European Radiology

, Volume 27, Issue 10, pp 4037–4043 | Cite as

CT and histopathologic characteristics of lung adenocarcinoma with pure ground-glass nodules 10 mm or less in diameter

  • Fang Wu
  • Shu-ping Tian
  • Xin Jin
  • Rui Jing
  • Yue-qing Yang
  • Mei Jin
  • Shao-hong ZhaoEmail author



To evaluate CT and histopathologic features of lung adenocarcinoma with pure ground-glass nodule (pGGN) ≤10 mm in diameter.


CT appearances of 148 patients (150 lesions) who underwent curative resection of lung adenocarcinoma with pGGN ≤10 mm (25 atypical adenomatous hyperplasias, 42 adenocarcinoma in situs, 38 minimally invasive adenocarcinomas, and 45 invasive pulmonary adenocarcinomas) were analyzed for lesion size, density, bubble-like sign, air bronchogram, vessel changes, margin, and tumour-lung interface. CT characteristics were compared among different histopathologic subtypes. Univariate and multivariate analysis were used to assess the relationship between CT characteristics of pGGN and lesion invasiveness, respectively.


There were statistically significant differences among histopathologic subtypes in lesion size, vessel changes, and tumour-lung interface (P<0.05). Univariate analysis revealed significant differences of vessel changes, margin and tumour-lung interface between preinvasive and invasive lesions (P<0.05). Logistic regression analysis showed that the vessel changes, unsmooth margin and clear tumour-lung interface were significant predictive factors for lesion invasiveness, with odds ratios (95% CI) of 2.57 (1.17-5.62), 1.83 (1.25-2.68) and 4.25 (1.78-10.14), respectively.


Invasive lesions are found in 55.3% of subcentimeter pGGNs in our cohort. Vessel changes, unsmooth margin, and clear lung-tumour interface may indicate the invasiveness of lung adenocarcinoma with subcentimeter pGGN.

Key points

• Invasive lesions were found in 55.3% of lung adenocarcinomas with subcentimeter pGGNs

• Lesion size, vessel changes, and tumour-lung interface showed different among histopathologic subtypes

• Vessel changes, unsmooth margin and clear tumour-lung interface were predictors for lesion invasiveness


Ground-glass nodule Lung neoplasms Adenocarcinoma Histopathology Tomography, X-ray computed 



Computed tomography


Pure ground-glass nodule


Atypical adenomatous hyperplasia


Adenocarcinoma in situ


Minimally invasive adenocarcinoma


Invasive pulmonary adenocarcinoma


Hounsfield unit


One-way analysis of variance




International Association for the Study of Lung Cancer


American Thoracic Society


European Respiratory Society


Compliance with ethical standards


The scientific guarantor of this publication is Dr. Shaohong Zhao.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.


The authors state that this work has not received any funding.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Ethical approval

Institutional Review Board approval was required.

Informed consent

Written informed consent was required for this study.


