Risk factors associated with lymph node metastasis in lung adenocarcinoma with a diameter≤3 cm_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

XIN Shaowei ^1,2,3 , XIN Xiangbing ¹ , ZHAO Yabo ¹ , WEN Miaomiao ¹ , JIANG Suxin ² ,  XIONG Yanlu ^1,4

1. Department of Thoracic Surgery, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, P. R. China;
2. Department of Thoracic Surgery, Air Force Medical Center, Air Force Medical University, Beijing, 100142, P. R. China;
3. Department of Thoracic Surgery, 962 Hospital of Joint Logistics Support Force, Harbin, 150000, P. R. China;
4. Innovation Center for Advanced Medicine, Tangdu Hospital, Air Force Medical University, Xi'an, 710038, P. R. China;

Corresponding?author：

XIONG Yanlu, Email: xiong21@fmmu.edu.cn

Keywords：

Lung adenocarcinoma; early-stage lung cancer; lymph node metastasis; micropapillary component; solid component; vascular invasion; pleural invasion; risk factor analysis

DOI：

10.7507/1007-4848.202402048

Video：

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Objective To explore the correlation between lymph node metastasis and clinicopathological features of lung adenocarcinoma with diameter≤3 cm. Methods The clinicopathologic data of the patients with lung adenocarcinoma≤3 cm in diameter were retrospectively analyzed. The relationship between lymph node metastasis and age, gender, smoking history, pathological subtype, tumor diameter, pleural invasion, vascular invasion and other factors was analyzed. The risk factors of lymph node metastasis were analyzed by univariate and multivariate logistic regression. Results Finally 1 718 patients were collected, including 697 males and 1 021 females with an average age of (58.89±9.85) years. The total lymph node metastasis rate was 12.9%, among whom 452 patients of adenocarcinoma in situ and minimally invasive adenocarcinoma did not have lymph node metastasis, and the lymph node metastasis rate of invasive lung adenocarcinoma was 17.5%. Multivariate analysis showed that tumor diameter, micropapillary subtype, solid subtype, micropapillary component, solid component, vascular invasion and pleural invasion were independent risk factors for lymph node metastasis of invasive lung adenocarcinoma with diameter≤3 cm (P<0.05). While age, lepidic subtype and lepidic component were independent protective factors for lymph node metastasis (P<0.05). Conclusion Clinicopathological features can help predict lymph node metastasis of lung adenocarcinoma with diameter≤3 cm.

Citation： XIN Shaowei, XIN Xiangbing, ZHAO Yabo, WEN Miaomiao, JIANG Suxin, XIONG Yanlu. Risk factors associated with lymph node metastasis in lung adenocarcinoma with a diameter≤3 cm. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2026, 33(2): 255-260. doi: 10.7507/1007-4848.202402048 Copy

