Recommendations for the Management of Subsolid Pulmonary Nodules Detected at CT: A Statement from the Fleischner Society
Abstract
This report is to complement the original Fleischner Society recommendations for incidentally detected solid nodules by proposing a set of recommendations specifically aimed at subsolid nodules.
This report is to complement the original Fleischner Society recommendations for incidentally detected solid nodules by proposing a set of recommendations specifically aimed at subsolid nodules. The development of a standardized approach to the interpretation and management of subsolid nodules remains critically important given that peripheral adenocarcinomas represent the most common type of lung cancer, with evidence of increasing frequency. Following an initial consideration of appropriate terminology to describe subsolid nodules and a brief review of the new classification system for peripheral lung adenocarcinomas sponsored by the International Association for the Study of Lung Cancer (IASLC), American Thoracic Society (ATS), and European Respiratory Society (ERS), six specific recommendations were made, three with regard to solitary subsolid nodules and three with regard to multiple subsolid nodules. Each recommendation is followed first by the rationales underlying the recommendation and then by specific pertinent remarks. Finally, issues for which future research is needed are discussed. The recommendations are the result of careful review of the literature now available regarding subsolid nodules. Given the complexity of these lesions, the current recommendations are more varied than the original Fleischner Society guidelines for solid nodules. It cannot be overemphasized that these guidelines must be interpreted in light of an individual’s clinical history. Given the frequency with which subsolid nodules are encountered in daily clinical practice, and notwithstanding continuing controversy on many of these issues, it is anticipated that further refinements and modifications to these recommendations will be forthcoming as information continues to emerge from ongoing research.
© RSNA, 2012
References
- 1 . Guidelines for management of small pulmonary nodules detected on CT scans: a statement from the Fleischner Society. Radiology 2005;237(2):395–400.
- 2 . Compliance with Fleischner Society guidelines for management of small lung nodules: a survey of 834 radiologists. Radiology 2010;255(1):218–224.
- 3 . Compliance with Fleischner Society guidelines for management of lung nodules: lessons and opportunities. Radiology 2010;255(1):14–15.
- 4 . Subsolid pulmonary nodules and the spectrum of peripheral adenocarcinomas of the lung: recommended interim guidelines for assessment and management. Radiology 2009;253(3):606–622.
- 5 . Management of multiple pure ground-glass opacity lesions in patients with bronchioloalveolar carcinoma. J Thorac Oncol 2010;5(2):206–210.
- 6 . Management of ground-glass opacity lesions detected in patients with otherwise operable non–small cell lung cancer. J Thorac Oncol 2009;4(10):1242–1246.
- 7 . Management of small (3–5-mm) pulmonary nodules at chest CT: global survey of thoracic radiologists. Radiology 2008;247(3):847–853.
- 8 . Management of lung nodules detected by volume CT scanning. N Engl J Med 2009;361(23):2221–2229.
- 9 . Ground-glass nodules on chest CT as imaging biomarkers in the management of lung adenocarcinoma. AJR Am J Roentgenol 2011;196(3):533–543.
- 10 . Management of patients with small pulmonary nodules: a survey of radiologists, pulmonologists, and thoracic surgeons. AJR Am J Roentgenol 2006;187(1):143–148.
- 11 . Variation in experts’ beliefs about lung cancer growth, progression, and prognosis. J Thorac Oncol 2008;3(4):422–426.
- 12 . Cancer statistics, 2010. CA Cancer J Clin 2010;60(5):277–300.
- 13 . 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.
- 14 . The revised TNM staging system for lung cancer. Ann Thorac Cardiovasc Surg 2009;15(1):4–9.
- 15 . Implications of new (seventh) TNM classification of lung cancer on general radiologists: a pictorial review. Curr Probl Diagn Radiol 2011;40(2):85–93.
- 16 . Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med 2011;365(5):395–409.
- 17 . Fleischner Society: glossary of terms for thoracic imaging. Radiology 2008;246(3):697–722.
- 18 . Glossary of terms for CT of the lungs: recommendations of the nomenclature committee of the Fleischner Society. Radiology 1996;200(2):327–331.
