Advancements in the Diagnosis and Treatment of Multiple Lung Cancer: A Review of Research Progress_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WANG Yilun ^1,2,3 , ZHANG Yaojing ^1,2,3 ,  SHI Hongcan ^1,2,3

1. Clinical Medical College, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;
2. Institute of Translational Medicine, Medical College, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;
3. Jiangsu Key Laboratory of Integrated Traditional Chinese and Western Medicine for Prevention and Treatment of Senile Diseases, Yangzhou University, Yangzhou, 225009, Jiangsu, P. R. China;

Corresponding author：

SHI Hongcan, Email: shihongcan@yzu.edu.cn

Keywords：

Multiple primary lung cancer; diagnosis; thoracic surgery; lobectomy; ablation; review

DOI：

10.7507/1007-4848.202311074

Video：

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Abstract Full text Figures/Tables Video References Cited by

With the popularization of CT technology, more and more multiple primary lung cancer, that is, the simultaneous presence of more than one primary cancer in the lungs, has been detected. Imaging can make a rough judgment, histopathology is still the diagnostic gold standard, and molecular genetics examination can better distinguish it from intrapulmonary metastatic cancer when necessary. At present, there is no unified treatment standard for multiple primary lung cancer. Surgery is the most important and effective means, and the surgical method needs to be personalized according to the size and distribution of the patient's lesions, one-sided lobectomy and the other side sublobar resection is considered safe and feasible. At the same time, local nonsurgical treatment is also an option or a supplement to surgical treatment. This article reviews the diagnosis and treatment of multiple primary lung cancer in recent years.

