European Radiology

, Volume 29, Issue 3, pp 1586–1594 | Cite as

Implication of total tumor size on the prognosis of patients with clinical stage IA lung adenocarcinomas appearing as part-solid nodules: Does only the solid portion size matter?

  • Hyungjin Kim
  • Jin Mo GooEmail author
  • Young Joo Suh
  • Chang Min Park
  • Young Tae Kim



The aim was to investigate the effect of clinico-radiologic variables, including total tumor (Ttotal) size and clinical T category, on the prognosis of patients with stage IA (T1N0M0) lung adenocarcinomas appearing as part-solid nodules (PSNs).


This institutional review board-approved retrospective study included 506 patients (male:female = 200:306; median age, 62 years) with PSNs of the adenocarcinoma spectrum in clinical stage IA who underwent standard lobectomy at a single tertiary medical center. Prognostic stratification of the patients in terms of disease-free survival was analyzed with variables including age, sex, Ttotal size, solid portion size, clinical T category, and tumor location using univariate and subsequent multivariate Cox regression analysis. Subgroup analysis was performed to reveal the effect of the Ttotal size at each clinical T category.


Multivariate Cox regression analysis demonstrated that Ttotal size*cT1b [interaction term; hazard ratio (HR) = 1.091; 95% confidence interval (CI): 1.015, 1.173; p = 0.019] and cT1c (HR = 68.436; 95% CI: 2.797, 1674.415; p = 0.010) were independent risk factors for the tumor recurrence. When patients with cT1b were dichotomized based on a Ttotal size cutoff of 3.0 cm, PSNs with Ttotal > 3.0 cm showed a significantly worse outcome (HR = 3.796; 95% CI: 1.006, 14.317; p = 0.049). No significant difference was observed in the probability of recurrence between cT1b with Ttotal > 3.0 cm and cT1c (p = 0.915).


Ttotal size is a significant prognostic factor in adenocarcinoma patients in cT1b without lymph node or distant metastasis. PSNs in cT1b with Ttotal > 3.0 cm have a comparable risk of lung cancer recurrence to those in cT1c.

Key Points

• Current T descriptor was a powerful prognostic factor in stage IA adenocarcinomas appearing as part-solid nodules.

Total tumor size further stratified risk of recurrence of adenocarcinomas in cT1b.

Upstaging of tumors in cT1b with total tumor size > 3.0 cm may be more appropriate.


Lung neoplasms Adenocarcinoma Prognosis Disease-free survival Neoplasm staging 





Consolidation-to-tumor ratio


Disease-free survival


Hounsfield unit


Interquartile range


Minimally invasive adenocarcinoma


Part-solid nodule


Subsolid nodule


Total tumor



We sincerely express our gratitude to Sunkyung Jeon, Jong Hyuk Lee, Su Yeon Ahn, Roh-Eul Yoo, Hyun-ju Lim, Juil Park, and Woo Hyeon Lim for their help in data acquisition.


This study has received funding by a grant from the National R&D Program for Cancer Control, Ministry for Health and Welfare, Republic of Korea (1520230).

Compliance with Ethical Standards


The scientific guarantor of this publication is Jin Mo Goo.

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.

Statistics and Biometry

No complex statistical methods were necessary for this paper.

Informed Consent

Written informed consent was waived by the Institutional Review Board.

Ethical Approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in journal articles (Eur Radiol 2016 26:4465-4474; Eur J Radiol 2016 85:1174-1180; Eur Radiol 2017 27:3266-3274; Eur Radiol 2018 28:2124-2133; Eur Radiol 2017 27:1369-1376).


