Current status and advancement of medical imaging management for multiple pulmonary nodules_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WU Qiang ^1,2 , ZHANG Boyou ^1,2 , SUN Fei ² ,  SHI Hongcan ²

1. Department of Thoracic Surgery, The Second Xiangya Hospital of Central South University, Changsha, 410011, P.R.China;
2. Department of Cardiothoracic Surgery, Clinical Medical College of Yangzhou University, Center of Translational Medicine, Yangzhou University, Key Laboratory of Integrative Medicine in Geriatrics Control of Jiangsu Province, Yangzhou University, Yangzhou, 225001, Jiangsu, P.R.China;

Corresponding author：

SHI Hongcan, Email: shihongcan@yzu.edu.cn

Keywords：

Multiple pulmonary nodules; pulmonary neoplasms; low-dose computed tomography; positron emission tomography-computed tomography; multidisciplinary consultation; review

DOI：

10.7507/1007-4848.202005083

Video：

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Abstract Full text Figures/Tables Video References Cited by

The widespread use of low-dose computed tomography (LDCT) in lung cancer screening has enabled more and more lung nodules to get identified of which more than 20% are multiple pulmonary nodules. At present, there is no guideline or consensus for multiple pulmonary nodules whose management is based primarily on the pulmonary imaging characteristics and associated risk factors. Herein, this review covers the imaging methods, CT appearances and management of multiple pulmonary nodules.

Citation： WU Qiang, ZHANG Boyou, SUN Fei, SHI Hongcan. Current status and advancement of medical imaging management for multiple pulmonary nodules. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2021, 28(3): 363-367. doi: 10.7507/1007-4848.202005083 Copy

