The advancements in natural growth history of pulmonary ground-glass nodules_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

FAN Ziwen , XIE Dong , JIANG Gening ,  CHEN Chang

Department of Thoracic Surgery, Shanghai Pulmonary Hospital, Tongji University, Shanghai, 200433, P.R.China;

Corresponding author：

CHEN Chang, Email: changchenc@hotmail.com

Keywords：

Ground-glass nodules; early stage lung cancer; growth history; radiomics

DOI：

10.7507/1007-4848.201804045

Video：

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With the development of thin section axial computed tomography scan, the detection rate of pulmonary ground-glass nodules (GGN) continues increasing. GGN has a special natural growth history: pure ground-glass nodules (PGGN) smaller than 10 mm can hold steady for a long term, surgery resection is unnecessary, patients need regular follow up. Larger part solid ground-glass nodules (PSN) with a solid component can be malignant early stage lung cancer, which requires early surgery intervention. Establishment of a standard definition of GGN growth, investments in the long term natural growth history of GGN, validation of the clinical, radiology and genetic risk factors would be beneficial for the management of GGN patients.

Citation： FAN Ziwen, XIE Dong, JIANG Gening, CHEN Chang. The advancements in natural growth history of pulmonary ground-glass nodules. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2019, 26(2): 175-179. doi: 10.7507/1007-4848.201804045 Copy

