High risk factors in images for infiltrating lung adenocarcinoma manifesting as peripheral ground-glass nodules_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

LIU Jiangjiang ¹ , YU Xiaojun ¹ , HUANG Haitao ² , CHEN Shaomu ² , PAN Liangbin ² , FENG Yu ² , CHEN Ke ² , MAO Guocai ² ,  MA Haitao ^1,2

1. Department of Thoracic Surgery, Du Shu Lake Hospital Affiliated to Soochow University, Suzhou, 215006, Jiangsu, P. R. China;
2. Department of Thoracic Surgery, The First Affiliated Hospital of Soochow University, Suzhou, 215006, Jiangsu, P. R. China;

Corresponding author：

MA Haitao, Email: mht7403@163.com

Keywords：

Ground-glass pulmonary nodules; invasive; lung adenocarcinoma; thin-section CT; imaging features

DOI：

10.7507/1007-4848.202203004

Video：

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Objective To explore the correlation between the imaging features of peripheral ground-glass pulmonary nodules and the invasion degree of lung adenocarcinoma, and the high risk factors for infiltrating lung adenocarcinoma under thin-slice CT, which provides some reference for clinicians to plan the surgical methods of pulmonary nodules before operation and to better communicate with patients, and assists in building a clinical predictive model for invasive adenocarcinoma. Methods Clinical data of the patients with peripheral ground-glass pulmonary nodules (diameter≤3 cm) in thin-slice chest CT in the First Affiliated Hospital of Soochow University from January 2019 to January 2020 were continuously collected. All patients underwent thin-slice CT scan and thoracoscopic surgery in our center. According to the pathological examination results, they were divided into two groups: an adenocarcinoma lesions before infiltration group, and an invasive lung adenocarcinoma group. The thin-slice CT imaging parameters of pulmonary nodules were collected. The nodular diameter, mean CT value, consolidation tumor ratio (CTR), nodular shape, vacuolar sign, bronchial air sign, lobulation sign, burr sign, lesion boundary, pleural depression sign, vascular cluster sign and other clinical data were collected. Univariate and multivariate analyses were conducted to analyze the independent risk factors for the infiltrating lung adenocarcinoma, and to analyze the threshold value and efficacy of each factor for the identification of infiltrating lung adenocarcinoma. Results Finally 190 patients were enrolled. There were 110 patients in the adenocarcinoma lesions before infiltration group, including 21 males and 89 females with a mean age of 53.57±10.90 years, and 80 patients in the invasive lung adenocarcinoma group, including 31 males and 49 females with a mean age of 56.45±11.30 years. There was a statistical difference in the mean CT value, nodular diameter, CTR, gender, smoking, nodular type, nodular shape, vacuolar sign, lobulation sign, burr sign, lesion boundary, pleural depression sign, vascular cluster sign between the two groups (P＜0.05). However, there was no statistical difference between the two groups in age (P=0.081), lesion site (P=0.675), and bronchial air sign (P=0.051). Multiple logistic regression analysis showed that nodular diameter, mean CT value, CTR and lobulation sign were independent risk factors for differentiating preinvasive adenocarcinoma from invasive adenocarcinoma. At the same time, the threshold value was calculated by Youden index, indicating that the CTR was 0.45, the nodal diameter was 10.5 mm and the mean CT value was –452 Hu. Conclusion In the peripheral ground-glass pulmonary nodules, according to the patient's CT imaging features, such as mixed ground-glass nodules, irregular shapes, vacuoles, short burrs, clear boundaries, pleural indentations, and vascular clusters, have a certain reference value in the discrimination of the invasion degree of ground-glass pulmonary nodules. At the same time, it is found in this research that peripheral ground-glass pulmonary nodules with diameter greater than 10.5 mm, CT value greater than –452 Hu, CTR greater than 0.45 and lobulation sign are more likely to be infiltrating lung adenocarcinoma.