1.	赵俊松, 崔利, 何江波, 等. 上海22351例无症状体检者低剂量CT肺癌筛查及随访结果初步分析. 诊断学理论与实践, 2019, 18(2): 183-188.
2.	Church TR, Black WC, Aberle DR, et al. Results of initial low-dose computed tomographic screening for lung cancer. N Engl J Med, 2013, 368(21): 1980-1991.
3.	李为希, 周洁, 张芬, 等. 低剂量螺旋CT对高危人群的肺癌筛查结果分析. 中国肿瘤, 2019, 28(12): 896-900.
4.	Lopes Pegna A, Picozzi G, Falaschi F, et al. Four-year results of low-dose CT screening and nodule management in the ITALUNG trial. J Thorac Oncol, 2013, 8(7): 866-875.
5.	He YT, Zhang YC, Shi GF, et al. Risk factors for pulmonary nodules in north China: A prospective cohort study. Lung Cancer, 2018, 120: 122-129.
6.	Sihoe ADL, Petersen RH, Cardillo G. Multiple pulmonary ground glass opacities: is it time for new guidelines? J Thorac Dis, 2018, 10(11): 5970-5973.
7.	Trinidad López C, Delgado Sánchez-Gracián C, Utrera Pérez E, et al. Incidental pulmonary nodules: characterization and management. Radiologia, 2019, 61(5): 357-369.
8.	中华医学会呼吸病学分会肺癌学组, 中国肺癌防治联盟专家组. 肺结节诊治中国专家共识(2018年版). 中华结核和呼吸杂志, 2018, 41(10): 763-771.
9.	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.
10.	van Riel SJ, Ciompi F, Jacobs C, et al. Malignancy risk estimation of screen-detected nodules at baseline CT: comparison of the PanCan model, Lung-RADS and NCCN guidelines. Eur Radiol, 2017, 27(10): 4019-4029.
11.	Ren Y, Huang S, Dai C, et al. Germline predisposition and copy number alteration in pre-stage lung adenocarcinomas presenting as ground-glass nodules. Front Oncol, 2019, 9: 288.
12.	Li X, Hu B, Li H, et al. Application of artificial intelligence in the diagnosis of multiple primary lung cancer. Thorac Cancer, 2019, 10(11): 2168-2174.
13.	中国肺癌防治联盟, 中华医学会呼吸病学分会肺癌学组, 中国医师协会呼吸医师分会肺癌工作委员会. 肺癌筛查与管理中国专家共识. 国际呼吸杂志, 2019, 39(21): 1604-1615.
14.	Garcia-Velloso MJ, Bastarrika G, de-Torres JP, et al. Assessment of indeterminate pulmonary nodules detected in lung cancer screening: Diagnostic accuracy of FDG PET/CT. Lung Cancer, 2016, 97: 81-86.
15.	Chun EJ, Lee HJ, Kang WJ, et al. Differentiation between malignancy and inflammation in pulmonary ground-glass nodules: The feasibility of integrated (18)F-FDG PET/CT. Lung Cancer, 2009, 65(2): 180-186.
16.	Taralli S, Scolozzi V, Foti M, et al. (18)F-FDG PET/CT diagnostic performance in solitary and multiple pulmonary nodules detected in patients with previous cancer history: reports of 182 nodules. Eur J Nucl Med Mol Imaging, 2019, 46(2): 429-436.
17.	Messerli M, Kluckert T, Knitel M, et al. Ultralow dose CT for pulmonary nodule detection with chest x-ray equivalent dose — a prospective intra-individual comparative study. Eur Radiol, 2017, 27(8): 3290-3299.
18.	Dewes P, Frellesen C, Al-Butmeh F, et al. Comparative evaluation of non-contrast CAIPIRINHA-VIBE 3T-MRI and multidetector CT for detection of pulmonary nodules: In vivo evaluation of diagnostic accuracy and image quality. Eur J Radiol, 2016, 85(1): 193-198.
19.	Huber A, Landau J, Ebner L, et al. Performance of ultralow-dose CT with iterative reconstruction in lung cancer screening: limiting radiation exposure to the equivalent of conventional chest X-ray imaging. Eur Radiol, 2016, 26(10): 3643-3652.
20.	Ludwig M, Chipon E, Cohen J, et al. Detection of pulmonary nodules: a clinical study protocol to compare ultra-low dose chest CT and standard low-dose CT using ASIR-V. BMJ Open, 2019, 9(8): e025661.
21.	Larici AR, Farchione A, Franchi P, et al. Lung nodules: size still matters. Eur Respir Rev, 2017, 26(146): 170025.
22.	周清华, 范亚光, 王颖, 等. 中国肺癌低剂量螺旋CT筛查指南(2018年版). 中国肺癌杂志, 2018, 21(2): 67-75.
23.	Ettinger DS, Wood DE, Aisner DL, et al. Non-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2017, 15(4): 504-535.