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.	Succony L, Rassl DM, Barker AP, et al. Adenocarcinoma spectrum lesions of the lung: detection, pathology and treatment strategies. Cancer Treat Rev, 2021, 99: 102237.
3.	Asamura H, Nishimura KK, Giroux DJ, et al. IASLC lung cancer staging project: the new database to inform revisions in the ninth edition of the TNM classification of lung cancer. J Thorac Oncol, 2023, 18(5): 564-575.
4.	Ito H, Date H, Shintani Y, et al. The prognostic impact of lung adenocarcinoma predominance classification relating to pathological factors in lobectomy, the Japanese Joint Committee of Lung Cancer Registry Database in 2010. BMC Cancer, 2022, 22(1): 875.
5.	吳思凱, 王子民, 孫鏵, 等. CALGB140503研究: 亞肺葉切除是早期周圍型肺癌的標準術式? 中國胸心血管外科臨床雜志, 2023, 30(8): 1097-1101.Wu SK, Wang ZM, Sun H, et al. CALGB 140503 trial: is sublobectomy a standard surgical procedure for early-stage peripheral lung cancer? Chin J Clin Thorac Cardiovasc Surg, 2023, 30(8): 1097-1101.
6.	李剛, 羅俊, 鄧漢宇, 等. 非小細胞肺癌術中淋巴結清掃方式的研究進展. 中國胸心血管外科臨床雜志, 2019, 26(3): 282-289.Li G, Luo J, Deng HY, et al. Research advances in lymph node dissection in non-small cell lung cancer. Chin J Clin Thorac Cardiovasc Surg, 2019, 26(3): 282-289.
7.	Matsushima K, Sonoda D, Mitsui A, et al. Factors associated with lymph node metastasis upstage after resection for patients with micropapillary lung adenocarcinoma. Thorac Cancer, 2022, 13(1): 48-53.
8.	尹純同, 張春巖, 李華偉, 等. T1期肺腺癌患者淋巴結轉移相關因素分析. 中國胸心血管外科臨床雜志, 2018, 25(9): 755-761.Yin CT, Zhang CY, Li HW, et al. Factors associated with lymph node metastasis in patients with T1 stage lung adenocarcinoma. Chin J Clin Thorac Cardiovasc Surg, 2018, 25(9): 755-761.
9.	張杰石, 秦應之, 黃誠, 等. 侵襲性肺腺癌微乳頭亞型與淋巴結轉移的相關性分析. 臨床外科雜志, 2017, 25(7): 498-499.Zhang JS, Qin YZ, Huang C, et al. Correlation analysis of invasive pulmonary adenocarcinoma micropapillary subtype and lymph node metastasis. J Clin Surg, 2017, 25(7): 498-499.
10.	楊彥輝, 李季, 王毅, 等. 直徑≤3 cm肺腺癌胸腔鏡術后淋巴結轉移的預測模型構建. 中國胸心血管外科臨床雜志, 2024, 31(1): 71-77.Yang YH, Li J, Wang Y, et al. A predictive model of lymph node metastasis after thoracoscopic surgery for lung adenocarcinoma with a diameter ≤3 cm. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(1): 71-77.
11.	林耀彬, 林勇斌, 趙澤銳, 等. 《人工智能在肺結節診治中的應用專家共識(2022年版)》解讀. 中國胸心血管外科臨床雜志, 2023, 30(5): 665-671.Lin YB, Lin YB, Zhao ZR, et al. Interpretation of the expert consensus on artificial intelligence assisted management for pulmonary nodules (2022 edition). Chin J Clin Thorac Cardiovasc Surg, 2023, 30(5): 665-671.
12.	Cardillo G, Petersen RH, Ricciardi S, et al. European guidelines for the surgical management of pure ground-glass opacities and part-solid nodules: Task Force of the European Association of Cardio-Thoracic Surgery and the European Society of Thoracic Surgeons. Eur J Cardiothorac Surg, 2023, 64(4): ezad222.
13.	Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
14.	Aokage K, Miyoshi T, Ishii G, et al. Influence of ground glass opacity and the corresponding pathological findings on survival in patients with clinical stageⅠnon-small cell lung cancer. J Thorac Oncol, 2018, 13(4): 533-542.
15.	Suzuki K, Watanabe SI, Wakabayashi M, et al. A single-arm study of sublobar resection for ground-glass opacity dominant peripheral lung cancer. J Thorac Cardiovasc Surg, 2022, 163(1): 289-301.
16.	Aokage K, Suzuki K, Saji H, et al. Segmentectomy for ground-glass-dominant lung cancer with a tumour diameter of 3 cm or less including ground-glass opacity (JCOG1211): a multicentre, single-arm, confirmatory, phase 3 trial. Lancet Respir Med, 2023, 11(6): 540-549.
17.	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.
18.	Altorki N, Wang X, Kozono D, et al. Lobar or sublobar resection for peripheral stage ⅠA non-small-cell lung cancer. N Engl J Med, 2023, 388(6): 489-498.
19.	Zhang W, Mu G, Huang J, et al. Lymph node metastasis and its risk factors in T1 lung adenocarcinoma. Thorac Cancer, 2023, 14(30): 2993-3000.
20.	Liu C, Wang LC, Chen HS, et al. Outcomes of patients with different lepidic percentage and tumor size of stageⅠlung adenocarcinoma. Thorac Cancer, 2022, 13(14): 2005-2013.
21.	于航, 張永奎, 竺王玉, 等. 浸潤性肺腺癌淋巴結轉移情況及相關危險因素分析. 浙江醫學, 2022, 44(4): 388-391.Yu H, Zhang YK, Zhu WY, et al. Risk factors of lymph node metastasis in patients with invasive adenocarcinoma. Zhejiang Med J, 2022, 44(4): 388-391.
22.	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.
23.	Wang Z, Wu Y, Wang L, et al. Predicting occult lymph node metastasis by nomogram in patients with lung adenocarcinoma≤2 cm. Future Oncol, 2021, 17(16): 2005-2013.
24.	何慧, 張永奎. 1 085例手術切除浸潤性肺腺癌淋巴結轉移的相關因素分析及諾模圖模型的建立. 中國腫瘤臨床, 2021, 48(4): 169-173.He H, Zhang YK. Analysis of factors associated with lymph node metastasis in 1 085 patients with invasive lung adenocarcinoma and construction of a nomogram. Chin J Clin Oncol, 2021, 48(4): 169-173.
25.	孫嘉陽, 魯志剛, 郭占林, 等. 老年臨床N0期非小細胞肺癌患者術后N1-2期淋巴結轉移的危險因素分析. 中華實用診斷與治療雜志, 2023, 37(2): 129-132.Sun JY, Lu ZG, Guo ZL, et al. Risk factors of postoperative N1-2 stage lymph node metastasis in elderly patients with clinical N0 stage non-small cell lung cancer. J Chin Pract Diagn Ther, 2023, 37(2): 129-132.
26.	馬杰, 馬冬春, 陳啟斌, 等. 直徑≤3 cm浸潤性肺腺癌脈管侵犯的危險因素分析. 實用癌癥雜志, 2021, 36(1): 135-138.Ma J, Ma DC, Chen QB, et al. Analysis of risk factors of vascular invasion for invasive lung adenocarcinoma≤3 cm in diameter. Pract J Cancer, 2021, 36(1): 135-138.
27.	Shigenobu T, Takahashi Y, Masugi Y, et al. Micropapillary predominance is a risk factor for brain metastasis in resected lung adenocarcinoma. Clin Lung Cancer, 2021, 22(6): e820-e828.