Citation： LIU Jiangjiang, YU Xiaojun, HUANG Haitao, CHEN Shaomu, PAN Liangbin, FENG Yu, CHEN Ke, MAO Guocai, MA Haitao. High risk factors in images for infiltrating lung adenocarcinoma manifesting as peripheral ground-glass nodules. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(1): 85-91. doi: 10.7507/1007-4848.202203004 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.	Cao M, Chen W. Epidemiology of lung cancer in China. Thorac Cancer, 2019, 10(1): 3-7.
3.	Yang D, Liu Y, Bai C, et al. Epidemiology of lung cancer and lung cancer screening programs in China and the United States. Cancer Lett, 2020, 468: 82-87.
4.	Zheng S, Guo J, Cui X, et al. Automatic pulmonary nodule detection in CT scans using convolutional neural networks based on maximum intensity projection. IEEE Trans Med Imaging, 2020, 39(3): 797-805.
5.	蔡顺达, 吴湘萍. 多排螺旋CT对肺小结节及早期肺癌的诊断价值. 临床医药文献电子杂志, 2019, 6(A4): 171-172.
6.	Bade BC, Dela Cruz CS. Lung cancer 2020: Epidemiology, etiology, and prevention. Clin Chest Med, 2020, 41(1): 1-24.
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.	Ettinger DS, Wood DE, Aggarwal C, et al. NCCN guidelines insights: Non-small cell lung cancer, version 1. 2020. J Natl Compr Canc Netw, 2019, 17(12): 1464-1472.
9.	Yang J, Wang H, Geng C, et al. Advances in intelligent diagnosis methods for pulmonary ground-glass opacity nodules. Biomed Eng Online, 2018, 17(1): 20.
10.	车思雨, 蒋依宁, 韩广庆, 等. 基于CT图像的神经网络模型鉴别纯磨玻璃样微浸润性腺癌和浸润性腺癌. 实用医学杂志, 2020, 36(23): 3273-3278.
11.	Wu L, Gao C, Xiang P, et al. CT-imaging based analysis of invasive lung adenocarcinoma presenting as ground glass nodules using peri- and intra-nodular radiomic features. Front Oncol, 2020, 10: 838.
12.	耿国军, 米彦军, 朱晓雷, 等. 肺结节交互印证式诊断准确性及可行性研究: 1368例报告. 中国胸心血管外科临床杂志, 2020, 27(6): 669-674.
13.	Suzuki K, Koike T, Asakawa T, et al. A prospective radiological study of thin-section computed tomography to predict pathological noninvasiveness in peripheral clinical ⅠA lung cancer (Japan Clinical Oncology Group 0201). J Thorac Oncol, 2011, 6(4): 751-756.
14.	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.
15.	明星, 吴非. 肺磨玻璃结节CT征象对早期肺腺癌的诊断价值. 国际医学放射学杂志, 2017, 40(1): 37-40.
16.	高丰, 葛虓俊, 李铭, 等. 不同病理类型肺部磨玻璃结节的CT诊断. 中华肿瘤杂志, 2014, 36(3): 188-192.
17.	李丽, 刘周, 杨倩, 等. 肺微小结节的CT影像学表现及诊断价值. 中国癌症防治杂志, 2020, 12(1): 90-95.
18.	Ding H, Shi J, Zhou X, et al. Value of CT characteristics in predicting invasiveness of adenocarcinoma presented as pulmonary ground-glass nodules. Thorac Cardiovasc Surg, 2017, 65(2): 136-141.
19.	Liu Y, Sun H, Zhou F, et al. Imaging features of TSCT predict the classification of pulmonary preinvasive lesion, minimally and invasive adenocarcinoma presented as ground glass nodules. Lung Cancer, 2017, 108: 192-197.
20.	Lee HJ, Kim YT, Kang CH, et al. Epidermal growth factor receptor mutation in lung adenocarcinomas: Relationship with CT characteristics and histologic subtypes. Radiology, 2013, 268(1): 254-264.