24.	Horeweg N, van Rosmalen J, Heuvelmans MA, et al. Lung cancer probability in patients with CT-detected pulmonary nodules: a prespecified analysis of data from the NELSON trial of low-dose CT screening. Lancet Oncol, 2014, 15(12): 1332-1341.
25.	Missrie I, Hochhegger B, Zanon M, et al. Small low-risk pulmonary nodules on chest digital radiography: can we predict whether the nodule is benign? Clin Radiol, 2018, 73(10): 902-906.
26.	Heuvelmans MA, Walter JE, Vliegenthart R, et al. Disagreement of diameter and volume measurements for pulmonary nodule size estimation in CT lung cancer screening. Thorax, 2018, 73(8): 779-781.
27.	Koslow M, Young JR, Yi ES, et al. Rheumatoid pulmonary nodules: clinical and imaging features compared with malignancy. Eur Radiol, 2019, 29(4): 1684-1692.
28.	Liu Y, Wang H, Li Q, et al. Radiologic features of small pulmonary nodules and lung cancer risk in the national lung screening trial: A nested case-control study. Radiology, 2018, 286(1): 298-306.
29.	Webb WR, Higgins CB. Thoracic imaging: pulmonary and cardiovascular radiology. Third edition. Philadelphia: Wolters Kluwer, 2016. 952-1065.
30.	Walter JE, Heuvelmans MA, Ten Haaf K, et al. Persisting new nodules in incidence rounds of the NELSON CT lung cancer screening study. Thorax, 2019, 74(3): 247-253.
31.	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.
32.	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.
33.	Revel MP, Mannes I, Benzakoun J, et al. Subsolid lung nodule classification: A CT criterion for improving interobserver agreement. Radiology, 2018, 286(1): 316-325.
34.	Heuvelmans MA, Walter JE, Peters RB, et al. Relationship between nodule count and lung cancer probability in baseline CT lung cancer screening: The NELSON study. Lung Cancer, 2017, 113: 45-50.
35.	Walter JE, Heuvelmans MA, de Bock GH, et al. Relationship between the number of new nodules and lung cancer probability in incidence screening rounds of CT lung cancer screening: The NELSON study. Lung Cancer, 2018, 125: 103-108.
36.	Slatore CG, Wiener RS. Pulmonary nodules: A small problem for many, severe distress for some, and how to communicate about it. Chest, 2018, 153(4): 1004-1015.
37.	Walter JE, Heuvelmans MA, Bock GH, et al. Characteristics of new solid nodules detected in incidence screening rounds of low-dose CT lung cancer screening: the NELSON study. Thorax, 2018, 73(8): 741-747.
38.	Karki A, Shah R, Fein A. Multiple pulmonary nodules in malignancy. Curr Opin Pulm Med, 2017, 23(4): 285-289.
39.	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.
40.	Hattori A, Matsunaga T, Takamochi K, et al. Surgical management of multifocal ground-glass opacities of the lung: Correlation of clinicopathologic and radiologic findings. Thorac Cardiovasc Surg, 2017, 65(2): 142-149.
41.	Marcus MW, Duffy SW, Devaraj A, et al. Probability of cancer in lung nodules using sequential volumetric screening up to 12 months: the UKLS trial. Thorax, 2019, 74(8): 761-767.
42.	Winter A, Aberle DR, Hsu W. External validation and recalibration of the Brock model to predict probability of cancer in pulmonary nodules using NLST data. Thorax, 2019, 74(6): 551-563.
43.	Tanner NT, Porter A, Gould MK, et al. Physician assessment of pretest probability of malignancy and adherence with guidelines for pulmonary nodule evaluation. Chest, 2017, 152(2): 263-270.
44.	Silvestri GA, Tanner NT, Kearney P, et al. Assessment of plasma proteomics biomarker's ability to distinguish benign from malignant lung nodules: Results of the PANOPTIC (Pulmonary Nodule Plasma Proteomic Classifier) Trial. Chest, 2018, 154(3): 491-500.
45.	Ather S, Kadir T, Gleeson F. Artificial intelligence and radiomics in pulmonary nodule management: current status and future applications. Clin Radiol, 2020, 75(1): 13-19.

