Invasiveness assessment by CT quantitative and qualitative features of lung cancers manifesting ground-glass nodules in 555 patients: A retrospective cohort study_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

YANG Yantao ¹ , WANG Wei ² , YANG Yichen ¹ , WANG Biying ¹ , HU Huilian ¹ , JIANG Ziqi ¹ , CAI Dezhong ¹ , DUAN Yaowu ¹ , JIANG Jiezhi ³ , LUO Jia ⁴ , ZHAO Guangqiang ¹ , HUANG Yunchao ¹ ,  YE Lianhua ¹

1. Department of Thoracic and Cardiovascular Surgery, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Kunming, 650000, P. R. China;
2. Department of Thoracic and Cardiovascular Surgery, Shiyan Taihe Hospital (Hubei University of Medicine), Shiyan, 442000, Hubei,P. R. China;
3. Department of Radiology, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Kunming, 650000,P. R. China;
4. Department of Pathology, Yunnan Cancer Hospital, The Third Affiliated Hospital of Kunming Medical University, Kunming, 650000,P. R. China;

Corresponding author：

YE Lianhua, Email: Lhye1204@aliyun.com

Keywords：

Ground-glass nodule; radiologic feature; lung adenocarcinoma; invasiveness; prediction model

DOI：

10.7507/1007-4848.202302012

Video：

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Objective To explore the correlation between the quantitative and qualitative features of CT images and the invasiveness of pulmonary ground-glass nodules, providing reference value for preoperative planning of patients with ground-glass nodules. Methods The patients with ground-glass nodules who underwent surgical treatment and were diagnosed with pulmonary adenocarcinoma from September 2020 to July 2022 at the Third Affiliated Hospital of Kunming Medical University were collected. Based on the pathological diagnosis results, they were divided into two groups: a non-invasive adenocarcinoma group with in situ and minimally invasive adenocarcinoma, and an invasive adenocarcinoma group. Imaging features were collected, and a univariate logistic regression analysis was conducted on the clinical and imaging data of the patients. Variables with statistical difference were selected for multivariate logistic regression analysis to establish a predictive model of invasive adenocarcinoma based on independent risk factors. Finally, the sensitivity and specificity were calculated based on the Youden index. Results A total of 555 patients were collected. The were 310 patients in the non-invasive adenocarcinoma group, including 235 females and 75 males, with a meadian age of 49 (43, 58) years, and 245 patients in the invasive adenocarcinoma group, including 163 females and 82 males, with a meadian age of 53 (46, 61) years. The binary logistic regression analysis showed that the maximum diameter (OR=4.707, 95%CI 2.060 to 10.758), consolidation/tumor ratio (CTR, OR=1.027, 95%CI 1.011 to 1.043), maximum CT value (OR=1.025, 95%CI 1.004 to 1.047), mean CT value (OR=1.035, 95%CI 1.008 to 1.063), spiculation sign (OR=2.055, 95%CI 1.148 to 3.679), and vascular convergence sign (OR=2.508, 95%CI 1.345 to 4.676) were independent risk factors for the occurrence of invasive adenocarcinoma (P<0.05). Based on the independent predictive factors, a predictive model of invasive adenocarcinoma was constructed. The formula for the model prediction was: Logit(P)=–1.293+1.549×maximum diameter of lesion+0.026×CTR+0.025×maximum CT value+0.034×mean CT value+0.72×spiculation sign+0.919×vascular convergence sign. The area under the receiver operating characteristic curve of the model was 0.910 (95%CI 0.885 to 0.934), indicating that the model had good discrimination ability. The calibration curve showed that the predictive model had good calibration, and the decision analysis curve showed that the model had good clinical utility. Conclusion The predictive model combining quantitative and qualitative features of CT has a good predictive ability for the invasiveness of ground-glass nodules. Its predictive performance is higher than any single indicator.

Citation： YANG Yantao, WANG Wei, YANG Yichen, WANG Biying, HU Huilian, JIANG Ziqi, CAI Dezhong, DUAN Yaowu, JIANG Jiezhi, LUO Jia, ZHAO Guangqiang, HUANG Yunchao, YE Lianhua. Invasiveness assessment by CT quantitative and qualitative features of lung cancers manifesting ground-glass nodules in 555 patients: A retrospective cohort study. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2024, 31(1): 51-58. doi: 10.7507/1007-4848.202302012 Copy