1.	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.
2.	MacMahon H, Naidich DP, Goo JM, et al. Guidelines for management of incidental pulmonary nodules detected on CT images: From the fleischner society 2017. Radiology, 2017, 284(1): 228-243.
3.	Baldwin DR, Callister ME, Guideline development group. The British Thoracic Society guidelines on the investigation and management of pulmonary nodules. Thorax, 2015, 70(8): 794-798.
4.	Travis WD, Asamura H, Bankier AA, et al. The IASLC lung cancer staging project: proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol, 2016, 11(8): 1204-1223.
5.	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: 354-363.
6.	Revel MP, Bissery A, Bienvenu M, et al. Are two-dimensional CT measurements of small noncalcified pulmonary nodules reliable? Radiology, 2004, 231(2): 453-458.
7.	Kakinuma R, Ashizawa K, Kuriyama K, et al. Measurement of focal ground-glass opacity diameters on CT images: interobserver agreement in regard to identifying increases in the size of ground-glass opacities. Acad Radiol, 2012, 19(4): 389-394.
8.	Kim H, Park CM, Hwang EJ, et al. Pulmonary subsolid nodules: value of semi-automatic measurement in diagnostic accuracy, diagnostic reproducibility and nodule classification agreement. Eur Radiol, 2018, 28(5): 2124-2133.
9.	Hiramatsu M, Inagaki T, Inagaki T, et al. Pulmonary ground-glass opacity (GGO) lesions-large size and a history of lung cancer are risk factors for growth. J Thorac Oncol, 2008, 3(11): 1245-1250.
10.	de Hoop B, Gietema H, van de Vorst S, et al. Pulmonary ground-glass nodules: increase in mass as an early indicator of growth. Radiology, 2010, 255(1): 199-206.
11.	Kim H, Park CM, Woo S, et al. Pure and part-solid pulmonary ground-glass nodules: measurement variability of volume and mass in nodules with a solid portion less than or equal to 5 mm. Radiology, 2013, 269(2): 585-593.
12.	Song YS, Park CM, Park SJ, et al. Volume and mass doubling times of persistent pulmonary subsolid nodules detected in patients without known malignancy. Radiology, 2014, 273(1): 276-284.
13.	Scholten ET, de Jong PA, de Hoop B, et al. Towards a close computed tomography monitoring approach for screen detected subsolid pulmonary nodules? Eur Respir J, 2015, 45: 765-773.
14.	Lee JH, Park CM, Lee SM, et al. Persistent pulmonary subsolid nodules with solid portions of 5 mm or smaller: Their natural course and predictors of interval growth. Eur Radiol, 2016, 26(6): 1529-1537.
15.	Matsuguma H, Mori K, Nakahara R, et al. Characteristics of subsolid pulmonary nodules showing growth during follow-up with CT scanning. Chest, 2013, 143(2): 436-443.
16.	Kobayashi Y, Sakao Y, Deshpande GA, et al. The association between baseline clinical-radiological characteristics and growth of pulmonary nodules with ground-glass opacity. Lung Cancer, 2014, 83(1): 61-66.
17.	Chang B, Hwang JH, Choi YH, et al. Natural history of pure ground-glass opacity lung nodules detected by low-dose CT scan. Chest, 2013, 143(1): 172-178.
18.	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.
19.	Cho J, Kim ES, Kim SJ, et al. Long-term follow-up of small pulmonary ground-glass nodules stable for 3 years: implications of the proper follow-up period and risk factors for subsequent growth. J Thorac Oncol, 2016, 11(9): 1453-1459.
20.	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.
21.	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.
22.	Kakinuma R, Muramatsu Y, Kusumoto M, et al. Solitary pure ground-glass nodules 5 mm or smaller: frequency of growth. Radiology, 2015, 276(3): 873-882.
23.	Burt BM, Leung AN, Yanagawa M, et al. Diameter of solid tumor component alone should be tsed to establish T stage in lung adenocarcinoma. Ann Surg Oncol, 2015, 22 Suppl 3: S1318-S1323.
24.	Tsutani Y, Miyata Y, Yamanaka T, et al. Solid tumors versus mixed tumors with a ground-glass opacity component in patients with clinical stage ⅠA lung adenocarcinoma: prognostic comparison using high-resolution computed tomography findings. J Thorac Cardiovasc Surg, 2013, 146(1): 17-23.
25.	Tsutani Y, Miyata Y, Nakayama H, et al. Prognostic significance of using solid versus whole tumor size on high-resolution computed tomography for predicting pathologic malignant grade of tumors in clinical stage ⅠA lung adenocarcinoma: a multicenter study. J Thorac Cardiovasc Surg, 2012, 143(3): 607-612.