• retrospective

• diagnostic or prognostic study

• performed at one institution


  1. 1.
    Matsuguma H, Mori K, Nakahara R et al (2012) Characteristics of subsolid pulmonary nodules showing growth during follow-up with CT scanning. Chest 143:436–443CrossRefGoogle Scholar
  2. 2.
    Chang B, Hwang JH, Choi YH et al (2013) Natural history of pure ground-glass opacity lung nodules detected by low-dose CT scan. Chest 143:172–178CrossRefPubMedGoogle Scholar
  3. 3.
    Sawabata N, Kanzaki R, Sakamoto T et al (2014) Clinical predictor of pre- or minimally invasive pulmonary adenocarcinoma: possibility of sub-classification of clinical T1a. Eur J Cardiothorac Surg 45:256–261CrossRefPubMedGoogle Scholar
  4. 4.
    Yoshizawa A, Motoi N, Riely GJ et al (2011) 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 24:653–664Google Scholar
  5. 5.
    Lim HJ, Ahn S, Lee KS et al (2013) Persistent pure ground-glass opacity lung nodules ≥ 10 mm in diameter at CT scan: histopathologic comparisons and prognostic implications. Chest 144:1291–1299Google Scholar
  6. 6.
    Lee HJ, Jin MG, Chang HL et al (2009) Predictive CT findings of malignancy in ground-glass nodules on thin-section chest CT: the effects on radiologist performance. Eur Radiol 19:552–560CrossRefPubMedGoogle Scholar
  7. 7.
    Jiang B, Wang J, Jia P et al (2013) The value of CT attenuation in distinguishing atypical adenomatous hyperplasia from adenocarcinoma in situ. Zhongguo Fei Ai Za Zhi 16:579–583PubMedGoogle Scholar
  8. 8.
    Lee SM, Park CM, Goo JM et al (2013) Invasive pulmonary adenocarcinomas versus preinvasive lesions appearing as ground-glass nodules: differentiation by using CT features. Radiology 268:265–273CrossRefPubMedGoogle Scholar
  9. 9.
    Nakata M, Sawada S, Saeki H et al (2003) Prospective study of thoracoscopic limited resection for ground-glass opacity selected by computed tomography. Ann Thorac Surg 75:1601–1605CrossRefPubMedGoogle Scholar
  10. 10.
    Asamura H, Suzuki K, Watanabe S et al (2003) A clinicopathological study of resected subcentimeter lung cancers: a favorable prognosis for ground glass opacity lesions. Ann Thorac Surg 76:1016–1022CrossRefPubMedGoogle Scholar
  11. 11.
    Zhou Q, Suzuki K, Anami Y et al (2009) Clinicopathologic features in resected subcentimeter lung cancer--status of lymph node metastases. Interact Cardiovasc Thorac Surg 10:53–57CrossRefPubMedGoogle Scholar
  12. 12.
    Sakurai H, Nakagawa K, Watanabe SI et al (2015) Clinicopathologic features of resected subcentimeter lung cancer. Ann Thorac Surg 99:1731–1738CrossRefPubMedGoogle Scholar
  13. 13.
    Mao H, Labh K, Han F et al (2015) Diagnosis of the invasiveness of lung adenocarcinoma manifesting as ground glass opacities on high-resolution computed tomography. Thorac Cancer 7:129–135CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Travis WD, Brambilla E, Noguchi M et al (2011) International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society: international multidisciplinary classification of lung adenocarcinoma: executive summary. Proc Am Thorac Soc 8:381–385CrossRefPubMedGoogle Scholar
  15. 15.
    Travis WD, Brambilla E, Nicholson AG et al (2015) The 2015 world health organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. J Thorac Oncol 10:1243–1260CrossRefPubMedGoogle Scholar
  16. 16.
    Liao JH, Amin VB, Kadoch MA et al (2014) Subsolid pulmonary nodules: CT–pathologic correlation using the 2011 IASLC/ATS/ERS classification. Clin Imaging 39:344–351CrossRefPubMedGoogle Scholar
  17. 17.
    Yip R, Wolf A, Tam K et al (2016) Outcomes of lung cancers manifesting as nonsolid nodules. Lung Cancer 97:35–42CrossRefPubMedGoogle Scholar
  18. 18.
    Kato F, Hamasaki M, Miyake Y et al (2012) Clinicopathological characteristics of subcentimeter adenocarcinomas of the lung. Lung Cancer 77:495–500CrossRefPubMedGoogle Scholar
  19. 19.
    Hamatake D, Yoshida Y, Miyahara S et al (2012) Surgical outcomes of lung cancer measuring less than 1 cm in diameter. Interact Cardiovasc Thorac Surg 15:854–858CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Lee HY, Choi YL, Lee KS et al (2014) Pure ground-glass opacity neoplastic lung nodules: histopathology, imaging, and management. AJR 202:224–233CrossRefGoogle Scholar
  21. 21.
    Naidich DP, Bankier AA, Macmahon H et al (2013) Recommendations for the management of subsolid pulmonary nodules detected at CT: a statement from the fleischner society. Radiology 266(1):304–317CrossRefPubMedGoogle Scholar
  22. 22.
    Sim HJ, Choi SH, Chae EJ et al (2014) Surgical management of pulmonary adenocarcinoma presenting as a pure ground-glass nodule. Eur J Cardiothorac Surg 46:632–636CrossRefPubMedGoogle Scholar
  23. 23.
    Jin X, Zhao SH, Gao J et al (2015) CT characteristics and pathological implications of early stage (T1N0M0) lung adenocarcinoma with pure ground-glass opacity. Eur Radiol 25:2532–2540CrossRefPubMedGoogle Scholar
  24. 24.
    Jones KD (2013) Whence lepidic?: the history of a Canadian neologism. Arch Pathol Lab Med 137:1822–1824CrossRefPubMedGoogle Scholar
  25. 25.
    Wu F, Cai ZL, Tian SP et al (2016) Value of baseline clinical and CT characteristics for predicting the progression of persistent pure ground-glass nodule 10 mm or less in diameter. Acta Academiae Medicinae Sinicae 38(4):371–377PubMedGoogle Scholar
  26. 26.
    Honda T, Kondo T, Murakami S et al (2013) Radiographic and pathological analysis of small lung adenocarcinoma using the new IASLC classification. Clin Radiol 68:21–26CrossRefGoogle Scholar
  27. 27.
    Gao F, Li M, Ge X et al (2013) Multi-detector spiral CT study of the relationships between pulmonary ground-glass nodules and blood vessels. Eur Radiol 23:3271–3277CrossRefPubMedGoogle Scholar
  28. 28.
    Fan L, Liu SY, Li QC et al (2011) Pulmonary malignant focal ground-glass opacity nodules and solid nodules of 3 cm or less: comparison of multi-detector CT features. Eur Radiol 55:279–285Google Scholar
  29. 29.
    Si MJ, Tao XF, Du GY et al (2016) 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 Radiol 85:1708–1715CrossRefGoogle Scholar

Copyright information

© European Society of Radiology 2017

Authors and Affiliations

  • Fang Wu
    • 1
    • 2
  • Shu-ping Tian
    • 3
  • Xin Jin
    • 1
  • Rui Jing
    • 1
  • Yue-qing Yang
    • 1
  • Mei Jin
    • 1
  • Shao-hong Zhao
    • 1
    Email author
  1. 1.Department of RadiologyChinese PLA General HospitalBeijingChina
  2. 2.Department of Radiology, Xuanwu HospitalCapital Medical UniversityBeijingChina
  3. 3.Department of RadiologyNavy General HospitalBeijingChina

Personalised recommendations