Skip to main content

Advertisement

Log in

Intratumoral and peritumoral radiomics nomograms for the preoperative prediction of lymphovascular invasion and overall survival in non-small cell lung cancer

  • Imaging Informatics and Artificial Intelligence
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To evaluate the predictive value of intratumoral and peritumoral radiomics and radiomics nomogram for preoperative lymphovascular invasion (LVI) status and overall survival (OS) in patients with non-small cell lung cancer (NSCLC).

Methods

In total, 240 NSCLC patients from our institution were randomly divided into the training cohort (n = 145) and internal validation cohort (n = 95) with a ratio of 6:4, and 65 patients from the Cancer Imaging Archive were enrolled as the external validation cohort. We extracted 1217 CT-based radiomics features from the gross tumor volume (GTV) and gross tumor volume incorporating peritumoral 3, 6, and 9 mm regions (GPTV3, GPTV6, GPTV9). A radiomics nomogram based on clinical independent predictors and radiomics score (Radscore) of the best radiomics model was constructed. The correlation between factors and OS was evaluated with the Kaplan-Meier survival analysis and Cox proportional hazards regression analysis.

Results

Compared with GTV, GPTV3, and GPTV6 radiomics models, GPTV9 radiomics model exhibited better prediction performance with the AUCs of 0.82, 0.75, and 0.67 in the training, internal validation, and external validation cohorts, respectively. In the clinical model, smoking and clinical stage were independent predictors. The nomogram incorporating independent predictors and GPTV9-Radscore was clinically useful, with the AUCs of 0.89, 0.83, and 0.66 in three cohorts. Pathological LVI, GPTV9-Radscore-predicted, and Nomoscore-predicted LVI were associated with poor OS (p < 0.05).

Conclusions

CT-based radiomics nomogram can predict LVI and OS in patients with NSCLC and may help in making personalized treatment strategies before surgery.

Key Points

• Compared with GTV, GPTV 3 , and GPTV 6 radiomics models, GPTV 9 radiomics model showed better prediction performance for LVI status in NSCLC.

• The radiomics nomogram based on GPTV 9 radiomics features and clinical independent predictors could effectively predict LVI status and OS in NSCLC and outperformed the clinical model.

• The radiomics nomogram had a wider scope of clinical application.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AUC:

Area under curve

CT:

Computed tomography

GPTV:

Gross peritumoral tumor volume

GTV:

Gross tumor volume

ICC:

Intraclass correlation coefficient

LASSO:

Least absolute shrinkage and selection operator

LVI:

Lymphovascular invasion

NSCLC:

Non-small cell lung cancer

OS:

Overall survival

TCIA:

The Cancer Imaging Archive

References

  1. Clark ME, Bedford LE, Young B et al (2018) Lung cancer CT screening: psychological responses in the presence and absence of pulmonary nodules. Lung Cancer 124:160–167

    Article  Google Scholar 

  2. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2012) Global cancer statistics. CA Cancer J Clin 65(2):87–108

    Article  Google Scholar 

  3. Ettinger DS, Wood DE, Aisner DL et al (2021) NCCN guidelines insights: non-small cell lung cancer, version 2.2021. J Natl Compr Canc Netw 19(3):254–266

  4. Sung SY, Kwak YK, Lee SW et al (2018) Lymphovascular invasion increases the risk of nodal and distant recurrence in node-negative stage I-iia non-small-cell lung cancer. Oncology 95(3):156–162

    Article  Google Scholar 

  5. Okada S, Mizuguchi S, Izumi N et al (2017) Prognostic value of the frequency of vascular invasion in stage I non-small cell lung cancer. Gen Thorac Cardiovasc Surg 65:32–39

    Article  Google Scholar 

  6. Shimada Y, Saji H, Kato Y et al (2016) The frequency and prognostic impact of pathological microscopic vascular invasion according to tumor size in non-small cell lung cancer. Chest 149:775–785

    Article  Google Scholar 

  7. Ramnefjell M, Aamelfot C, Helgeland L, Akslen LA (2017) Vascular invasion is an adverse prognostic factor in resected non-small-cell lung cancer. APMIS 125(3):197–206