- 19 . Persistent pulmonary nodular ground-glass opacity at thin-section CT: histopathologic comparisons. Radiology 2007;245(1):267–275.
- 20 . Treatment strategy for patients with small peripheral lung lesion(s): intermediate-term results of prospective study. Eur J Cardiothorac Surg 2008;34(5):1068–1074.
- 21 . CT findings and progression of small peripheral lung neoplasms having a replacement growth pattern. AJR Am J Roentgenol 2003;180(3):817–826.
- 22 . Limited resection trial for pulmonary ground-glass opacity nodules: fifty-case experience. J Thorac Cardiovasc Surg 2005;129(5):991–996.
- 23 . High-resolution CT analysis of small peripheral lung adenocarcinomas revealed on screening helical CT. AJR Am J Roentgenol 2001;176(6):1399–1407.
- 24 . Radiographic imaging of bronchioloalveolar carcinoma: screening, patterns of presentation and response assessment. J Thorac Oncol 2006;1(9 Suppl):S20–S26.
- 25 . A clinicopathological study of resected adenocarcinoma 2 cm or less in diameter. Ann Thorac Surg 2004;78(3):1011–1016.
- 26 . Curative wedge resection for non-invasive bronchioloalveolar carcinoma. Tohoku J Exp Med 2009;217(2):133–137.
- 27 . Prognostic value of bronchiolo-alveolar carcinoma component of small lung adenocarcinoma. Ann Thorac Surg 1999;68(6):2069–2073.
- 28 . Proportion of ground-glass opacity on high-resolution computed tomography in clinical T1 N0 M0 adenocarcinoma of the lung: a predictor of lymph node metastasis. J Thorac Cardiovasc Surg 2002;124(2):278–284.
- 29 . One-dimensional quantitative evaluation of peripheral lung adenocarcinoma with or without ground-glass opacity on thin-section CT images using profile curves. Br J Radiol 2009;82(979):532–540.
- 30 . Automated assessment of malignant degree of small peripheral adenocarcinomas using volumetric CT data: correlation with pathologic prognostic factors. Lung Cancer 2010;70(3):286–294.
- 31 . The proportion of consolidation to ground-glass opacity on high resolution CT is a good predictor for distinguishing the population of non-invasive peripheral adenocarcinoma. Lung Cancer 2003;42(3):303–310.
- 32 . The new IASLC/ATS/ERS international multidisciplinary lung adenocarcinoma classification [abstr]. J Thorac Oncol 2009;4(9):S86–S89.
- 33 . A grading system of lung adenocarcinomas based on histologic pattern is predictive of disease recurrence in stage I tumors. Am J Surg Pathol 2010;34(8):1155–1162.
- 34 . Small adenocarcinoma of the lung: histologic characteristics and prognosis. Cancer 1995;75(12):2844–2852.
- 35 . 5-year lung cancer screening experience: growth curves of 18 lung cancers compared to histologic type, CT attenuation, stage, survival, and size. Chest 2009;136(6):1586–1595.
- 36 . Grading strength of recommendations and quality of evidence in clinical guidelines: report from an American College of Chest Physicians task force. Chest 2006;129(1):174–181.
- 37 . Clinicopathologic analysis of multiple (five or more) atypical adenomatous hyperplasias (AAHs) of the lung: evidence for the AAH-adenocarcinoma sequence. J Thorac Oncol 2010;5(4):466–471.
- 38 . Stepwise evolution from a focal pure pulmonary ground-glass opacity nodule into an invasive lung adenocarcinoma: an observation for more than 10 years. Lung Cancer 2010;69(1):123–126.
- 39 . Management of the peripheral small ground-glass opacities. Thorac Surg Clin 2007;17(2):191–201, viii.
- 40 . Growth rate of small lung cancers detected on mass CT screening. Br J Radiol 2000;73(876):1252–1259.
- 41 . Overdiagnosis in cancer. J Natl Cancer Inst 2010;102(9): 605–613.
- 42 . Persistent pure ground-glass nodules in the lung: interscan variability of semiautomated volume and attenuation measurements. AJR Am J Roentgenol 2010;195(6):W408–W414.