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2.	Sands J, Tammemägi MC, Couraud S, et al. Lung screening benefits and challenges: A review of the data and outline for implementation. J Thorac Oncol, 2021, 16(1): 37-53.
3.	Liao Z, Rivin Del Campo E, Salem A, et al. Optimizing lung cancer radiation treatment worldwide in COVID-19 outbreak. Lung Cancer, 2020, 146: 230-235.
4.	Martini N, Melamed MR. Multiple primary lung cancers. J Thorac Cardiovasc Surg, 1975, 70(4): 606-612.
5.	Detterbeck FC, Jones DR, Kernstine KH, et al. Lung cancer. Special treatment issues. Chest, 2003, 123(1 Suppl): 244S-258S.
6.	Shen KR, Meyers BF, Larner JM, et al. Special treatment issues in lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest, 2007, 132(3 Suppl): 290S-305S.
7.	Kozower BD, Larner JM, Detterbeck FC, et al. Special treatment issues in non-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): e369S-e399S.
8.	Suh YJ, Lee HJ, Sung P, et al. A novel algorithm to differentiate between multiple primary lung cancers and intrapulmonary metastasis in multiple lung cancers with multiple pulmonary sites of involvement. J Thorac Oncol, 2020, 15(2): 203-215.
9.	Liu Y, Tang Y, Xue Z, et al. SUVmax Ratio on PET/CT may differentiate between lung metastases and synchronous multiple primary lung cancer. Acad Radiol, 2020, 27(5): 618-623.
10.	Rami-Porta R, Asamura H, Travis WD, et al. Lung cancer: Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(2): 138-155.
11.	Nicholson AG, Torkko K, Viola P, et al. Interobserver variation among pathologists and refinement of criteria in distinguishing separate primary tumors from intrapulmonary metastases in lung. J Thorac Oncol, 2018, 13(2): 205-217.
12.	Kim M, Hwang J, Kim KA, et al. Genomic characteristics of invasive mucinous adenocarcinoma of the lung with multiple pulmonary sites of involvement. Mod Pathol, 2022, 35(2): 202-209.
13.	Girard N, Deshpande C, Lau C, et al. Comprehensive histologic assessment helps to differentiate multiple lung primary nonsmall cell carcinomas from metastases. Am J Surg Pathol, 2009, 33(12): 1752-1764.
14.	Sun W, Feng L, Yang X, et al. Clonality assessment of multifocal lung adenocarcinoma by pathology evaluation and molecular analysis. Hum Pathol, 2018, 81: 261-271.
15.	Chiang CL, Tsai PC, Yeh YC, et al. Recent advances in the diagnosis and management of multiple primary lung cancer. Cancers (Basel), 2022, 14(1): 242.
16.	Zhu D, Cao D, Shen M, et al. Morphological and genetic heterogeneity of synchronous multifocal lung adenocarcinoma in a Chinese cohort. BMC Cancer, 2021, 21(1): 176.
17.	Yang SR, Chang JC, Leduc C, et al. Invasive mucinous adenocarcinomas with spatially separate lung lesions: Analysis of clonal relationship by comparative molecular profiling. J Thorac Oncol, 2021, 16(7): 1188-1199.
18.	Hu C, Zhao L, Liu W, et al. Genomic profiles and their associations with TMB, PD-L1 expression, and immune cell infiltration landscapes in synchronous multiple primary lung cancers. J Immunother Cancer, 2021, 9(12): e003773.
19.	Yu F, Peng M, Bai J, et al. Comprehensive characterization of genomic and radiologic features reveals distinct driver patterns of RTK/RAS pathway in ground-glass opacity pulmonary nodules. Int J Cancer, 2022, 151(11): 2020-2030.
20.	Mansuet-Lupo A, Barritault M, Alifano M, et al. Proposal for a combined histomolecular algorithm to distinguish multiple primary adenocarcinomas from intrapulmonary metastasis in patients with multiple lung tumors. J Thorac Oncol, 2019, 14(5): 844-856.
21.	Takahashi Y, Shien K, Tomida S, et al. Comparative mutational evaluation of multiple lung cancers by multiplex oncogene mutation analysis. Cancer Sci, 2018, 109(11): 3634-3642.
22.	Guo W, Zhou B, Bie F, et al. Single-cell RNA sequencing analysis reveals transcriptional heterogeneity of multiple primary lung cancer. Clin Transl Med, 2023, 13(10): e1453.
23.	Goodwin D, Rathi V, Conron M, et al. Genomic and clinical significance of multiple primary lung cancers as determined by next-generation sequencing. J Thorac Oncol, 2021, 16(7): 1166-1175.
24.	Zheng R, Shen Q, Mardekian S, et al. Molecular profiling of key driver genes improves staging accuracy in multifocal non-small cell lung cancer. J Thorac Cardiovasc Surg, 2020, 160(2): e71-e79.
25.	Detterbeck FC, Nicholson AG, Franklin WA, et al. The IASLC Lung Cancer Staging Project: Summary of proposals for revisions of the classification of lung cancers with multiple pulmonary sites of involvement in the forthcoming eighth edition of the TNM classification. J Thorac Oncol, 2016, 11(5): 639-650.
26.	上海市医学会胸外科专科分会, 上海市医师协会胸外科医师分会, 普胸外科临床能力促进与提升专科联盟. 多原发早期肺癌诊疗专家共识. 中国胸心血管外科临床杂志, 2022, 29(12): 1545-1553.
27.	Lee DS, LaChapelle C, Taioli E, et al. Second primary lung cancers demonstrate similar survival with wedge resection and lobectomy. Ann Thorac Surg, 2019, 108(6): 1724-1728.
28.	Postmus PE, Kerr KM, Oudkerk M, et al. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2017, 28(suppl_4): iv1-iv21.
29.	Chen TF, Xie CY, Rao BY, et al. Surgical treatment to multiple primary lung cancer patients: A systematic review and meta-analysis. BMC Surg, 2019, 19(1): 185.