1. 赵俊松, 崔利, 何江波, 等. 上海22351例无症状体检者低剂量CT肺癌筛查及随访结果初步分析. 诊断学理论与实践, 2019, 18(2): 183-188.
2. Church TR, Black WC, Aberle DR, et al. Results of initial low-dose computed tomographic screening for lung cancer. N Engl J Med, 2013, 368(21): 1980-1991.
3. 李为希, 周洁, 张芬, 等. 低剂量螺旋CT对高危人群的肺癌筛查结果分析. 中国肿瘤, 2019, 28(12): 896-900.
4. Lopes Pegna A, Picozzi G, Falaschi F, et al. Four-year results of low-dose CT screening and nodule management in the ITALUNG trial. J Thorac Oncol, 2013, 8(7): 866-875.
5. He YT, Zhang YC, Shi GF, et al. Risk factors for pulmonary nodules in north China: A prospective cohort study. Lung Cancer, 2018, 120: 122-129.
6. Sihoe ADL, Petersen RH, Cardillo G. Multiple pulmonary ground glass opacities: is it time for new guidelines? J Thorac Dis, 2018, 10(11): 5970-5973.
7. Trinidad López C, Delgado Sánchez-Gracián C, Utrera Pérez E, et al. Incidental pulmonary nodules: characterization and management. Radiologia, 2019, 61(5): 357-369.
8. 中华医学会呼吸病学分会肺癌学组, 中国肺癌防治联盟专家组. 肺结节诊治中国专家共识(2018年版). 中华结核和呼吸杂志, 2018, 41(10): 763-771.
9. 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.
10. van Riel SJ, Ciompi F, Jacobs C, et al. Malignancy risk estimation of screen-detected nodules at baseline CT: comparison of the PanCan model, Lung-RADS and NCCN guidelines. Eur Radiol, 2017, 27(10): 4019-4029.
11. Ren Y, Huang S, Dai C, et al. Germline predisposition and copy number alteration in pre-stage lung adenocarcinomas presenting as ground-glass nodules. Front Oncol, 2019, 9: 288.
12. Li X, Hu B, Li H, et al. Application of artificial intelligence in the diagnosis of multiple primary lung cancer. Thorac Cancer, 2019, 10(11): 2168-2174.
13. 中国肺癌防治联盟, 中华医学会呼吸病学分会肺癌学组, 中国医师协会呼吸医师分会肺癌工作委员会. 肺癌筛查与管理中国专家共识. 国际呼吸杂志, 2019, 39(21): 1604-1615.
14. Garcia-Velloso MJ, Bastarrika G, de-Torres JP, et al. Assessment of indeterminate pulmonary nodules detected in lung cancer screening: Diagnostic accuracy of FDG PET/CT. Lung Cancer, 2016, 97: 81-86.
15. Chun EJ, Lee HJ, Kang WJ, et al. Differentiation between malignancy and inflammation in pulmonary ground-glass nodules: The feasibility of integrated (18)F-FDG PET/CT. Lung Cancer, 2009, 65(2): 180-186.
16. Taralli S, Scolozzi V, Foti M, et al. (18)F-FDG PET/CT diagnostic performance in solitary and multiple pulmonary nodules detected in patients with previous cancer history: reports of 182 nodules. Eur J Nucl Med Mol Imaging, 2019, 46(2): 429-436.
17. Messerli M, Kluckert T, Knitel M, et al. Ultralow dose CT for pulmonary nodule detection with chest x-ray equivalent dose — a prospective intra-individual comparative study. Eur Radiol, 2017, 27(8): 3290-3299.
18. Dewes P, Frellesen C, Al-Butmeh F, et al. Comparative evaluation of non-contrast CAIPIRINHA-VIBE 3T-MRI and multidetector CT for detection of pulmonary nodules: In vivo evaluation of diagnostic accuracy and image quality. Eur J Radiol, 2016, 85(1): 193-198.
19. Huber A, Landau J, Ebner L, et al. Performance of ultralow-dose CT with iterative reconstruction in lung cancer screening: limiting radiation exposure to the equivalent of conventional chest X-ray imaging. Eur Radiol, 2016, 26(10): 3643-3652.
20. Ludwig M, Chipon E, Cohen J, et al. Detection of pulmonary nodules: a clinical study protocol to compare ultra-low dose chest CT and standard low-dose CT using ASIR-V. BMJ Open, 2019, 9(8): e025661.
21. Larici AR, Farchione A, Franchi P, et al. Lung nodules: size still matters. Eur Respir Rev, 2017, 26(146): 170025.
22. 周清华, 范亚光, 王颖, 等. 中国肺癌低剂量螺旋CT筛查指南(2018年版). 中国肺癌杂志, 2018, 21(2): 67-75.
23. Ettinger DS, Wood DE, Aisner DL, et al. Non-small cell lung cancer, version 5.2017, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw, 2017, 15(4): 504-535.
24. Horeweg N, van Rosmalen J, Heuvelmans MA, et al. Lung cancer probability in patients with CT-detected pulmonary nodules: a prespecified analysis of data from the NELSON trial of low-dose CT screening. Lancet Oncol, 2014, 15(12): 1332-1341.