1.	Marx A, Chan JK, Coindre JM, et al. The 2015 World Health Organization classification of tumors of the thymus: Continuity and changes. J Thorac Oncol, 2015, 10(10): 1383-1395.
2.	Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
3.	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.
4.	Watanabe Y, Hattori A, Nojiri S, et al. Clinical impact of a small component of ground-glass opacity in solid-dominant clinical stage ⅠA non-small cell lung cancer. J Thorac Cardiovasc Surg, 2022, 163(3): 791-801.
5.	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.
6.	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.
7.	姜格宁, 陈昶, 朱余明, 等. 上海市肺科医院磨玻璃结节早期肺腺癌的诊疗共识(第一版). 中国肺癌杂志, 2018, 21(3): 147-159.
8.	Wang XL, Sun XS, Yan CX, et al. CT-assisted improvements in the accuracy of the intraoperative frozen section examination of ground-glass density nodules. Comput Math Methods Med, 2022, 2022: 8967643.
9.	Fu F, Zhang Y, Wang S, et al. Computed tomography density is not associated with pathological tumor invasion for pure ground-glass nodules. J Thorac Cardiovasc Surg, 2021, 162(2): 451-459.
10.	韩丽珠, 叶兆祥, 李绪斌, 等. CT定量参数预测评估肺混合磨玻璃结节侵袭性的临床价值. 中国肿瘤临床, 2018, 45(6): 286-290.
11.	Dai J, Yu G, Yu J. Can CT imaging features of ground-glass opacity predict invasiveness? A meta-analysis. Thorac Cancer, 2018, 9(4): 452-458.
12.	Liang J, Xu XQ, Xu H, et al. Using the CT features to differentiate invasive pulmonary adenocarcinoma from pre-invasive lesion appearing as pure or mixed ground-glass nodules. Br J Radiol, 2015, 88(1053): 20140811.
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.	He S, Chen C, Wang Z, et al. The use of the mean computed-tomography value to predict the invasiveness of ground-glass nodules: A meta-analysis. Asian J Surg, 2023, 46(2): 677-682.
15.	Ichinose J, Kawaguchi Y, Nakao M, et al. Utility of maximum CT value in predicting the invasiveness of pure ground-glass nodules. Clin Lung Cancer, 2020, 21(3): 281-287.
16.	Zhou QJ, Zheng ZC, Zhu YQ, et al. Tumor invasiveness defined by IASLC/ATS/ERS classification of ground-glass nodules can be predicted by quantitative CT parameters. J Thorac Dis, 2017, 9(5): 1190-1200.
17.	郑慧, 李建玉, 王珊, 等. 基于肺磨玻璃结节CT征象的诊断模型列线图评估肺癌浸润性. 放射学实践, 2021, 36(4): 470-474.
18.	Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
19.	Wiener RS, Gould MK, Arenberg DA, et al. An official American Thoracic Society/American College of Chest Physicians policy statement: Implementation of low-dose computed tomography lung cancer screening programs in clinical practice. Am J Respir Crit Care Med, 2015, 192(7): 881-891.
20.	Sadate A, Occean BV, Beregi JP, et al. Systematic review and meta-analysis on the impact of lung cancer screening by low-dose computed tomography. Eur J Cancer, 2020, 134: 107-114.
21.	National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
22.	Li X, Zhang W, Yu Y, et al. CT features and quantitative analysis of subsolid nodule lung adenocarcinoma for pathological classification prediction. BMC Cancer, 2020, 20(1): 60.
23.	Zhang N, Liu JF, Wang YN, et al. A nomogram to predict invasiveness in lung adenocarcinoma presenting as ground glass nodule. Transl Cancer Res, 2020, 9(3): 1660-1669.
24.	Wu FZ, Chen PA, Wu CC, et al. Semiquantative visual assessment of sub-solid pulmonary nodules ≦3 cm in differentiation of lung adenocarcinoma spectrum. Sci Rep, 2017, 7(1): 15790.
25.	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.
26.	Han L, Zhang P, Wang Y, et al. CT quantitative parameters to predict the invasiveness of lung pure ground-glass nodules (pGGNs). Clin Radiol, 2018, 73(5): 504. e1-504. e7.
27.	Li Q, Gu YF, Fan L, et al. Effect of CT window settings on size measurements of the solid component in subsolid nodules: Evaluation of prediction efficacy of the degree of pathological malignancy in lung adenocarcinoma. Br J Radiol, 2018, 91(1088): 20180251.
28.	Yoo RE, Goo JM, Hwang EJ, et al. Retrospective assessment of interobserver agreement and accuracy in classifications and measurements in subsolid nodules with solid components less than 8 mm: Which window setting is better? Eur Radiol, 2017, 27(4): 1369-1376.
29.	Asamura H, Hishida T, Suzuki K, et al. Radiographically determined noninvasive adenocarcinoma of the lung: Survival outcomes of Japan Clinical Oncology Group 0201. J Thorac Cardiovasc Surg, 2013, 146(1): 24-30.
30.	Katsumata S, Aokage K, Nakasone S, et al. Radiologic criteria in predicting pathologic less invasive lung cancer according to TNM 8th edition. Clin Lung Cancer, 2019, 20(2): e163-e170.
31.	Ye T, Deng L, Xiang J, et al. Predictors of pathologic tumor invasion and prognosis for ground glass opacity featured lung adenocarcinoma. Ann Thorac Surg, 2018, 106(6): 1682-1690.
32.	Zhan Y, Peng X, Shan F, et al. Attenuation and morphologic characteristics distinguishing a ground-glass nodule measuring 5-10 mm in diameter as invasive lung adenocarcinoma on thin-slice CT. AJR Am J Roentgenol, 2019, 213(4): W162-W170.
33.	Hu F, Huang H, Jiang Y, et al. Discriminating invasive adenocarcinoma among lung pure ground-glass nodules: A multi-parameter prediction model. J Thorac Dis, 2021, 13(9): 5383-5394.
34.	Si MJ, Tao XF, Du GY, et al. Thin-section computed tomography-histopathologic comparisons of pulmonary focal interstitial fibrosis, atypical adenomatous hyperplasia, adenocarcinoma in situ, and minimally invasive adenocarcinoma with pure ground-glass opacity. Eur J Radiol, 2016, 85(10): 1708-1715.
35.	Gao F, Li M, Ge X, et al. Multi-detector spiral CT study of the relationships between pulmonary ground-glass nodules and blood vessels. Eur Radiol, 2013, 23(12): 3271-3277.
36.	Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer, 1995, 75(12): 2844-2852.
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.	Zhang Y, Shen Y, Qiang JW, et al. HRCT features distinguishing pre-invasive from invasive pulmonary adenocarcinomas appearing as ground-glass nodules. Eur Radiol, 2016, 26(9): 2921-2928.
39.	Ikehara M, Saito H, Kondo T, et al. Comparison of thin-section CT and pathological findings in small solid-density type pulmonary adenocarcinoma: Prognostic factors from CT findings. Eur J Radiol, 2012, 81(1): 189-194.
40.	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.