• retrospective

• diagnostic or prognostic study

• performed at one institution


  1. 1.
    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 266:304–317Google Scholar
  2. 2.
    Kakinuma R, Noguchi M, Ashizawa K et al (2016) Natural history of pulmonary subsolid nodules: a prospective multicenter study. J Thorac Oncol 11:1012–1028Google Scholar
  3. 3.
    Matsuguma H, Mori K, Nakahara R et al (2013) Characteristics of subsolid pulmonary nodules showing growth during follow-up with CT scanning. Chest 143:436–443Google Scholar
  4. 4.
    Silva M, Sverzellati N, Manna C et al (2012) Long-term surveillance of ground-glass nodules: evidence from the MILD trial. J Thorac Oncol 7:1541–1546Google Scholar
  5. 5.
    Henschke CI, Yankelevitz DF, Mirtcheva R et al (2002) CT screening for lung cancer: frequency and significance of part-solid and nonsolid nodules. AJR Am J Roentgenol 178:1053–1057Google Scholar
  6. 6.
    Hwang EJ, Park CM, Ryu Y et al (2015) Pulmonary adenocarcinomas appearing as part-solid ground-glass nodules: is measuring solid component size a better prognostic indicator? Eur Radiol 25:558–567Google Scholar
  7. 7.
    Maeyashiki T, Suzuki K, Hattori A, Matsunaga T, Takamochi K, Oh S (2013) The size of consolidation on thin-section computed tomography is a better predictor of survival than the maximum tumour dimension in resectable lung cancer. Eur J Cardiothorac Surg 43:915–918Google Scholar
  8. 8.
    Tsutani Y, Miyata Y, Nakayama H et al (2012) 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 143:607–612Google Scholar
  9. 9.
    Detterbeck FC, Boffa DJ, Kim AW, Tanoue LT (2017) The eighth edition lung cancer stage classification. Chest 151:193–203Google Scholar
  10. 10.
    Travis WD, Asamura H, Bankier AA et al (2016) 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 11:1204–1223Google Scholar
  11. 11.
    Aokage K, Miyoshi T, Ishii G et al (2018) Influence of ground glass opacity and the corresponding pathological findings on survival in patients with clinical stage I non-small cell lung cancer. J Thorac Oncol 13:533–542Google Scholar
  12. 12.
    Cohen JG, Goo JM, Yoo RE et al (2016) Software performance in segmenting ground-glass and solid components of subsolid nodules in pulmonary adenocarcinomas. Eur Radiol 26:4465–4474Google Scholar
  13. 13.
    Cohen JG, Goo JM, Yoo RE et al (2016) The effect of late-phase contrast enhancement on semi-automatic software measurements of CT attenuation and volume of part-solid nodules in lung adenocarcinomas. Eur J Radiol 85:1174–1180Google Scholar
  14. 14.
    Cohen JG, Kim H, Park SB et al (2017) Comparison of the effects of model-based iterative reconstruction and filtered back projection algorithms on software measurements in pulmonary subsolid nodules. Eur Radiol 27:3266–3274Google Scholar
  15. 15.
    Kim H, Park CM, Hwang EJ, Ahn SY, Goo JM (2018) Pulmonary subsolid nodules: value of semi-automatic measurement in diagnostic accuracy, diagnostic reproducibility and nodule classification agreement. Eur Radiol 28:2124–2133Google Scholar
  16. 16.
    Yoo RE, Goo JM, Hwang EJ et al (2017) Retrospective assessment of interobserver agreement and accuracy in classifications and measurements in subsolid nodules with solid components less than 8mm: which window setting is better? Eur Radiol 27:1369–1376Google Scholar
  17. 17.
    Hansell DM, Bankier AA, MacMahon H, McLoud TC, Muller NL, Remy J (2008) Fleischner Society: glossary of terms for thoracic imaging. Radiology 246:697–722Google Scholar
  18. 18.
    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. J Thorac Oncol 6:244–285Google Scholar
  19. 19.