25. Missrie I, Hochhegger B, Zanon M, et al. Small low-risk pulmonary nodules on chest digital radiography: can we predict whether the nodule is benign? Clin Radiol, 2018, 73(10): 902-906.
26. Heuvelmans MA, Walter JE, Vliegenthart R, et al. Disagreement of diameter and volume measurements for pulmonary nodule size estimation in CT lung cancer screening. Thorax, 2018, 73(8): 779-781.
27. Koslow M, Young JR, Yi ES, et al. Rheumatoid pulmonary nodules: clinical and imaging features compared with malignancy. Eur Radiol, 2019, 29(4): 1684-1692.
28. Liu Y, Wang H, Li Q, et al. Radiologic features of small pulmonary nodules and lung cancer risk in the national lung screening trial: A nested case-control study. Radiology, 2018, 286(1): 298-306.
29. Webb WR, Higgins CB. Thoracic imaging: pulmonary and cardiovascular radiology. Third edition. Philadelphia: Wolters Kluwer, 2016. 952-1065.
30. Walter JE, Heuvelmans MA, Ten Haaf K, et al. Persisting new nodules in incidence rounds of the NELSON CT lung cancer screening study. Thorax, 2019, 74(3): 247-253.
31. 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.
32. 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.
33. Revel MP, Mannes I, Benzakoun J, et al. Subsolid lung nodule classification: A CT criterion for improving interobserver agreement. Radiology, 2018, 286(1): 316-325.
34. Heuvelmans MA, Walter JE, Peters RB, et al. Relationship between nodule count and lung cancer probability in baseline CT lung cancer screening: The NELSON study. Lung Cancer, 2017, 113: 45-50.
35. Walter JE, Heuvelmans MA, de Bock GH, et al. Relationship between the number of new nodules and lung cancer probability in incidence screening rounds of CT lung cancer screening: The NELSON study. Lung Cancer, 2018, 125: 103-108.
36. Slatore CG, Wiener RS. Pulmonary nodules: A small problem for many, severe distress for some, and how to communicate about it. Chest, 2018, 153(4): 1004-1015.
37. Walter JE, Heuvelmans MA, Bock GH, et al. Characteristics of new solid nodules detected in incidence screening rounds of low-dose CT lung cancer screening: the NELSON study. Thorax, 2018, 73(8): 741-747.
38. Karki A, Shah R, Fein A. Multiple pulmonary nodules in malignancy. Curr Opin Pulm Med, 2017, 23(4): 285-289.
39. 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.
40. Hattori A, Matsunaga T, Takamochi K, et al. Surgical management of multifocal ground-glass opacities of the lung: Correlation of clinicopathologic and radiologic findings. Thorac Cardiovasc Surg, 2017, 65(2): 142-149.
41. Marcus MW, Duffy SW, Devaraj A, et al. Probability of cancer in lung nodules using sequential volumetric screening up to 12 months: the UKLS trial. Thorax, 2019, 74(8): 761-767.
42. Winter A, Aberle DR, Hsu W. External validation and recalibration of the Brock model to predict probability of cancer in pulmonary nodules using NLST data. Thorax, 2019, 74(6): 551-563.
43. Tanner NT, Porter A, Gould MK, et al. Physician assessment of pretest probability of malignancy and adherence with guidelines for pulmonary nodule evaluation. Chest, 2017, 152(2): 263-270.
44. Silvestri GA, Tanner NT, Kearney P, et al. Assessment of plasma proteomics biomarker's ability to distinguish benign from malignant lung nodules: Results of the PANOPTIC (Pulmonary Nodule Plasma Proteomic Classifier) Trial. Chest, 2018, 154(3): 491-500.
45. Ather S, Kadir T, Gleeson F. Artificial intelligence and radiomics in pulmonary nodule management: current status and future applications. Clin Radiol, 2020, 75(1): 13-19.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Current status and advancement of medical imaging management for multiple pulmonary nodules

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