1. Marx A, Chan JK, Coindre JM, et al. The 2015 World Health Organization classification of tumors of the thymus: Continuity and changes. J Thorac Oncol, 2015, 10(10): 1383-1395.
2. Naidich DP, Bankier AA, MacMahon H, et al. Recommendations for the management of subsolid pulmonary nodules detected at CT: A statement from the Fleischner Society. Radiology, 2013, 266(1): 304-317.
3. 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.
4. Watanabe Y, Hattori A, Nojiri S, et al. Clinical impact of a small component of ground-glass opacity in solid-dominant clinical stage ⅠA non-small cell lung cancer. J Thorac Cardiovasc Surg, 2022, 163(3): 791-801.
5. 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.
6. 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.
7. 姜格宁, 陈昶, 朱余明, 等. 上海市肺科医院磨玻璃结节早期肺腺癌的诊疗共识(第一版). 中国肺癌杂志, 2018, 21(3): 147-159.
8. Wang XL, Sun XS, Yan CX, et al. CT-assisted improvements in the accuracy of the intraoperative frozen section examination of ground-glass density nodules. Comput Math Methods Med, 2022, 2022: 8967643.
9. Fu F, Zhang Y, Wang S, et al. Computed tomography density is not associated with pathological tumor invasion for pure ground-glass nodules. J Thorac Cardiovasc Surg, 2021, 162(2): 451-459.
10. 韩丽珠, 叶兆祥, 李绪斌, 等. CT定量参数预测评估肺混合磨玻璃结节侵袭性的临床价值. 中国肿瘤临床, 2018, 45(6): 286-290.
11. Dai J, Yu G, Yu J. Can CT imaging features of ground-glass opacity predict invasiveness? A meta-analysis. Thorac Cancer, 2018, 9(4): 452-458.
12. Liang J, Xu XQ, Xu H, et al. Using the CT features to differentiate invasive pulmonary adenocarcinoma from pre-invasive lesion appearing as pure or mixed ground-glass nodules. Br J Radiol, 2015, 88(1053): 20140811.
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. He S, Chen C, Wang Z, et al. The use of the mean computed-tomography value to predict the invasiveness of ground-glass nodules: A meta-analysis. Asian J Surg, 2023, 46(2): 677-682.
15. Ichinose J, Kawaguchi Y, Nakao M, et al. Utility of maximum CT value in predicting the invasiveness of pure ground-glass nodules. Clin Lung Cancer, 2020, 21(3): 281-287.
16. Zhou QJ, Zheng ZC, Zhu YQ, et al. Tumor invasiveness defined by IASLC/ATS/ERS classification of ground-glass nodules can be predicted by quantitative CT parameters. J Thorac Dis, 2017, 9(5): 1190-1200.
17. 郑慧, 李建玉, 王珊, 等. 基于肺磨玻璃结节CT征象的诊断模型列线图评估肺癌浸润性. 放射学实践, 2021, 36(4): 470-474.
18. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2020. CA Cancer J Clin, 2020, 70(1): 7-30.
19. Wiener RS, Gould MK, Arenberg DA, et al. An official American Thoracic Society/American College of Chest Physicians policy statement: Implementation of low-dose computed tomography lung cancer screening programs in clinical practice. Am J Respir Crit Care Med, 2015, 192(7): 881-891.
20. Sadate A, Occean BV, Beregi JP, et al. Systematic review and meta-analysis on the impact of lung cancer screening by low-dose computed tomography. Eur J Cancer, 2020, 134: 107-114.
21. National Lung Screening Trial Research Team, Aberle DR, Adams AM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med, 2011, 365(5): 395-409.
22. Li X, Zhang W, Yu Y, et al. CT features and quantitative analysis of subsolid nodule lung adenocarcinoma for pathological classification prediction. BMC Cancer, 2020, 20(1): 60.
23. Zhang N, Liu JF, Wang YN, et al. A nomogram to predict invasiveness in lung adenocarcinoma presenting as ground glass nodule. Transl Cancer Res, 2020, 9(3): 1660-1669.