21.	金鑫, 赵绍宏, 高洁, 等. 纯磨玻璃密度肺腺癌病理分类及影像表现特点分析. 中华放射学杂志, 2014, 48(4): 283-287.
22.	Kobayashi Y, Mitsudomi T. Management of ground-glass opacities: Should all pulmonary lesions with ground-glass opacity be surgically resected? Transl Lung Cancer Res, 2013, 2(5): 354-363.
23.	Park CM, Goo JM, Lee HJ, et al. Nodular ground-glass opacity at thin-section CT: Histologic correlation and evaluation of change at follow-up. Radiographics, 2007, 27(2): 391-408.
24.	Berry MF, Gao R, Kunder CA, et al. Presence of even a small ground-glass component in lung adenocarcinoma predicts better survival. Clin Lung Cancer, 2018, 19(1): e47-e51.
25.	刘国荣, 程传虎, 蓝博文, 等. 多层螺旋CT探讨血管集束征对周围型小肺癌的诊断价值. 中国介入影像与治疗学, 2006, 3(4): 294-296.
26.	李惠民, 肖湘生. 肺结节CT影像评价. 中国医学计算机成像杂志, 2001, 7(1): 30-41.
27.	Wu F, Tian SP, Jin X, et al. CT and histopathologic characteristics of lung adenocarcinoma with pure ground-glass nodules 10 mm or less in diameter. Eur Radiol, 2017, 27(10): 4037-4043.
28.	巴文娟, 许迪, 尹柯, 等. HRCT征象评估纯磨玻璃结节浸润性: 肺结节圆度优于长-短径比值和分叶深度. 放射学实践, 2020, 35(12): 1542-1546.
29.	Heidinger BH, Anderson KR, Nemec U, et al. Lung adenocarcinoma manifesting as pure ground-glass nodules: Correlating CT size, volume, density, and roundness with histopathologic invasion and size. J Thorac Oncol, 2017, 12(8): 1288-1298.
30.	Lee HY, Choi YL, Lee KS, et al. Pure ground-glass opacity neoplastic lung nodules: Histopathology, imaging, and management. AJR Am J Roentgenol, 2014, 202(3): W224-W233.
31.	Lim HJ, Ahn S, Lee KS, et al. Persistent pure ground-glass opacity lung nodules≥ 10 mm in diameter at CT scan: Histopathologic comparisons and prognostic implications. Chest, 2013, 144(4): 1291-1299.
32.	吴汉然, 柳常青, 徐美青, 等. m-CT值在预测临床Ⅰa期肺癌和癌前病变恶性程度中的应用研究. 中国肺癌杂志, 2018, 21(3): 190-196.
33.	She Y, Zhao L, Dai C, et al. Preoperative nomogram for identifying invasive pulmonary adenocarcinoma in patients with pure ground-glass nodule: A multi-institutional study. Oncotarget, 2017, 8(10): 17229-17238.
34.	Jiang B, Wang J, Jia P, et al. The value of CT attenuation in distinguishing atypical adenomatous hyperplasia from adenocarcinoma in situ. Zhongguo Fei Ai Za Zhi, 2013, 16(11): 579-583.
35.	Kakinuma R, Noguchi M, Ashizawa K, et al. Natural history of pulmonary subsolid nodules: A prospective multicenter study. J Thorac Oncol, 2016, 11(7): 1012-1028.
36.	Sawada S, Yamashita N, Sugimoto R, et al. Long-term outcomes of patients with ground-glass opacities detected using CT scanning. Chest, 2017, 151(2): 308-315.
37.	Lee SM, Park CM, Goo JM, et al. Invasive pulmonary adenocarcinomas versus preinvasive lesions appearing as ground-glass nodules: Differentiation by using CT features. Radiology, 2013, 268(1): 265-273.
38.	Son JY, Lee HY, Lee KS, et al. Quantitative CT analysis of pulmonary ground-glass opacity nodules for the distinction of invasive adenocarcinoma from pre-invasive or minimally invasive adenocarcinoma. PLoS One, 2014, 9(8): e104066.