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. Succony L, Rassl DM, Barker AP, et al. Adenocarcinoma spectrum lesions of the lung: detection, pathology and treatment strategies. Cancer Treat Rev, 2021, 99: 102237.
3. Asamura H, Nishimura KK, Giroux DJ, et al. IASLC lung cancer staging project: the new database to inform revisions in the ninth edition of the TNM classification of lung cancer. J Thorac Oncol, 2023, 18(5): 564-575.
4. Ito H, Date H, Shintani Y, et al. The prognostic impact of lung adenocarcinoma predominance classification relating to pathological factors in lobectomy, the Japanese Joint Committee of Lung Cancer Registry Database in 2010. BMC Cancer, 2022, 22(1): 875.
5. 吳思凱, 王子民, 孫鏵, 等. CALGB140503研究: 亞肺葉切除是早期周圍型肺癌的標準術式? 中國胸心血管外科臨床雜志, 2023, 30(8): 1097-1101.Wu SK, Wang ZM, Sun H, et al. CALGB 140503 trial: is sublobectomy a standard surgical procedure for early-stage peripheral lung cancer? Chin J Clin Thorac Cardiovasc Surg, 2023, 30(8): 1097-1101.
6. 李剛, 羅俊, 鄧漢宇, 等. 非小細胞肺癌術中淋巴結清掃方式的研究進展. 中國胸心血管外科臨床雜志, 2019, 26(3): 282-289.Li G, Luo J, Deng HY, et al. Research advances in lymph node dissection in non-small cell lung cancer. Chin J Clin Thorac Cardiovasc Surg, 2019, 26(3): 282-289.
7. Matsushima K, Sonoda D, Mitsui A, et al. Factors associated with lymph node metastasis upstage after resection for patients with micropapillary lung adenocarcinoma. Thorac Cancer, 2022, 13(1): 48-53.
8. 尹純同, 張春巖, 李華偉, 等. T1期肺腺癌患者淋巴結轉移相關因素分析. 中國胸心血管外科臨床雜志, 2018, 25(9): 755-761.Yin CT, Zhang CY, Li HW, et al. Factors associated with lymph node metastasis in patients with T1 stage lung adenocarcinoma. Chin J Clin Thorac Cardiovasc Surg, 2018, 25(9): 755-761.
9. 張杰石, 秦應之, 黃誠, 等. 侵襲性肺腺癌微乳頭亞型與淋巴結轉移的相關性分析. 臨床外科雜志, 2017, 25(7): 498-499.Zhang JS, Qin YZ, Huang C, et al. Correlation analysis of invasive pulmonary adenocarcinoma micropapillary subtype and lymph node metastasis. J Clin Surg, 2017, 25(7): 498-499.
10. 楊彥輝, 李季, 王毅, 等. 直徑≤3 cm肺腺癌胸腔鏡術后淋巴結轉移的預測模型構建. 中國胸心血管外科臨床雜志, 2024, 31(1): 71-77.Yang YH, Li J, Wang Y, et al. A predictive model of lymph node metastasis after thoracoscopic surgery for lung adenocarcinoma with a diameter ≤3 cm. Chin J Clin Thorac Cardiovasc Surg, 2024, 31(1): 71-77.
11. 林耀彬, 林勇斌, 趙澤銳, 等. 《人工智能在肺結節診治中的應用專家共識(2022年版)》解讀. 中國胸心血管外科臨床雜志, 2023, 30(5): 665-671.Lin YB, Lin YB, Zhao ZR, et al. Interpretation of the expert consensus on artificial intelligence assisted management for pulmonary nodules (2022 edition). Chin J Clin Thorac Cardiovasc Surg, 2023, 30(5): 665-671.
12. Cardillo G, Petersen RH, Ricciardi S, et al. European guidelines for the surgical management of pure ground-glass opacities and part-solid nodules: Task Force of the European Association of Cardio-Thoracic Surgery and the European Society of Thoracic Surgeons. Eur J Cardiothorac Surg, 2023, 64(4): ezad222.
13. Ginsberg RJ, Rubinstein LV. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg, 1995, 60(3): 615-622.