    Article  CAS  Google Scholar 

  8. Shimada Y, Saji H, Yoshida K et al (2012) Pathological vascular invasion and tumor differentiation predict cancer recurrence in stage IA non-small-cell lung cancer after complete surgical resection. J Thorac Oncol 7(8):1263–1270

    Article  Google Scholar 

  9. Wang S, Xu J, Wang R et al (2018) Adjuvant chemotherapy may improve prognosis after resection of stage I lung cancer with lymphovascular invasion. J Thorac Cardiovasc Surg 156(5):2006–2015.e2

    Article  Google Scholar 

  10. Tsutani Y, Miyata Y, Kushitani K, Takeshima Y, Yoshimura M, Okada M (2014) Propensity score-matched analysis of adjuvant chemotherapy for stage I non-small cell lung cancer. J Thorac Cardiovasc Surg 148:1179–1185

    Article  Google Scholar 

  11. Yun JK, Lee GD, Choi S et al (2020) Comparison of prognostic impact of lymphovascular invasion in stage IA non-small cell lung cancer after lobectomy versus sublobar resection: a propensity score-matched analysis. Lung Cancer 146:105–111

    Article  Google Scholar 

  12. Zhao S, Li F, Guo X et al (2020) New additional scoring formula on the pathological features in stage I lung adenocarcinoma patients: impact on survival. Int J Med Sci 17(13):1871–1878

    Article  Google Scholar 

  13. Ito R, Iwano S, Shimamoto H et al (2017) A comparative analysis of dual-phase dual-energy CT and FDG-PET/CT for the prediction of histopathological invasiveness of non-small cell lung cancer. Eur J Radiol 95:186–191

    Article  Google Scholar 

  14. Gu Q, Feng Z, Liang Q et al (2019) Machine learning-based radiomics strategy for prediction of cell proliferation in non-small cell lung cancer. Eur J Radiol 118:32–37

    Article  Google Scholar 

  15. Lubner MG, Smith AD, Sandrasegaran K, Sahani DV, Pickhardt PJ (2017) CT texture analysis: definitions, applications, biologic correlates, and challenges. Radiographics 37(5):1483–1503

    Article  Google Scholar 

  16. Yang G, Nie P, Zhao L et al (2020) 2D and 3D texture analysis to predict lymphovascular invasion in lung adenocarcinoma. Eur J Radiol 129:109–111

    Article  Google Scholar 

  17. Pietras K, Ostman A (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 316(8):1324–1331

    Article  CAS  Google Scholar 

  18. Wang X, Wan Q, Chen H, Li Y, Li X (2020) Classification of pulmonary lesion based on multiparametric MRI: utility of radiomics and comparison of machine learning methods. Eur Radiol 30(8):4595–4605

    Article  Google Scholar 

  19. Dercle L, Fronheiser M, Lu L et al (2020) Identification of non-small cell lung cancer sensitive to systemic cancer therapies using radiomics. Clin Cancer Res 26(9):2151–2162

    Article  CAS  Google Scholar 

  20. Giraud P, Antoine M, Larrouy A et al (2000) Evaluation of microscopic tumor extension in non-small-cell lung cancer for three-dimensional conformal radiotherapy planning. Int J Radiat Oncol Biol Phys 48(4):1015–1024

    Article  CAS  Google Scholar 

  21. Liu K, Li K, Wu T et al (2022) Improving the accuracy of prognosis for clinical stage I solid lung adenocarcinoma by radiomics models covering tumor per se and peritumoral changes on CT. Eur Radiol 32(2):1065–1077

    Article  Google Scholar 

  22. Zhang R, Cai Z, Luo Y, Wang Z, Wang W (2021) Preliminary exploration of response the course of radiotherapy for stage III non-small cell lung cancer based on longitudinal CT radiomics features. Eur J Radiol Open 9:100391

    Article  Google Scholar 

  23. Feng Z, Rong P, Cao P et al (2018) Machine learning-based quantitative texture analysis of CT images of small renal masses: differentiation of angiomyolipoma without visible fat from renal cell carcinoma. Eur Radiol 28(4):1625–1633

    Article  Google Scholar 

  24. Ren J, Yuan Y, Qi M, Tao X (2020) Machine learning-based CT texture analysis to predict HPV status in oropharyngeal squamous cell carcinoma: comparison of 2D and 3D segmentation. Eur Radiol 30(12):6858–6866