- 43 . Evaluation of reader variability in the interpretation of follow-up CT scans at lung cancer screening. Radiology 2011;259(1):263–270.
- 44 . Radiation risk from medical imaging. Mayo Clin Proc 2010;85(12):1142–1146; quiz 1146.
- 45 . Nodular ground-glass opacity at thin-section CT: histologic correlation and evaluation of change at follow-up. RadioGraphics 2007;27(2):391–408.
- 46 . Ground-glass nodules found in two patients with malignant melanomas: different growth rate and different histology. Clin Imaging 2010;34(5):396–399.
- 47 . Pulmonary nodular ground-glass opacities in patients with extrapulmonary cancers: what is their clinical significance and how can we determine whether they are malignant or benign lesions? Chest 2008;133(6):1402–1409.
- 48 . Natural history of pure ground-glass opacity after long-term follow-up of more than 2 years. Ann Thorac Surg 2002;73(2):386–392; discussion 392–393.
- 49 . Computer-aided volumetry of pulmonary nodules exhibiting ground-glass opacity at MDCT. AJR Am J Roentgenol 2010;194(2):398–406.
- 50 . Ground-glass opacities on thin-section helical CT: differentiation between bronchioloalveolar carcinoma and atypical adenomatous hyperplasia. AJR Am J Roentgenol 2008;190(5):1363–1368.
- 51 . Ground-glass centrilobular nodules on multidetector CT scan: incidental diagnosis in a patient with pneumonia. Chest 2010;138(2):427–433.
- 52 . Focal ground-glass opacity detected by low-dose helical CT. Chest 2002;121:1464–1467.
- 53 . 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.
- 54 . Evaluation of lesions corresponding to ground-glass opacities that were resected after computed tomography follow-up examination. Lung Cancer 2009;65(2):176–179.
- 55 . CT screening for lung cancer: past and ongoing studies. Semin Thorac Cardiovasc Surg 2005;17(2):99–106.
- 56 . CT screening for lung cancer: five-year prospective experience. Radiology 2005;235(1):259–265.
- 57 . Antibiotic use in the management of pulmonary nodules. Chest 2010;137(2):369–375.
- 58 . Detection of nodules showing ground-glass opacity in the lungs at low-dose multidetector computed tomography: phantom and clinical study. J Comput Assist Tomogr 2009;33(1):49–53.
- 59 . Linear and volume measurements of pulmonary nodules at different CT dose levels: intrascan and interscan analysis. Rofo 2009;181(1):24–31.
- 60 . Limitations of dual time point PET in the assessment of lung nodules with low FDG avidity. Lung Cancer 2010;68(1):66–71.
- 61 . Tumor fluoro-2-deoxy-D-glucose avidity on positron emission tomographic scan predicts mortality in patients with early-stage pure and mixed bronchioloalveolar carcinoma. J Thorac Cardiovasc Surg 2006;132(5):1189–1195.
- 62 . PET imaging in patients with bronchioloalveolar cell carcinoma. Lung Cancer 2002;38(3):261–266.
- 63 . FDG PET measurement of the proliferative potential of non–small cell lung cancer. J Nucl Med 2000;41(1):85–92.
- 64 . Mucinous versus nonmucinous solitary pulmonary nodular bronchioloalveolar carcinoma: CT and FDG PET findings and pathologic comparisons. Lung Cancer 2009;65(2):170–175.
- 65 . The maximum standardized uptake values on positron emission tomography to predict the Noguchi classification and invasiveness in clinical stage IA adenocarcinoma measuring 2 cm or less in size. Interact Cardiovasc Thorac Surg 2009;9(1):70–73.
- 66 . Positron emission tomography in relation to Noguchi’s classification for diagnosis of peripheral non–small-cell lung cancer 2 cm or less in size. World J Surg 2007;31(2):314–317.
- 67 . 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.
- 68 . FDG-PET imaging in lung cancer: how sensitive is it for bronchioloalveolar carcinoma? Eur J Nucl Med Mol Imaging 2002;29(9):1166–1173.