30.	Yang H, Sun Y, Yao F, et al. Surgical therapy for bilateral multiple primary lung cancer. Ann Thorac Surg, 2016, 101(3): 1145-1152.
31.	Hattori A, Takamochi K, Oh S, et al. Prognostic classification of multiple primary lung cancers based on a ground-glass opacity component. Ann Thorac Surg, 2020, 109(2): 420-427.
32.	Zhao K, Xia C, Qiu M, et al. Lobar or sublobar resection for early-stage second primary lung cancer≤3 cm in size: A SEER population-based study. J Cancer Res Clin Oncol, 2023, 149(18): 16679-16690.
33.	Shimada Y, Saji H, Otani K, et al. Survival of a surgical series of lung cancer patients with synchronous multiple ground-glass opacities, and the management of their residual lesions. Lung Cancer, 2015, 88(2): 174-180.
34.	Shimada Y, Maehara S, Kudo Y, et al. Profiles of lung adenocarcinoma with multiple ground-glass opacities and the fate of residual lesions. Ann Thorac Surg, 2020, 109(6): 1722-1730.
35.	Nie Y, Wang X, Yang F, et al. Surgical prognosis of synchronous multiple primary lung cancer: Systematic review and meta-analysis. Clin Lung Cancer, 2021, 22(4): 341-350.
36.	Ball D, Mai GT, Vinod S, et al. Stereotactic ablative radiotherapy versus standard radiotherapy in stageⅠnon-small-cell lung cancer (TROG 09.02 CHISEL): A phase 3, open-label, randomised controlled trial. Lancet Oncol, 2019, 20(4): 494-503.
37.	Nyman J, Hallqvist A, Lund JÅ, et al. SPACE: A randomized study of SBRT vs. conventional fractionated radiotherapy in medically inoperable stage I NSCLC. Radiother Oncol, 2016, 121(1): 1-8.
38.	Nikitas J, DeWees T, Rehman S, et al. Stereotactic body radiotherapy for early-stage multiple primary lung cancers. Clin Lung Cancer, 2019, 20(2): 107-116.
39.	Videtic GMM, Donington J, Giuliani M, et al. Stereotactic body radiation therapy for early-stage non-small cell lung cancer: Executive summary of an ASTRO evidence-based guideline. Pract Radiat Oncol, 2017, 7(5): 295-301.
40.	Ni Y, Xu H, Ye X. Image-guided percutaneous microwave ablation of early-stage non-small cell lung cancer. Asia Pac J Clin Oncol, 2020, 16(6): 320-325.
41.	Páez-Carpio A, Gómez FM, Isus Olivé G, et al. Image-guided percutaneous ablation for the treatment of lung malignancies: Current state of the art. Insights Imaging, 2021, 12(1): 57.
42.	Huang G, Yang X, Li W, et al. A feasibility and safety study of computed tomography-guided percutaneous microwave ablation: A novel therapy for multiple synchronous ground-glass opacities of the lung. Int J Hyperthermia, 2020, 37(1): 414-422.
43.	Liu B, Ye X. Computed tomography-guided percutaneous microwave ablation: A novel perspective to treat multiple pulmonary ground-glass opacities. Thorac Cancer, 2020, 11(9): 2385-2388.
44.	叶欣, 王俊, 危志刚, 等. 热消融治疗肺部亚实性结节专家共识(2021年版). 中国肺癌杂志, 2021, 24(5): 305-322.
45.	Bao F, Yu F, Wang R, et al. Electromagnetic bronchoscopy guided microwave ablation for early stage lung cancer presenting as ground glass nodule. Transl Lung Cancer Res, 2021, 10(9): 3759-3770.
46.	Nomori H, Yamazaki I, Shiraishi A, et al. Cryoablation for T1N0M0 non-small cell lung cancer using liquid nitrogen. Eur J Radiol, 2020, 133: 109334.
47.	Mal R, Domini J, Wadhwa V, et al. Thermal ablation for primary and metastatic lung tumors: Single-center analysis of peri-procedural and intermediate-term clinical outcomes. Clin Imaging, 2023, 98: 11-15.
48.	Gao S, Stein S, Petre EN, et al. Micropapillary and/or solid histologic subtype based on pre-treatment biopsy predicts local recurrence after thermal ablation of lung adenocarcinoma. Cardiovasc Intervent Radiol, 2018, 41(2): 253-259.
49.	Herbst RS, Wu YL, John T, et al. Adjuvant Osimertinib for resected EGFR-mutated stageⅠB-ⅢA non-small-cell lung cancer: Updated results from the phaseⅢrandomized ADAURA trial. J Clin Oncol, 2023, 41(10): 1830-1840.
50.	Zhou D, Yao T, Huang X, et al. Real-world comprehensive diagnosis and "Surgery+X" treatment strategy of early-stage synchronous multiple primary lung cancer. Cancer Med, 2023, 12(12): 12996-13006.
51.	Teng F, Xu J, Wang J, et al. Correlation between gene mutation status and clinicopathologic features in early multiple primary lung cancer. Front Oncol, 202, 13: 1110259.
52.	Wang M, Herbst RS, Boshoff C. Toward personalized treatment approaches for non-small-cell lung cancer. Nat Med, 2021, 27(8): 1345-1356.
53.	Haratake N, Toyokawa G, Takada K, et al. Programmed death-ligand 1 expression and EGFR mutations in multifocal lung cancer. Ann Thorac Surg, 2018, 105(2): 448-454.
54.	Liu M, He WX, Song N, et al. Discrepancy of epidermal growth factor receptor mutation in lung adenocarcinoma presenting as multiple ground-glass opacities. Eur J Cardiothorac Surg, 2016, 50(5): 909-913.
55.	Xu L, Shi M, Wang S, et al. Immunotherapy for bilateral multiple ground glass opacities: An exploratory study for synchronous multiple primary lung cancer. Front Immunol, 2022, 13: 1009621.
56.	Zhang C, Yin K, Liu SY, et al. Multiomics analysis reveals a distinct response mechanism in multiple primary lung adenocarcinoma after neoadjuvant immunotherapy. J Immunother Cancer, 2021, 9(4): e002312.

