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.	蔡順達, 吳湘萍. 多排螺旋CT對肺小結節及早期肺癌的診斷價值. 臨床醫藥文獻電子雜志, 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.	車思雨, 蔣依寧, 韓廣慶, 等. 基于CT圖像的神經網絡模型鑒別純磨玻璃樣微浸潤性腺癌和浸潤性腺癌. 實用醫學雜志, 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.	耿國軍, 米彥軍, 朱曉雷, 等. 肺結節交互印證式診斷準確性及可行性研究: 1368例報告. 中國胸心血管外科臨床雜志, 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, 吳非. 肺磨玻璃結節CT征象對早期肺腺癌的診斷價值. 國際醫學放射學雜志, 2017, 40(1): 37-40.
16.	高豐, 葛虓俊, 李銘, 等. 不同病理類型肺部磨玻璃結節的CT診斷. 中華腫瘤雜志, 2014, 36(3): 188-192.
17.	李麗, 劉周, 楊倩, 等. 肺微小結節的CT影像學表現及診斷價值. 中國癌癥防治雜志, 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, 趙紹宏, 高潔, 等. 純磨玻璃密度肺腺癌病理分類及影像表現特點分析. 中華放射學雜志, 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.	劉國榮, 程傳虎, 藍博文, 等. 多層螺旋CT探討血管集束征對周圍型小肺癌的診斷價值. 中國介入影像與治療學, 2006, 3(4): 294-296.
26.	李惠民, 肖湘生. 肺結節CT影像評價. 中國醫學計算機成像雜志, 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, 許迪, 尹柯, 等. HRCT征象評估純磨玻璃結節浸潤性: 肺結節圓度優于長-短徑比值和分葉深度. 放射學實踐, 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.	吳漢然, 柳常青, 徐美青, 等. m-CT值在預測臨床Ⅰa期肺癌和癌前病變惡性程度中的應用研究. 中國肺癌雜志, 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. 蔡順達, 吳湘萍. 多排螺旋CT對肺小結節及早期肺癌的診斷價值. 臨床醫藥文獻電子雜志, 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. 車思雨, 蔣依寧, 韓廣慶, 等. 基于CT圖像的神經網絡模型鑒別純磨玻璃樣微浸潤性腺癌和浸潤性腺癌. 實用醫學雜志, 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. 耿國軍, 米彥軍, 朱曉雷, 等. 肺結節交互印證式診斷準確性及可行性研究: 1368例報告. 中國胸心血管外科臨床雜志, 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, 吳非. 肺磨玻璃結節CT征象對早期肺腺癌的診斷價值. 國際醫學放射學雜志, 2017, 40(1): 37-40.
16. 高豐, 葛虓俊, 李銘, 等. 不同病理類型肺部磨玻璃結節的CT診斷. 中華腫瘤雜志, 2014, 36(3): 188-192.
17. 李麗, 劉周, 楊倩, 等. 肺微小結節的CT影像學表現及診斷價值. 中國癌癥防治雜志, 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, 趙紹宏, 高潔, 等. 純磨玻璃密度肺腺癌病理分類及影像表現特點分析. 中華放射學雜志, 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. 劉國榮, 程傳虎, 藍博文, 等. 多層螺旋CT探討血管集束征對周圍型小肺癌的診斷價值. 中國介入影像與治療學, 2006, 3(4): 294-296.
26. 李惠民, 肖湘生. 肺結節CT影像評價. 中國醫學計算機成像雜志, 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, 許迪, 尹柯, 等. HRCT征象評估純磨玻璃結節浸潤性: 肺結節圓度優于長-短徑比值和分葉深度. 放射學實踐, 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. 吳漢然, 柳常青, 徐美青, 等. m-CT值在預測臨床Ⅰa期肺癌和癌前病變惡性程度中的應用研究. 中國肺癌雜志, 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

Abstract Full text Figures/Tables Video References Cited by

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