24. Wu FZ, Chen PA, Wu CC, et al. Semiquantative visual assessment of sub-solid pulmonary nodules ≦3 cm in differentiation of lung adenocarcinoma spectrum. Sci Rep, 2017, 7(1): 15790.
25. 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.
26. Han L, Zhang P, Wang Y, et al. CT quantitative parameters to predict the invasiveness of lung pure ground-glass nodules (pGGNs). Clin Radiol, 2018, 73(5): 504. e1-504. e7.
27. Li Q, Gu YF, Fan L, et al. Effect of CT window settings on size measurements of the solid component in subsolid nodules: Evaluation of prediction efficacy of the degree of pathological malignancy in lung adenocarcinoma. Br J Radiol, 2018, 91(1088): 20180251.
28. Yoo RE, Goo JM, Hwang EJ, et al. Retrospective assessment of interobserver agreement and accuracy in classifications and measurements in subsolid nodules with solid components less than 8 mm: Which window setting is better? Eur Radiol, 2017, 27(4): 1369-1376.
29. Asamura H, Hishida T, Suzuki K, et al. Radiographically determined noninvasive adenocarcinoma of the lung: Survival outcomes of Japan Clinical Oncology Group 0201. J Thorac Cardiovasc Surg, 2013, 146(1): 24-30.
30. Katsumata S, Aokage K, Nakasone S, et al. Radiologic criteria in predicting pathologic less invasive lung cancer according to TNM 8th edition. Clin Lung Cancer, 2019, 20(2): e163-e170.
31. Ye T, Deng L, Xiang J, et al. Predictors of pathologic tumor invasion and prognosis for ground glass opacity featured lung adenocarcinoma. Ann Thorac Surg, 2018, 106(6): 1682-1690.
32. Zhan Y, Peng X, Shan F, et al. Attenuation and morphologic characteristics distinguishing a ground-glass nodule measuring 5-10 mm in diameter as invasive lung adenocarcinoma on thin-slice CT. AJR Am J Roentgenol, 2019, 213(4): W162-W170.
33. Hu F, Huang H, Jiang Y, et al. Discriminating invasive adenocarcinoma among lung pure ground-glass nodules: A multi-parameter prediction model. J Thorac Dis, 2021, 13(9): 5383-5394.
34. Si MJ, Tao XF, Du GY, et al. Thin-section computed tomography-histopathologic comparisons of pulmonary focal interstitial fibrosis, atypical adenomatous hyperplasia, adenocarcinoma in situ, and minimally invasive adenocarcinoma with pure ground-glass opacity. Eur J Radiol, 2016, 85(10): 1708-1715.
35. Gao F, Li M, Ge X, et al. Multi-detector spiral CT study of the relationships between pulmonary ground-glass nodules and blood vessels. Eur Radiol, 2013, 23(12): 3271-3277.
36. Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer, 1995, 75(12): 2844-2852.
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. Zhang Y, Shen Y, Qiang JW, et al. HRCT features distinguishing pre-invasive from invasive pulmonary adenocarcinomas appearing as ground-glass nodules. Eur Radiol, 2016, 26(9): 2921-2928.
39. Ikehara M, Saito H, Kondo T, et al. Comparison of thin-section CT and pathological findings in small solid-density type pulmonary adenocarcinoma: Prognostic factors from CT findings. Eur J Radiol, 2012, 81(1): 189-194.
40. 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.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Invasiveness assessment by CT quantitative and qualitative features of lung cancers manifesting ground-glass nodules in 555 patients: A retrospective cohort study

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