1. Siegel RL, Miller KD, Wagle NS, et al. Cancer statistics, 2023. CA Cancer J Clin, 2023, 73(1): 17-48.
2. Sands J, Tammemägi MC, Couraud S, et al. Lung screening benefits and challenges: A review of the data and outline for implementation. J Thorac Oncol, 2021, 16(1): 37-53.
3. Liao Z, Rivin Del Campo E, Salem A, et al. Optimizing lung cancer radiation treatment worldwide in COVID-19 outbreak. Lung Cancer, 2020, 146: 230-235.
4. Martini N, Melamed MR. Multiple primary lung cancers. J Thorac Cardiovasc Surg, 1975, 70(4): 606-612.
5. Detterbeck FC, Jones DR, Kernstine KH, et al. Lung cancer. Special treatment issues. Chest, 2003, 123(1 Suppl): 244S-258S.
6. Shen KR, Meyers BF, Larner JM, et al. Special treatment issues in lung cancer: ACCP evidence-based clinical practice guidelines (2nd edition). Chest, 2007, 132(3 Suppl): 290S-305S.
7. Kozower BD, Larner JM, Detterbeck FC, et al. Special treatment issues in non-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): e369S-e399S.
8. Suh YJ, Lee HJ, Sung P, et al. A novel algorithm to differentiate between multiple primary lung cancers and intrapulmonary metastasis in multiple lung cancers with multiple pulmonary sites of involvement. J Thorac Oncol, 2020, 15(2): 203-215.
9. Liu Y, Tang Y, Xue Z, et al. SUVmax Ratio on PET/CT may differentiate between lung metastases and synchronous multiple primary lung cancer. Acad Radiol, 2020, 27(5): 618-623.
10. Rami-Porta R, Asamura H, Travis WD, et al. Lung cancer: Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA Cancer J Clin, 2017, 67(2): 138-155.
11. Nicholson AG, Torkko K, Viola P, et al. Interobserver variation among pathologists and refinement of criteria in distinguishing separate primary tumors from intrapulmonary metastases in lung. J Thorac Oncol, 2018, 13(2): 205-217.
12. Kim M, Hwang J, Kim KA, et al. Genomic characteristics of invasive mucinous adenocarcinoma of the lung with multiple pulmonary sites of involvement. Mod Pathol, 2022, 35(2): 202-209.
13. Girard N, Deshpande C, Lau C, et al. Comprehensive histologic assessment helps to differentiate multiple lung primary nonsmall cell carcinomas from metastases. Am J Surg Pathol, 2009, 33(12): 1752-1764.
14. Sun W, Feng L, Yang X, et al. Clonality assessment of multifocal lung adenocarcinoma by pathology evaluation and molecular analysis. Hum Pathol, 2018, 81: 261-271.
15. Chiang CL, Tsai PC, Yeh YC, et al. Recent advances in the diagnosis and management of multiple primary lung cancer. Cancers (Basel), 2022, 14(1): 242.
16. Zhu D, Cao D, Shen M, et al. Morphological and genetic heterogeneity of synchronous multifocal lung adenocarcinoma in a Chinese cohort. BMC Cancer, 2021, 21(1): 176.
17. Yang SR, Chang JC, Leduc C, et al. Invasive mucinous adenocarcinomas with spatially separate lung lesions: Analysis of clonal relationship by comparative molecular profiling. J Thorac Oncol, 2021, 16(7): 1188-1199.
18. Hu C, Zhao L, Liu W, et al. Genomic profiles and their associations with TMB, PD-L1 expression, and immune cell infiltration landscapes in synchronous multiple primary lung cancers. J Immunother Cancer, 2021, 9(12): e003773.
19. Yu F, Peng M, Bai J, et al. Comprehensive characterization of genomic and radiologic features reveals distinct driver patterns of RTK/RAS pathway in ground-glass opacity pulmonary nodules. Int J Cancer, 2022, 151(11): 2020-2030.
20. Mansuet-Lupo A, Barritault M, Alifano M, et al. Proposal for a combined histomolecular algorithm to distinguish multiple primary adenocarcinomas from intrapulmonary metastasis in patients with multiple lung tumors. J Thorac Oncol, 2019, 14(5): 844-856.