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. Cao M, Chen W. Epidemiology of lung cancer in China. Thorac Cancer, 2019, 10(1): 3-7.
3. Yang D, Liu Y, Bai C, et al. Epidemiology of lung cancer and lung cancer screening programs in China and the United States. Cancer Lett, 2020, 468: 82-87.
4. Zheng S, Guo J, Cui X, et al. Automatic pulmonary nodule detection in CT scans using convolutional neural networks based on maximum intensity projection. IEEE Trans Med Imaging, 2020, 39(3): 797-805.
5. 蔡顺达, 吴湘萍. 多排螺旋CT对肺小结节及早期肺癌的诊断价值. 临床医药文献电子杂志, 2019, 6(A4): 171-172.
6. Bade BC, Dela Cruz CS. Lung cancer 2020: Epidemiology, etiology, and prevention. Clin Chest Med, 2020, 41(1): 1-24.
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. Ettinger DS, Wood DE, Aggarwal C, et al. NCCN guidelines insights: Non-small cell lung cancer, version 1. 2020. J Natl Compr Canc Netw, 2019, 17(12): 1464-1472.
9. Yang J, Wang H, Geng C, et al. Advances in intelligent diagnosis methods for pulmonary ground-glass opacity nodules. Biomed Eng Online, 2018, 17(1): 20.
10. 车思雨, 蒋依宁, 韩广庆, 等. 基于CT图像的神经网络模型鉴别纯磨玻璃样微浸润性腺癌和浸润性腺癌. 实用医学杂志, 2020, 36(23): 3273-3278.
11. Wu L, Gao C, Xiang P, et al. CT-imaging based analysis of invasive lung adenocarcinoma presenting as ground glass nodules using peri- and intra-nodular radiomic features. Front Oncol, 2020, 10: 838.
12. 耿国军, 米彦军, 朱晓雷, 等. 肺结节交互印证式诊断准确性及可行性研究: 1368例报告. 中国胸心血管外科临床杂志, 2020, 27(6): 669-674.
13. Suzuki K, Koike T, Asakawa T, et al. A prospective radiological study of thin-section computed tomography to predict pathological noninvasiveness in peripheral clinical ⅠA lung cancer (Japan Clinical Oncology Group 0201). J Thorac Oncol, 2011, 6(4): 751-756.
14. 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.
15. 明星, 吴非. 肺磨玻璃结节CT征象对早期肺腺癌的诊断价值. 国际医学放射学杂志, 2017, 40(1): 37-40.
16. 高丰, 葛虓俊, 李铭, 等. 不同病理类型肺部磨玻璃结节的CT诊断. 中华肿瘤杂志, 2014, 36(3): 188-192.
17. 李丽, 刘周, 杨倩, 等. 肺微小结节的CT影像学表现及诊断价值. 中国癌症防治杂志, 2020, 12(1): 90-95.
18. Ding H, Shi J, Zhou X, et al. Value of CT characteristics in predicting invasiveness of adenocarcinoma presented as pulmonary ground-glass nodules. Thorac Cardiovasc Surg, 2017, 65(2): 136-141.
19. Liu Y, Sun H, Zhou F, et al. Imaging features of TSCT predict the classification of pulmonary preinvasive lesion, minimally and invasive adenocarcinoma presented as ground glass nodules. Lung Cancer, 2017, 108: 192-197.
20. Lee HJ, Kim YT, Kang CH, et al. Epidermal growth factor receptor mutation in lung adenocarcinomas: Relationship with CT characteristics and histologic subtypes. Radiology, 2013, 268(1): 254-264.
21. 金鑫, 赵绍宏, 高洁, 等. 纯磨玻璃密度肺腺癌病理分类及影像表现特点分析. 中华放射学杂志, 2014, 48(4): 283-287.
22. Kobayashi Y, Mitsudomi T. Management of ground-glass opacities: Should all pulmonary lesions with ground-glass opacity be surgically resected? Transl Lung Cancer Res, 2013, 2(5): 354-363.
