Ito H, et al. Long-term outcomes after sublobar resection versus lobectomy in patients with clinical stageⅠa lung adenocarcinoma meeting the node-negative criteria defined by high-resolution computed tomography and [18F]-fluoro-2-deoxy-d-glucose positron emission tomography. Clin Lung Cancer, 2021, 22(3): e431-e437.
14. Veluswamy RR, Ezer N, Mhango G, et al. Limited resection versus lobectomy for older patients with early-stage lung cancer: Impact of histology. J Clin Oncol, 2015, 33(30): 3447-3453.
15. 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.
16. Nitadori J, Bograd AJ, Kadota K, et al. Impact of micropapillary histologic subtype in selecting limited resection vs. lobectomy for lung adenocarcinoma of 2 cm or smaller. J Natl Cancer Inst, 2013, 105(16): 1212-1220.
17. 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 stageⅠ lung adenocarcinomas. J Thorac Oncol, 2015, 10(5): 806-814.
18. 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.
19. Huang W, Deng HY, Lin MY, et al. Treatment modality for stageⅠb peripheral non-small cell lung cancer with visceral pleural invasion and ≤3 cm in size. Front Oncol, 2022, 12: 830470.
20. 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.
21. WHO Classification of Tumours, 5th Edition, Volume 5: Thoracic Tumour. 2021. 60-149.
22. Board WCOTE. WHO Classification of Tumours of Thoracic Tumours, 5th Edition, Volume 5. IARC Publications 2021.
23. 李媛, 谢惠康, 武春燕. WHO胸部肿瘤分类(第5版)中肺肿瘤部分解读. 中国癌症杂志, 2021, 31(7): 574-580.
24. Xu Y, Bai L, Zhang L, et al. Analysis of the choice of operation mode and prognosis factors of patients with tumors of the lung metastasis. Zhongguo Fei Ai Za Zhi, 2015, 18(4): 206-211.
25. 徐丽伟, 刘金石, 李德川. 可手术切除直肠癌肺转移患者临床病理特征及异时性肺转移发生率分析. 结直肠肛门外科, 2020, 26(2): 158-161.
26. 徐璐茜, 祁雪玲, 王娟, 等. 宫颈癌肺转移患者预后分析及列线图的构建. 医学理论与实践, 2021, 34(21): 3699-3703.
27. 中华医学会, 中华医学会肿瘤学分会, 中华医学会杂志社. 中华医学会肺癌临床诊疗指南(2019版). 中华肿瘤杂志, 2020, 42(4): 257-287.
28. 谢惠康, 陈岗. 肺腺癌的最早期: 原位腺癌的病理诊断和临床意义. 中国肺癌杂志, 2021, 24(11): 753-755.
29. Hu B, Li Q. Strategies of individual surgical treatment for early stage non-small cell lung cancer and the guidance of intraoperative frozen pathology. Zhongguo Fei Ai Za Zhi, 2016, 19(6): 364-367.
30. 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.
31. Song J, Xu Y, Yang Z, et al. Coexistence of atypical adenomatous hyperplasia, minimally invasive adenocarcinoma and invasive adenocarcinoma: Gene mutation analysis. Thorac Cancer, 2021, 12(5): 693-698.
32. He P, Yao G, Guan Y, et al. Diagnosis of lung adenocarcinoma in situ and minimally invasive adenocarcinoma from intraoperative frozen sections: An analysis of 136 cases. J Clin Pathol, 2016, 69(12): 1076-1080.
33. Su H, Gu C, She Y, et al. Predictors of upstage and treatment strategies for stageⅠA lung cancers after sublobar resection for adenocarcinoma in situ and minimally invasive adenocarcinoma. Transl Lung Cancer Res, 2021, 10(1): 32-44.
34. 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.
35. 中华医学会病理学分会胸部疾病学组. 早期(非黏液型附壁生长方式)肺腺癌冷冻切片病理诊断专家共识. 中华病理学杂志, 2019, 48(1): 3-10.
36. Kameda K, Eguchi T, Lu S, et al. Implications of the eighth edition of the TNM proposal: Invasive versus total tumor size for the T descriptor in pathologic stageⅠ-ⅡA lung adenocarcinoma. J Thorac Oncol, 2018, 13(12): 1919-1929.
37. Travis WD, Asamura H, Bankier AA, et al. The IASLC lung cancer staging project: Proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol, 2016, 11(8): 1204-1223.
38. Warth A, Muley T, Meister M, et al. The novel histologic International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society classification system of lung adenocarcinoma is a stage-independent predictor of survival. J Clin Oncol, 2012, 30(13): 1438-1446.
39. Hung JJ, Jeng WJ, Chou TY, et al. Prognostic value of the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society lung adenocarcinoma classification on death and recurrence in completely resected stageⅠlung adenocarcinoma. Ann Surg, 2013, 258(6): 1079-1086.
40. Zhang J, Wu J, Tan Q, et al. Why do pathological stageⅠA lung adenocarcinomas vary from prognosis?: A clinicopathologic study of 176 patients with pathological stageⅠA lung adenocarcinoma based on the IASLC/ATS/ERS classification. J Thorac Oncol, 2013, 8(9): 1196-1202.
41. Yoshizawa A, Sumiyoshi S, Sonobe M, et al. Validation of the IASLC/ATS/ERS lung adenocarcinoma classification for prognosis and association with EGFR and KRAS gene mutations: Analysis of 440 Japanese patients. J Thorac Oncol, 2013, 8(1): 52-61.
42. Cox ML, Yang CJ, Speicher PJ, et al. The role of extent of surgical resection and lymph node assessment for clinical stageⅠ pulmonary lepidic adenocarcinoma: An analysis of 1991 patients. J Thorac Oncol, 2017, 12(4): 689-696.
43. Moon Y, Lee KY, Park JK. Margin width of resected lepidic lung cancer does not affect recurrence after sublobar resection. World J Surg, 2018, 42(5): 1449-1457.
44. Su H, Xie H, Dai C, et al. Procedure-specific prognostic impact of micropapillary subtype may guide resection strategy in small-sized lung adenocarcinomas: A multicenter study. Ther Adv Med Oncol, 2020, 12: 1758835920937893.
45. Zhao ZR, To KF, Mok TS, et al. Is there significance in identification of non-predominant micropapillary or solid components in early-stage lung adenocarcinoma? Interact Cardiovasc Thorac Surg, 2017, 24(1): 121-125.
46. Warth A, Muley T, Kossakowski C, et al. Prognostic impact and clinicopathological correlations of the cribriform pattern in pulmonary adenocarcinoma. J Thorac Oncol, 2015, 10(4): 638-644.
47. Moreira AL, Joubert P, Downey RJ, et al. Cribriform and fused glands are patterns of high-grade pulmonary adenocarcinoma. Hum Pathol, 2014, 45(2): 213-220.
48. Moreira AL, Ocampo PSS, Xia Y, et al. A grading system for invasive pulmonary adenocarcinoma: A proposal from the International Association for the Study of Lung Cancer Pathology Committee. J Thorac Oncol, 2020, 15(10): 1599-1610.
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