26.	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: 17229-17238.
27.	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.
28.	Kitami A, Kamio Y, Hayashi S, et al. One-dimensional mean computed tomography value evaluation of ground-glass opacity on high-resolution images. Gen Thorac Cardiovasc Surg, 2012, 60(7): 425-430.
29.	Tamura M, Shimizu Y, Yamamoto T, et al. Predictive value of one-dimensional mean computed tomography value of ground-glass opacity on high-resolution images for the possibility of future change. J Thorac Oncol, 2014, 9(4): 469-472.
30.	Yankeelov TE, Mankoff DA, Schwartz LH, et al. Quantitative imaging in cancer clinical trials. Clin Cancer Res, 2016, 22(2): 284-290.
31.	Lee G, Lee HY, Park H, et al. Radiomics and its emerging role in lung cancer research, imaging biomarkers and clinical management: State of the art. Eur J Radiol, 2017, 86: 297-307.
32.	Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology, 2016, 278(2): 563-577.
33.	Son JY, Lee HY, Kim JH, et al. Quantitative CT analysis of pulmonary ground-glass opacity nodules for distinguishing invasive adenocarcinoma from non-invasive or minimally invasive adenocarcinoma: the added value of using iodine mapping. Eur Radiol, 2016, 26(1): 43-54.
34.	Hwang IP, Park CM, Park SJ, et al. Persistent pure ground-glass nodules larger than 5 mm: differentiation of invasive pulmonary adenocarcinomas from preinvasive lesions or minimally invasive adenocarcinomas using texture analysis. Invest Radiol, 2015, 50(11): 798-804.
35.	Chae HD, Park CM, Park SJ, et al. Computerized texture analysis of persistent part-solid ground-glass nodules: differentiation of preinvasive lesions from invasive pulmonary adenocarcinomas. Radiology, 2014, 273(1): 285-293.
36.	Bak SH, Lee HY, Kim JH, et al. Quantitative CT scanning analysis of pure ground-glass opacity nodules predicts further CT scanning change. Chest, 2016, 149: 180-191.
37.	Dhillon SS. Solidifying our understanding of the natural history of subsolid pulmonary nodules-are we there yet? J Thorac Oncol, 2016, 11(7): 944-945.
38.	Silva M, Sverzellati N, Manna C, et al. Long-term surveillance of ground-glass nodules: evidence from the MILD trial. J Thorac Oncol, 2012, 7(10): 1541-1546.
39.	Eguchi T, Kondo R, Kawakami S, et al. Computed tomography attenuation predicts the growth of pure ground-glass nodules. Lung Cancer, 2014, 84(3): 242-247.
40.	Wu C, Zhao C, Yang Y, et al. High discrepancy of driver mutations in patients with NSCLC and synchronous multiple lung ground-glass nodules. J Thorac Oncol, 2015, 10(5): 778-783.
41.	Sato Y, Fujimoto D, Morimoto T, et al. Natural history and clinical characteristics of multiple pulmonary nodules with ground glass opacity. Respirology, 2017, 22(8): 1615-1621.
42.	Kim HS, Lee HJ, Jeon JH, et al. Natural history of ground-glass nodules detected on the chest computed tomography scan after major lung resection. Ann Thorac Surg, 2013, 96(6): 1952-1957.
43.	Kobayashi Y, Mitsudomi T, Sakao Y, et al. Genetic features of pulmonary adenocarcinoma presenting with ground-glass nodules: the differences between nodules with and without growth. Ann Oncol, 2015, 26(1): 156-161.
44.	Lambin P, Rios-Velazquez E, Leijenaar R, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer, 2012, 48(4): 441-446.
45.	Kumar V, Gu Y, Basu S, et al. Radiomics: the process and the challenges. Magn Reson Imaging, 2012, 30(9): 1234-1248.
46.	Gevaert O, Echegaray S, Khuong A, et al. Predictive radiogenomics modeling of EGFR mutation status in lung cancer. Sci Rep, 2017, 7: 41674.
47.	Wu W, Parmar C, Grossmann P, et al. Exploratory study to identify radiomics classifiers for lung cancer histology. Front Oncol, 2016, 6: 71.
48.	Pham TD, Watanabe Y, Higuchi M, et al. Texture analysis and synthesis of malignant and benign mediastinal lymph nodes in patients with lung cancer on computed tomography. Sci Rep, 2017, 7: 43209.
49.	Huynh E, Coroller TP, Narayan V, et al. CT-based radiomic analysis of stereotactic body radiation therapy patients with lung cancer. Radiother Oncol, 2016, 120(2): 258-266.