23. Park CM, Goo JM, Lee HJ, et al. Nodular ground-glass opacity at thin-section CT: Histologic correlation and evaluation of change at follow-up. Radiographics, 2007, 27(2): 391-408.
24. Berry MF, Gao R, Kunder CA, et al. Presence of even a small ground-glass component in lung adenocarcinoma predicts better survival. Clin Lung Cancer, 2018, 19(1): e47-e51.
25. 刘国荣, 程传虎, 蓝博文, 等. 多层螺旋CT探讨血管集束征对周围型小肺癌的诊断价值. 中国介入影像与治疗学, 2006, 3(4): 294-296.
26. 李惠民, 肖湘生. 肺结节CT影像评价. 中国医学计算机成像杂志, 2001, 7(1): 30-41.
27. Wu F, Tian SP, Jin X, et al. CT and histopathologic characteristics of lung adenocarcinoma with pure ground-glass nodules 10 mm or less in diameter. Eur Radiol, 2017, 27(10): 4037-4043.
28. 巴文娟, 许迪, 尹柯, 等. HRCT征象评估纯磨玻璃结节浸润性: 肺结节圆度优于长-短径比值和分叶深度. 放射学实践, 2020, 35(12): 1542-1546.
29. Heidinger BH, Anderson KR, Nemec U, et al. Lung adenocarcinoma manifesting as pure ground-glass nodules: Correlating CT size, volume, density, and roundness with histopathologic invasion and size. J Thorac Oncol, 2017, 12(8): 1288-1298.
30. Lee HY, Choi YL, Lee KS, et al. Pure ground-glass opacity neoplastic lung nodules: Histopathology, imaging, and management. AJR Am J Roentgenol, 2014, 202(3): W224-W233.
31. Lim HJ, Ahn S, Lee KS, et al. Persistent pure ground-glass opacity lung nodules≥ 10 mm in diameter at CT scan: Histopathologic comparisons and prognostic implications. Chest, 2013, 144(4): 1291-1299.
32. 吴汉然, 柳常青, 徐美青, 等. m-CT值在预测临床Ⅰa期肺癌和癌前病变恶性程度中的应用研究. 中国肺癌杂志, 2018, 21(3): 190-196.
33. She Y, Zhao L, Dai C, et al. Preoperative nomogram for identifying invasive pulmonary adenocarcinoma in patients with pure ground-glass nodule: A multi-institutional study. Oncotarget, 2017, 8(10): 17229-17238.
34. Jiang B, Wang J, Jia P, et al. The value of CT attenuation in distinguishing atypical adenomatous hyperplasia from adenocarcinoma in situ. Zhongguo Fei Ai Za Zhi, 2013, 16(11): 579-583.
35. Kakinuma R, Noguchi M, Ashizawa K, et al. Natural history of pulmonary subsolid nodules: A prospective multicenter study. J Thorac Oncol, 2016, 11(7): 1012-1028.
36. Sawada S, Yamashita N, Sugimoto R, et al. Long-term outcomes of patients with ground-glass opacities detected using CT scanning. Chest, 2017, 151(2): 308-315.
37. Lee SM, Park CM, Goo JM, et al. Invasive pulmonary adenocarcinomas versus preinvasive lesions appearing as ground-glass nodules: Differentiation by using CT features. Radiology, 2013, 268(1): 265-273.
38. Son JY, Lee HY, Lee KS, et al. Quantitative CT analysis of pulmonary ground-glass opacity nodules for the distinction of invasive adenocarcinoma from pre-invasive or minimally invasive adenocarcinoma. PLoS One, 2014, 9(8): e104066.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

High risk factors in images for infiltrating lung adenocarcinoma manifesting as peripheral ground-glass nodules

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