    Lee KH, Goo JM, Park SJ et al (2014) Correlation between the size of the solid component on thin-section CT and the invasive component on pathology in small lung adenocarcinomas manifesting as ground-glass nodules. J Thorac Oncol 9:74–82Google Scholar
  20. 20.
    Rami-Porta R, Ball D, Crowley J et al (2007) The IASLC lung cancer staging project: proposals for the revision of the T descriptors in the forthcoming (seventh) edition of the TNM classification for lung cancer. J Thorac Oncol 2:593–602Google Scholar
  21. 21.
    Berry MF, Gao R, Kunder CA et al (2018) Presence of even a small ground-glass component in lung adenocarcinoma predicts better survival. Clin Lung Cancer 19:e47–e51Google Scholar
  22. 22.
    Kim H, Park CM, Goo JM, Wildberger JE, Kauczor HU (2015) Quantitative computed tomography imaging biomarkers in the diagnosis and management of lung cancer. Invest Radiol 50:571–583Google Scholar
  23. 23.
    Asamura H, Hishida T, Suzuki K et al (2013) Radiographically determined noninvasive adenocarcinoma of the lung: survival outcomes of Japan Clinical Oncology Group 0201. J Thorac Cardiovasc Surg 146:24–30Google Scholar
  24. 24.
    Nitadori J, Bograd AJ, Morales EA et al (2013) Preoperative consolidation-to-tumor ratio and SUVmax stratify the risk of recurrence in patients undergoing limited resection for lung adenocarcinoma ≤ 2cm. Ann Surg Oncol 20:4282–4288Google Scholar
  25. 25.
    Aokage K, Yoshida J, Ishii G et al (2013) Identification of early T1b lung adenocarcinoma based on thin-section computed tomography findings. J Thorac Oncol 8:1289–1294Google Scholar
  26. 26.
    Tsurugai Y, Kozuka T, Ishizuka N, Oguchi M (2016) Relationship between the consolidation to maximum tumor diameter ratio and outcomes following stereotactic body radiotherapy for stage I non-small-cell lung cancer. Lung Cancer 92:47–52Google Scholar
  27. 27.
    Revel MP, Mannes I, Benzakoun J et al (2018) Subsolid lung nodule classification: a CT criterion for improving interobserver agreement. Radiology 286:316–325Google Scholar
  28. 28.
    Kadota K, Villena-Vargas J, Yoshizawa A et al (2014) Prognostic significance of adenocarcinoma in situ, minimally invasive adenocarcinoma, and nonmucinous lepidic predominant invasive adenocarcinoma of the lung in patients with stage I disease. Am J Surg Pathol 38:448–460Google Scholar
  29. 29.
    Behera M, Owonikoko TK, Gal AA et al (2016) Lung adenocarcinoma staging using the 2011 IASLC/ATS/ERS classification: a pooled analysis of adenocarcinoma in situ and minimally invasive adenocarcinoma. Clin Lung Cancer 17:e57–e64Google Scholar
  30. 30.
    Kamiya S, Iwano S, Umakoshi H et al (2018) Computer-aided volumetry of part-solid lung cancers by using CT: solid component size predicts prognosis. Radiology 287:1030–1040Google Scholar
  31. 31.
    Takenaka T, Yamazaki K, Miura N, Mori R, Takeo S (2016) The prognostic impact of tumor volume in patients with clinical stage IA non-small cell lung cancer. J Thorac Oncol 11:1074–1080Google Scholar
  32. 32.
    Yanagawa M, Tanaka Y, Leung AN et al (2014) Prognostic importance of volumetric measurements in stage I lung adenocarcinoma. Radiology 272:557–567Google Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  1. 1.Department of RadiologySeoul National University College of Medicine, and Institute of Radiation Medicine, Seoul National University Medical Research CenterSeoulKorea
  2. 2.Cancer Research InstituteSeoul National UniversitySeoulKorea
  3. 3.Department of Radiology, Research Institute of Radiological Science, Severance HospitalYonsei University College of MedicineSeoulKorea
  4. 4.Department of Thoracic and Cardiovascular SurgerySeoul National University College of MedicineSeoulKorea

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