    Article  Google Scholar 

  25. Chen Y, Xia Y, Tolat PP et al (2021) Comparison of conventional gadoxetate disodium-enhanced MRI features and radiomics signatures with machine learning for diagnosing microvascular invasion. AJR Am J Roentgenol 216(6):1510–1520

    Article  Google Scholar 

  26. Saijo T, Ishii G, Ochiai A et al (2007) Evaluation of extratumoral lymphatic permeation in non-small cell lung cancer as a means of predicting outcome. Lung Cancer 55(1):61–66

    Article  Google Scholar 

  27. Pérez-Morales J, Tunali I, Stringfield O et al (2020) Peritumoral and intratumoral radiomic features predict survival outcomes among patients diagnosed in lung cancer screening. Sci Rep 10(1):10528

    Article  Google Scholar 

  28. Tunali I, Hall LO, Napel S et al (2019) Stability and reproducibility of computed tomography radiomic features extracted from peritumoral regions of lung cancer lesions. Med Phys 46(11):5075–5085

    Article  Google Scholar 

  29. Joyce JA, Pollard JW et al (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9(4):239–252

    Article  CAS  Google Scholar 

  30. Jiang T, Song J, Wang X et al (2021) Intratumoral and peritumoral analysis of mammography, tomosynthesis, and multiparametric MRI for predicting Ki-67 level in breast cancer: a radiomics-based study. Mol Imaging Biol. https://doi.org/10.1007/s11307-021-01695-w

  31. Dou TH, Coroller TP, van Griethuysen JJM, Mak RH, Aerts HJWL (2018) Peritumoral radiomics features predict distant metastasis in locally advanced NSCLC. PLoS One 13(11):e0206108

  32. Wu DM, Deng SH, Zhou J et al (2020) PLEK2 mediates metastasis and vascular invasion via the ubiquitin-dependent degradation of SHIP2 in non-small cell lung cancer. Int J Cancer 146(9):2563–2575

    Article  CAS  Google Scholar 

  33. Alwithenani A, Bethune D, Castonguay M et al (2021) Profiling non-small cell lung cancer reveals that PD-L1 is associated with wild type EGFR and vascular invasion, and immunohistochemistry quantification of PD-L1 correlates weakly with RT-qPCR. PLoS One 16(5):e0251080

  34. Li C, Tian Y, Shen Y, Wen B, He Y (2021) Utility of volumetric metabolic parameters on preoperative FDG PET/CT for predicting tumor lymphovascular invasion in non-small cell lung cancer. AJR Am J Roentgenol 217(6):1433–1443

    Article  Google Scholar 

  35. Shimada Y, Ishii G, Hishida T, Yoshida J, Nishimura M, Nagai K (2010) Extratumoral vascular invasion is a significant prognostic indicator and a predicting factor of distant metastasis in non-small cell lung cancer. J Thorac Oncol 5(7):970–975

    Article  Google Scholar 

  36. Sun W, Jiang M, Dang J, Chang P, Yin FF (2018) Effect of machine learning methods on predicting NSCLC overall survival time based on radiomics analysis. Radiat Oncol 13(1):197

    Article  Google Scholar 

  37. Botta F, Raimondi S, Rinaldi L et al (2020) Association of a CT-based clinical and radiomics score of non-small cell lung cancer (NSCLC) with lymph node status and overall survival. Cancers (Basel) 12(6):1432

    Article  CAS  Google Scholar 

Download references

Funding

This study has received funding from Key Project of Nantong Science and Technology Bureau of China (grant number MS22021047) and Clinical Research Plan of SHDC (grant number SHDC2020CR3080B).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Feng Feng.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Feng Feng.

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

One of the authors (Shaofeng Duan) has significant statistical expertise.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• multicenter study

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Qiaoling Chen and JingJing Shao are the first authors.

Supplementary information

ESM 1

(PDF 597 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, Q., Shao, J., Xue, T. et al. Intratumoral and peritumoral radiomics nomograms for the preoperative prediction of lymphovascular invasion and overall survival in non-small cell lung cancer. Eur Radiol 33, 947–958 (2023). https://doi.org/10.1007/s00330-022-09109-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-022-09109-3

Keywords

Navigation