21. Takahashi Y, Shien K, Tomida S, et al. Comparative mutational evaluation of multiple lung cancers by multiplex oncogene mutation analysis. Cancer Sci, 2018, 109(11): 3634-3642.
22. Guo W, Zhou B, Bie F, et al. Single-cell RNA sequencing analysis reveals transcriptional heterogeneity of multiple primary lung cancer. Clin Transl Med, 2023, 13(10): e1453.
23. Goodwin D, Rathi V, Conron M, et al. Genomic and clinical significance of multiple primary lung cancers as determined by next-generation sequencing. J Thorac Oncol, 2021, 16(7): 1166-1175.
24. Zheng R, Shen Q, Mardekian S, et al. Molecular profiling of key driver genes improves staging accuracy in multifocal non-small cell lung cancer. J Thorac Cardiovasc Surg, 2020, 160(2): e71-e79.
25. Detterbeck FC, Nicholson AG, Franklin WA, et al. The IASLC Lung Cancer Staging Project: Summary of proposals for revisions of the classification of lung cancers with multiple pulmonary sites of involvement in the forthcoming eighth edition of the TNM classification. J Thorac Oncol, 2016, 11(5): 639-650.
26. 上海市医学会胸外科专科分会, 上海市医师协会胸外科医师分会, 普胸外科临床能力促进与提升专科联盟. 多原发早期肺癌诊疗专家共识. 中国胸心血管外科临床杂志, 2022, 29(12): 1545-1553.
27. Lee DS, LaChapelle C, Taioli E, et al. Second primary lung cancers demonstrate similar survival with wedge resection and lobectomy. Ann Thorac Surg, 2019, 108(6): 1724-1728.
28. Postmus PE, Kerr KM, Oudkerk M, et al. Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol, 2017, 28(suppl_4): iv1-iv21.
29. Chen TF, Xie CY, Rao BY, et al. Surgical treatment to multiple primary lung cancer patients: A systematic review and meta-analysis. BMC Surg, 2019, 19(1): 185.
30. Yang H, Sun Y, Yao F, et al. Surgical therapy for bilateral multiple primary lung cancer. Ann Thorac Surg, 2016, 101(3): 1145-1152.
31. Hattori A, Takamochi K, Oh S, et al. Prognostic classification of multiple primary lung cancers based on a ground-glass opacity component. Ann Thorac Surg, 2020, 109(2): 420-427.
32. Zhao K, Xia C, Qiu M, et al. Lobar or sublobar resection for early-stage second primary lung cancer≤3 cm in size: A SEER population-based study. J Cancer Res Clin Oncol, 2023, 149(18): 16679-16690.
33. Shimada Y, Saji H, Otani K, et al. Survival of a surgical series of lung cancer patients with synchronous multiple ground-glass opacities, and the management of their residual lesions. Lung Cancer, 2015, 88(2): 174-180.
34. Shimada Y, Maehara S, Kudo Y, et al. Profiles of lung adenocarcinoma with multiple ground-glass opacities and the fate of residual lesions. Ann Thorac Surg, 2020, 109(6): 1722-1730.
35. Nie Y, Wang X, Yang F, et al. Surgical prognosis of synchronous multiple primary lung cancer: Systematic review and meta-analysis. Clin Lung Cancer, 2021, 22(4): 341-350.
36. Ball D, Mai GT, Vinod S, et al. Stereotactic ablative radiotherapy versus standard radiotherapy in stageⅠnon-small-cell lung cancer (TROG 09.02 CHISEL): A phase 3, open-label, randomised controlled trial. Lancet Oncol, 2019, 20(4): 494-503.
37. Nyman J, Hallqvist A, Lund JÅ, et al. SPACE: A randomized study of SBRT vs. conventional fractionated radiotherapy in medically inoperable stage I NSCLC. Radiother Oncol, 2016, 121(1): 1-8.
38. Nikitas J, DeWees T, Rehman S, et al. Stereotactic body radiotherapy for early-stage multiple primary lung cancers. Clin Lung Cancer, 2019, 20(2): 107-116.