- 69 . Expert opinion: role of percutaneous biopsy of part-solid nodules in the IASLC/ATS/ERS international multidisciplinary classification of lung adenocarcinoma. J Thorac Imaging 2011;26(3):189.
- 70 . Percutaneous CT-guided fine needle aspiration for lung cancer smaller than 2 cm and revealed by ground-glass opacity at CT. Lung Cancer 2006;51(2):173–179.
- 71 . CT screening for lung cancer: implication of lung biopsy recommendations. AJR Am J Roentgenol 2012;198(2):351–358.
- 72 . Diagnostic accuracy of CT-guided core biopsy of ground-glass opacity pulmonary lesions. AJR Am J Roentgenol 2008;190(1):234–239.
- 73 . Nodular ground-glass opacities on thin-section CT: size change during follow-up and pathological results. Korean J Radiol 2007;8(1):22–31.
- 74 . CT screening for lung cancer: frequency and significance of part-solid and nonsolid nodules. AJR Am J Roentgenol 2002;178(5):1053–1057.
- 75 . Efficacy of thoracoscopic resection for multifocal bronchioloalveolar carcinoma showing pure ground-glass opacities of 20 mm or less in diameter. J Thorac Cardiovasc Surg 2007;134(4):877–882.
- 76 . Differential diagnosis of ground-glass opacity nodules: CT number analysis by three-dimensional computerized quantification. Chest 2007;132(3):984–990.
- 77 . Transient part-solid nodules detected at screening thin-section CT for lung cancer: comparison with persistent part-solid nodules. Radiology 2010;255(1):242–251.
- 78 . Distribution of stage I lung cancer growth rates determined with serial volumetric CT measurements. Radiology 2006;241(2):554–563.
- 79 . Objective radiologic analysis of ground-glass opacity aimed at curative limited resection for small peripheral non–small cell lung cancer. J Thorac Cardiovasc Surg 2005;129(6):1226–1231.
- 80 . Peripheral lung adenocarcinoma: correlation of thin-section CT findings with histologic prognostic factors and survival. Radiology 2001;220(3):803–809.
- 81 . Quantification of ground-glass opacity on high-resolution CT of small peripheral adenocarcinoma of the lung: pathologic and prognostic implications. AJR Am J Roentgenol 2001;177(6):1417–1422.
- 82 . Non-BAC component but not epidermal growth factor receptor gene mutation is associated with poor outcomes in small adenocarcinoma of the lung. J Thorac Oncol 2008;3(7):704–710.
- 83 . Solitary and multiple resected adenocarcinomas after CT screening for lung cancer: histopathologic features and their prognostic implications. Lung Cancer 2009;64(2):148–154.
- 84 . Pulmonary ground-glass nodules: increase in mass as an early indicator of growth. Radiology 2010;255(1):199–206.
- 85 . Lung tumor growth: assessment with CT—comparison of diameter and cross-sectional area with volume measurements. Radiology 2004;231(3):866–871.
- 86 . Five-year lung cancer screening experience: CT appearance, growth rate, location, and histologic features of 61 lung cancers. Radiology 2007;242(2):555–562.
- 87 . Pulmonary nodules: volume repeatability at multidetector CT lung cancer screening. Radiology 2009;251(3):919–925.
- 88 . Discrepancy of computed tomographic image between lung and mediastinal windows as a prognostic implication in small lung adenocarcinoma. Ann Thorac Surg 2003;76(6):1828–1832; discussion 1832.
- 89 . Pulmonary adenocarcinomas with ground-glass attenuation on thin-section CT: quantification by three-dimensional image analyzing method. Eur J Radiol 2008;65(1):104–111.
- 90 . Zone of transition: a potential source of error in tumor volume estimation. Radiology 2010;256(2):633–639.
- 91 . Evaluating variability in tumor measurements from same-day repeat CT scans of patients with non–small cell lung cancer. Radiology 2009;252(1):263–272.