1. 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.
2. MacMahon H, Naidich DP, Goo JM, et al. Guidelines for management of incidental pulmonary nodules detected on CT images: From the fleischner society 2017. Radiology, 2017, 284(1): 228-243.
3. Baldwin DR, Callister ME, Guideline development group. The British Thoracic Society guidelines on the investigation and management of pulmonary nodules. Thorax, 2015, 70(8): 794-798.
4. Travis WD, Asamura H, Bankier AA, et al. The IASLC lung cancer staging project: proposals for coding T categories for subsolid nodules and assessment of tumor size in part-solid tumors in the forthcoming eighth edition of the TNM classification of lung cancer. J Thorac Oncol, 2016, 11(8): 1204-1223.
5. 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: 354-363.
6. Revel MP, Bissery A, Bienvenu M, et al. Are two-dimensional CT measurements of small noncalcified pulmonary nodules reliable? Radiology, 2004, 231(2): 453-458.
7. Kakinuma R, Ashizawa K, Kuriyama K, et al. Measurement of focal ground-glass opacity diameters on CT images: interobserver agreement in regard to identifying increases in the size of ground-glass opacities. Acad Radiol, 2012, 19(4): 389-394.
8. Kim H, Park CM, Hwang EJ, et al. Pulmonary subsolid nodules: value of semi-automatic measurement in diagnostic accuracy, diagnostic reproducibility and nodule classification agreement. Eur Radiol, 2018, 28(5): 2124-2133.
9. Hiramatsu M, Inagaki T, Inagaki T, et al. Pulmonary ground-glass opacity (GGO) lesions-large size and a history of lung cancer are risk factors for growth. J Thorac Oncol, 2008, 3(11): 1245-1250.
10. de Hoop B, Gietema H, van de Vorst S, et al. Pulmonary ground-glass nodules: increase in mass as an early indicator of growth. Radiology, 2010, 255(1): 199-206.
11. Kim H, Park CM, Woo S, et al. Pure and part-solid pulmonary ground-glass nodules: measurement variability of volume and mass in nodules with a solid portion less than or equal to 5 mm. Radiology, 2013, 269(2): 585-593.
12. Song YS, Park CM, Park SJ, et al. Volume and mass doubling times of persistent pulmonary subsolid nodules detected in patients without known malignancy. Radiology, 2014, 273(1): 276-284.
13. Scholten ET, de Jong PA, de Hoop B, et al. Towards a close computed tomography monitoring approach for screen detected subsolid pulmonary nodules? Eur Respir J, 2015, 45: 765-773.
14. Lee JH, Park CM, Lee SM, et al. Persistent pulmonary subsolid nodules with solid portions of 5 mm or smaller: Their natural course and predictors of interval growth. Eur Radiol, 2016, 26(6): 1529-1537.
15. Matsuguma H, Mori K, Nakahara R, et al. Characteristics of subsolid pulmonary nodules showing growth during follow-up with CT scanning. Chest, 2013, 143(2): 436-443.
16. Kobayashi Y, Sakao Y, Deshpande GA, et al. The association between baseline clinical-radiological characteristics and growth of pulmonary nodules with ground-glass opacity. Lung Cancer, 2014, 83(1): 61-66.
17. Chang B, Hwang JH, Choi YH, et al. Natural history of pure ground-glass opacity lung nodules detected by low-dose CT scan. Chest, 2013, 143(1): 172-178.
18. 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.
19. Cho J, Kim ES, Kim SJ, et al. Long-term follow-up of small pulmonary ground-glass nodules stable for 3 years: implications of the proper follow-up period and risk factors for subsequent growth. J Thorac Oncol, 2016, 11(9): 1453-1459.
20. 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.
21. 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.
22. Kakinuma R, Muramatsu Y, Kusumoto M, et al. Solitary pure ground-glass nodules 5 mm or smaller: frequency of growth. Radiology, 2015, 276(3): 873-882.
23. Burt BM, Leung AN, Yanagawa M, et al. Diameter of solid tumor component alone should be tsed to establish T stage in lung adenocarcinoma. Ann Surg Oncol, 2015, 22 Suppl 3: S1318-S1323.
24. Tsutani Y, Miyata Y, Yamanaka T, et al. Solid tumors versus mixed tumors with a ground-glass opacity component in patients with clinical stage ⅠA lung adenocarcinoma: prognostic comparison using high-resolution computed tomography findings. J Thorac Cardiovasc Surg, 2013, 146(1): 17-23.
25. Tsutani Y, Miyata Y, Nakayama H, et al. Prognostic significance of using solid versus whole tumor size on high-resolution computed tomography for predicting pathologic malignant grade of tumors in clinical stage ⅠA lung adenocarcinoma: a multicenter study. J Thorac Cardiovasc Surg, 2012, 143(3): 607-612.