14. Aokage K, Miyoshi T, Ishii G, et al. Influence of ground glass opacity and the corresponding pathological findings on survival in patients with clinical stageⅠnon-small cell lung cancer. J Thorac Oncol, 2018, 13(4): 533-542.
15. Suzuki K, Watanabe SI, Wakabayashi M, et al. A single-arm study of sublobar resection for ground-glass opacity dominant peripheral lung cancer. J Thorac Cardiovasc Surg, 2022, 163(1): 289-301.
16. Aokage K, Suzuki K, Saji H, et al. Segmentectomy for ground-glass-dominant lung cancer with a tumour diameter of 3 cm or less including ground-glass opacity (JCOG1211): a multicentre, single-arm, confirmatory, phase 3 trial. Lancet Respir Med, 2023, 11(6): 540-549.
17. 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.
18. Altorki N, Wang X, Kozono D, et al. Lobar or sublobar resection for peripheral stage ⅠA non-small-cell lung cancer. N Engl J Med, 2023, 388(6): 489-498.
19. Zhang W, Mu G, Huang J, et al. Lymph node metastasis and its risk factors in T1 lung adenocarcinoma. Thorac Cancer, 2023, 14(30): 2993-3000.
20. Liu C, Wang LC, Chen HS, et al. Outcomes of patients with different lepidic percentage and tumor size of stageⅠlung adenocarcinoma. Thorac Cancer, 2022, 13(14): 2005-2013.
21. 于航, 張永奎, 竺王玉, 等. 浸潤性肺腺癌淋巴結轉移情況及相關危險因素分析. 浙江醫學, 2022, 44(4): 388-391.Yu H, Zhang YK, Zhu WY, et al. Risk factors of lymph node metastasis in patients with invasive adenocarcinoma. Zhejiang Med J, 2022, 44(4): 388-391.
22. 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.
23. Wang Z, Wu Y, Wang L, et al. Predicting occult lymph node metastasis by nomogram in patients with lung adenocarcinoma≤2 cm. Future Oncol, 2021, 17(16): 2005-2013.
24. 何慧, 張永奎. 1 085例手術切除浸潤性肺腺癌淋巴結轉移的相關因素分析及諾模圖模型的建立. 中國腫瘤臨床, 2021, 48(4): 169-173.He H, Zhang YK. Analysis of factors associated with lymph node metastasis in 1 085 patients with invasive lung adenocarcinoma and construction of a nomogram. Chin J Clin Oncol, 2021, 48(4): 169-173.
25. 孫嘉陽, 魯志剛, 郭占林, 等. 老年臨床N0期非小細胞肺癌患者術后N1-2期淋巴結轉移的危險因素分析. 中華實用診斷與治療雜志, 2023, 37(2): 129-132.Sun JY, Lu ZG, Guo ZL, et al. Risk factors of postoperative N1-2 stage lymph node metastasis in elderly patients with clinical N0 stage non-small cell lung cancer. J Chin Pract Diagn Ther, 2023, 37(2): 129-132.
26. 馬杰, 馬冬春, 陳啟斌, 等. 直徑≤3 cm浸潤性肺腺癌脈管侵犯的危險因素分析. 實用癌癥雜志, 2021, 36(1): 135-138.Ma J, Ma DC, Chen QB, et al. Analysis of risk factors of vascular invasion for invasive lung adenocarcinoma≤3 cm in diameter. Pract J Cancer, 2021, 36(1): 135-138.
27. Shigenobu T, Takahashi Y, Masugi Y, et al. Micropapillary predominance is a risk factor for brain metastasis in resected lung adenocarcinoma. Clin Lung Cancer, 2021, 22(6): e820-e828.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Risk factors associated with lymph node metastasis in lung adenocarcinoma with a diameter≤3 cm

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