- 92 . Performance evaluation of 4 measuring methods of ground-glass opacities for predicting the 5-year relapse-free survival of patients with peripheral nonsmall cell lung cancer: a multicenter study. J Comput Assist Tomogr 2008;32(5):792–798.
- 93 . Pulmonary nodules: growth rate assessment in patients by using serial CT and three-dimensional volumetry. Radiology 2012;262(2):662–671.
- 94 . The variation of prognostic significance of maximum standardized uptake value of [18F]-fluoro-2-deoxy-glucose positron emission tomography in different histological subtypes and pathological stages of surgically resected non–small cell lung carcinoma. Lung Cancer 2010;69(2):187–193.
- 95 . Combined evaluation of preoperative FDG uptake on PET, ground-glass opacity area on CT, and serum CEA level: identification of both low and high risk of recurrence in patients with resected T1 lung adenocarcinoma. Eur J Nucl Med Mol Imaging 2009;36(3):373–381.
- 96 . Lung adenocarcinoma as a solitary pulmonary nodule: prognostic determinants of CT, PET, and histopathologic findings. Lung Cancer 2009;66(3):379–385.
- 97 ;
Veterans Affairs Solitary Nodule Accuracy Project Cooperative Studies Group . PET scan 18F-fluorodeoxyglucose uptake and prognosis in patients with resected clinical stage IA non–small cell lung cancer. Chest 2010;137(5):1150–1156. - 98 . Associations among bronchioloalveolar carcinoma components, positron emission tomographic and computed tomographic findings, and malignant behavior in small lung adenocarcinomas. J Thorac Cardiovasc Surg 2007;133(6):1448–1454.
- 99 . Fluorodeoxyglucose uptake measured by positron emission tomography and standardized uptake value predicts long-term survival of CT screening detected lung cancer in heavy smokers. J Thorac Oncol 2009;4(11):1352–1356.
- 100 . [F-18]Fluorodeoxyglucose positron emission tomography can predict pathological tumor stage and proliferative activity determined by Ki-67 in clinical stage IA lung adenocarcinomas. Jpn J Clin Oncol 2006;36(7):403–409.
- 101 . Safe and effective minimally invasive approaches for small ground glass opacity. Ann Thorac Surg 2010;89(6):S2114–S2117.
- 102 . Limited resection for noninvasive bronchioloalveolar carcinoma diagnosed by intraoperative pathologic examination. Ann Thorac Surg 2009;88(4):1106–1111.
- 103 . Minimally invasive approach to early, peripheral adenocarcinoma with ground-glass opacity appearance. Ann Thorac Surg 2008;85(2):S701–S704.
- 104 . Comprehensive histologic assessment helps to differentiate multiple lung primary nonsmall cell carcinomas from metastases. Am J Surg Pathol 2009;33(12):1752–1764.
- 105 . Surgical treatments for multiple primary adenocarcinoma of the lung. Ann Thorac Surg 2004;78(4):1194–1199.
- 106 . Multicentric adenocarcinoma of the lung: CT-pathologic correlation. Radiology 1990;176(1):185–190.
- 107 . Predictors of outcomes after surgical treatment of synchronous primary lung cancers. J Thorac Oncol 2010;5(2):197–205.
- 108 . Surgical resection of multifocal non-small cell lung cancer is associated with prolonged survival. Ann Thorac Surg 2002;74(4):988–993; discussion 993–994.
- 109 . Resection of multifocal non–small cell lung cancer when the bronchioloalveolar subtype is involved. J Thorac Cardiovasc Surg 2003;126(5):1597–1602.
- 110 . Are there imaging characteristics associated with epidermal growth factor receptor and KRAS mutations in patients with adenocarcinoma of the lung with bronchioloalveolar features? J Thorac Oncol 2010;5(3):344–348.
- 111 . Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol 2011;24(5):653–664.
- 112 . 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.
- 113 . Comparison of pathologic findings of baseline and annual repeat cancers diagnosed on CT screening. Lung Cancer 2007;56(2):193–199.
Article History
Received April 12, 2012; revision requested May 21; revision received August 15; accepted August 23; final version accepted August 27.Published online: Jan 2013
Published in print: Jan 2013