39. Videtic GMM, Donington J, Giuliani M, et al. Stereotactic body radiation therapy for early-stage non-small cell lung cancer: Executive summary of an ASTRO evidence-based guideline. Pract Radiat Oncol, 2017, 7(5): 295-301.
40. Ni Y, Xu H, Ye X. Image-guided percutaneous microwave ablation of early-stage non-small cell lung cancer. Asia Pac J Clin Oncol, 2020, 16(6): 320-325.
41. Páez-Carpio A, Gómez FM, Isus Olivé G, et al. Image-guided percutaneous ablation for the treatment of lung malignancies: Current state of the art. Insights Imaging, 2021, 12(1): 57.
42. Huang G, Yang X, Li W, et al. A feasibility and safety study of computed tomography-guided percutaneous microwave ablation: A novel therapy for multiple synchronous ground-glass opacities of the lung. Int J Hyperthermia, 2020, 37(1): 414-422.
43. Liu B, Ye X. Computed tomography-guided percutaneous microwave ablation: A novel perspective to treat multiple pulmonary ground-glass opacities. Thorac Cancer, 2020, 11(9): 2385-2388.
44. 叶欣, 王俊, 危志刚, 等. 热消融治疗肺部亚实性结节专家共识(2021年版). 中国肺癌杂志, 2021, 24(5): 305-322.
45. Bao F, Yu F, Wang R, et al. Electromagnetic bronchoscopy guided microwave ablation for early stage lung cancer presenting as ground glass nodule. Transl Lung Cancer Res, 2021, 10(9): 3759-3770.
46. Nomori H, Yamazaki I, Shiraishi A, et al. Cryoablation for T1N0M0 non-small cell lung cancer using liquid nitrogen. Eur J Radiol, 2020, 133: 109334.
47. Mal R, Domini J, Wadhwa V, et al. Thermal ablation for primary and metastatic lung tumors: Single-center analysis of peri-procedural and intermediate-term clinical outcomes. Clin Imaging, 2023, 98: 11-15.
48. Gao S, Stein S, Petre EN, et al. Micropapillary and/or solid histologic subtype based on pre-treatment biopsy predicts local recurrence after thermal ablation of lung adenocarcinoma. Cardiovasc Intervent Radiol, 2018, 41(2): 253-259.
49. Herbst RS, Wu YL, John T, et al. Adjuvant Osimertinib for resected EGFR-mutated stageⅠB-ⅢA non-small-cell lung cancer: Updated results from the phaseⅢrandomized ADAURA trial. J Clin Oncol, 2023, 41(10): 1830-1840.
50. Zhou D, Yao T, Huang X, et al. Real-world comprehensive diagnosis and "Surgery+X" treatment strategy of early-stage synchronous multiple primary lung cancer. Cancer Med, 2023, 12(12): 12996-13006.
51. Teng F, Xu J, Wang J, et al. Correlation between gene mutation status and clinicopathologic features in early multiple primary lung cancer. Front Oncol, 202, 13: 1110259.
52. Wang M, Herbst RS, Boshoff C. Toward personalized treatment approaches for non-small-cell lung cancer. Nat Med, 2021, 27(8): 1345-1356.
53. Haratake N, Toyokawa G, Takada K, et al. Programmed death-ligand 1 expression and EGFR mutations in multifocal lung cancer. Ann Thorac Surg, 2018, 105(2): 448-454.
54. Liu M, He WX, Song N, et al. Discrepancy of epidermal growth factor receptor mutation in lung adenocarcinoma presenting as multiple ground-glass opacities. Eur J Cardiothorac Surg, 2016, 50(5): 909-913.
55. Xu L, Shi M, Wang S, et al. Immunotherapy for bilateral multiple ground glass opacities: An exploratory study for synchronous multiple primary lung cancer. Front Immunol, 2022, 13: 1009621.
56. Zhang C, Yin K, Liu SY, et al. Multiomics analysis reveals a distinct response mechanism in multiple primary lung adenocarcinoma after neoadjuvant immunotherapy. J Immunother Cancer, 2021, 9(4): e002312.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Latest ArticlesAdvancements in the Diagnosis and Treatment of Multiple Lung Cancer: A Review of Research Progress

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