26. 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: 17229-17238.
27. 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.
28. Kitami A, Kamio Y, Hayashi S, et al. One-dimensional mean computed tomography value evaluation of ground-glass opacity on high-resolution images. Gen Thorac Cardiovasc Surg, 2012, 60(7): 425-430.
29. Tamura M, Shimizu Y, Yamamoto T, et al. Predictive value of one-dimensional mean computed tomography value of ground-glass opacity on high-resolution images for the possibility of future change. J Thorac Oncol, 2014, 9(4): 469-472.
30. Yankeelov TE, Mankoff DA, Schwartz LH, et al. Quantitative imaging in cancer clinical trials. Clin Cancer Res, 2016, 22(2): 284-290.
31. Lee G, Lee HY, Park H, et al. Radiomics and its emerging role in lung cancer research, imaging biomarkers and clinical management: State of the art. Eur J Radiol, 2017, 86: 297-307.
32. Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology, 2016, 278(2): 563-577.
33. Son JY, Lee HY, Kim JH, et al. Quantitative CT analysis of pulmonary ground-glass opacity nodules for distinguishing invasive adenocarcinoma from non-invasive or minimally invasive adenocarcinoma: the added value of using iodine mapping. Eur Radiol, 2016, 26(1): 43-54.
34. Hwang IP, Park CM, Park SJ, et al. Persistent pure ground-glass nodules larger than 5 mm: differentiation of invasive pulmonary adenocarcinomas from preinvasive lesions or minimally invasive adenocarcinomas using texture analysis. Invest Radiol, 2015, 50(11): 798-804.
35. Chae HD, Park CM, Park SJ, et al. Computerized texture analysis of persistent part-solid ground-glass nodules: differentiation of preinvasive lesions from invasive pulmonary adenocarcinomas. Radiology, 2014, 273(1): 285-293.
36. Bak SH, Lee HY, Kim JH, et al. Quantitative CT scanning analysis of pure ground-glass opacity nodules predicts further CT scanning change. Chest, 2016, 149: 180-191.
37. Dhillon SS. Solidifying our understanding of the natural history of subsolid pulmonary nodules-are we there yet? J Thorac Oncol, 2016, 11(7): 944-945.
38. Silva M, Sverzellati N, Manna C, et al. Long-term surveillance of ground-glass nodules: evidence from the MILD trial. J Thorac Oncol, 2012, 7(10): 1541-1546.
39. Eguchi T, Kondo R, Kawakami S, et al. Computed tomography attenuation predicts the growth of pure ground-glass nodules. Lung Cancer, 2014, 84(3): 242-247.
40. Wu C, Zhao C, Yang Y, et al. High discrepancy of driver mutations in patients with NSCLC and synchronous multiple lung ground-glass nodules. J Thorac Oncol, 2015, 10(5): 778-783.
41. Sato Y, Fujimoto D, Morimoto T, et al. Natural history and clinical characteristics of multiple pulmonary nodules with ground glass opacity. Respirology, 2017, 22(8): 1615-1621.
42. Kim HS, Lee HJ, Jeon JH, et al. Natural history of ground-glass nodules detected on the chest computed tomography scan after major lung resection. Ann Thorac Surg, 2013, 96(6): 1952-1957.
43. Kobayashi Y, Mitsudomi T, Sakao Y, et al. Genetic features of pulmonary adenocarcinoma presenting with ground-glass nodules: the differences between nodules with and without growth. Ann Oncol, 2015, 26(1): 156-161.
44. Lambin P, Rios-Velazquez E, Leijenaar R, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer, 2012, 48(4): 441-446.
45. Kumar V, Gu Y, Basu S, et al. Radiomics: the process and the challenges. Magn Reson Imaging, 2012, 30(9): 1234-1248.
46. Gevaert O, Echegaray S, Khuong A, et al. Predictive radiogenomics modeling of EGFR mutation status in lung cancer. Sci Rep, 2017, 7: 41674.
47. Wu W, Parmar C, Grossmann P, et al. Exploratory study to identify radiomics classifiers for lung cancer histology. Front Oncol, 2016, 6: 71.
48. Pham TD, Watanabe Y, Higuchi M, et al. Texture analysis and synthesis of malignant and benign mediastinal lymph nodes in patients with lung cancer on computed tomography. Sci Rep, 2017, 7: 43209.
49. Huynh E, Coroller TP, Narayan V, et al. CT-based radiomic analysis of stereotactic body radiation therapy patients with lung cancer. Radiother Oncol, 2016, 120(2): 258-266.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

The advancements in natural growth history of pulmonary ground-glass nodules

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