Abstract
Objectives
To construct a radiomic model of low-dose CT (LDCT) to predict the differentiation grade of invasive non-mucinous pulmonary adenocarcinoma (IPA) and compare its diagnostic performance with quantitative-semantic model and radiologists.
Methods
A total of 682 pulmonary nodules were divided into the primary cohort (181 grade 1; 254 grade 2; 64 grade 3) and validation cohort (69 grade 1; 99 grade 2; 15 grade 3) according to scanners. The radiomic and quantitative-semantic models were built using ordinal logistic regression. The diagnostic performance of the models and radiologists was assessed by the area under the curve (AUC) of the receiver operating characteristic curve and accuracy.
Results
The radiomic model demonstrated excellent diagnostic performance in the validation cohort (AUC, 0.900 (95%CI: 0.847–0.939) for Grade 1 vs. Grade 2/Grade 3; AUC, 0.929 (95%CI: 0.882–0.962) for Grade 1/Grade 2 vs. Grade 3; accuracy, 0.803 (95%CI: 0.737–0.857)). No significant difference in diagnostic performance was found between the radiomic model and radiological expert (AUC, 0.840 (95%CI: 0.779–0.890) for Grade 1 vs. Grade 2/Grade 3, p = 0.130; AUC, 0.852 (95%CI: 0.793–0.900) for Grade 1/Grade 2 vs. Grade 3, p = 0.170; accuracy, 0.743 (95%CI: 0.673–0.804), p = 0.079), but the radiomic model outperformed the quantitative-semantic model and inexperienced radiologists (all p < 0.05).
Conclusions
The radiomic model of LDCT can be used to predict the differentiation grade of IPA in lung cancer screening, and its diagnostic performance is comparable to that of radiological expert.
Key Points
• Early identifying the novel differentiation grade of invasive non-mucinous pulmonary adenocarcinoma may provide guidance for further surveillance, surgical strategy, or more adjuvant treatment.
• The diagnostic performance of the radiomic model is comparable to that of a radiological expert and superior to that of the quantitative-semantic model and inexperienced radiologists.
• The radiomic model of low-dose CT can be used to predict the differentiation grade of invasive non-mucinous pulmonary adenocarcinoma in lung cancer screening.
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Abbreviations
- AI:
-
Artificial intelligence
- AIC:
-
Akaike’s information criterion
- AUC:
-
Area under the curve
- CI:
-
Confidence intervals
- GLCM:
-
Grey level co-occurrence matrix
- GLRLM:
-
Grey level run length matrix
- GLSZM:
-
Grey level size zone matrix
- IASLC:
-
International Association for the Study of Lung Cancer Pathology Committee
- IBSI:
-
Imaging Biomarker Standardization Initiative
- IPA:
-
Invasive non-mucinous pulmonary adenocarcinoma
- LDCT:
-
Low-dose computed tomography
- mRMR:
-
Minimum redundancy-maximum relevance
- NGLDM:
-
Neighborhood grey level difference matrix
- NGTDM:
-
Neighborhood grey tone difference matrix
- ROC:
-
Receiver operating characteristic
- ROI:
-
Region of interest
- TRIPOD:
-
Transparent Reporting of a Multivariable Prediction Model for Individual Prognosis or Diagnosis.
- VIF:
-
Variance inflation factor
- WHO:
-
World Health Organization
References
Sung H, Ferlay J, Siegel RL et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
National Lung Screening Trial Research T (2019) Lung cancer incidence and mortality with extended follow-up in the National Lung Screening Trial. J Thorac Oncol 14:1732–1742
de Koning HJ, van der Aalst CM, de Jong PA et al (2020) Reduced lung-cancer mortality with volume CT screening in a randomized trial. N Engl J Med 382:503–513
Moreira AL, Ocampo PSS, Xia Y et al (2020) A grading system for invasive pulmonary adenocarcinoma: a proposal from the International Association for the Study of Lung Cancer Pathology Committee. J Thorac Oncol 15:1599–1610
Nicholson AG, Tsao MS, Beasley MB et al (2022) The 2021 WHO classification of lung tumors: impact of advances since 2015. J Thorac Oncol 17:362–387
Deng C, Zheng Q, Zhang Y et al (2021) Validation of the novel international association for the study of lung cancer grading system for invasive pulmonary adenocarcinoma and association with common driver mutations. J Thorac Oncol 16:1684–1693
Rokutan-Kurata M, Yoshizawa A, Ueno K et al (2021) Validation study of the international association for the study of lung cancer histologic grading system of invasive lung adenocarcinoma. J Thorac Oncol 16:1753–1758
Hou L, Wang T, Chen D et al (2022) Prognostic and predictive value of the newly proposed grading system of invasive pulmonary adenocarcinoma in Chinese patients: a retrospective multicohort study. Mod Pathol 35:749–756
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 6:244–285
Lederlin M, Puderbach M, Muley T et al (2013) Correlation of radio- and histomorphological pattern of pulmonary adenocarcinoma. Eur Respir J 41:943–951
Miao Y, Zhang J, Zou J, Zhu Q, Lv T, Song Y (2017) Correlation in histological subtypes with high resolution computed tomography signatures of early stage lung adenocarcinoma. Transl Lung Cancer Res 6:14–22
Park S, Lee SM, Noh HN et al (2020) Differentiation of predominant subtypes of lung adenocarcinoma using a quantitative radiomics approach on CT. Eur Radiol 30:4883–4892
Wang C, Shao J, Lv J et al (2021) Deep learning for predicting subtype classification and survival of lung adenocarcinoma on computed tomography. Transl Oncol 14:101141
Russell PA, Wainer Z, Wright GM, Daniels M, Conron M, Williams RA (2011) Does lung adenocarcinoma subtype predict patient survival?: A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol 6:1496–1504
Liu J, Xu H, Qing H et al (2021) Comparison of radiomic models based on low-dose and standard-dose CT for prediction of adenocarcinomas and benign lesions in solid pulmonary nodules. Front Oncol 10:634298
Li Y, Liu J, Yang X et al (2022) Prediction of invasive adenocarcinomas manifesting as pure ground-glass nodules based on radiomic signature of low-dose CT in lung cancer screening. Br J Radiol 95:20211048
Wang Q, Zhou X, Wang C et al (2019) WGAN-based synthetic minority over-sampling technique: improving semantic fine-grained classification for lung nodules in CT images. IEEE Access 7:18450–18463
Mu G, Chen Y, Wu D, Zhan Y, Zhou XS, Gao Y (2019) Relu cascade of feature pyramid networks for CT pulmonary nodule detection. Springer International Publishing, Cham, Cham, pp 444–452
Shafiq-Ul-Hassan M, Zhang GG, Latifi K et al (2017) Intrinsic dependencies of CT radiomic features on voxel size and number of gray levels. Med Phys 44:1050–1062
Zwanenburg A, Vallières M, Abdalah MA et al (2020) The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology 295:328–338
Bettinelli A, Marturano F, Avanzo M et al (2022) A novel benchmarking approach to assess the agreement among radiomic tools. Radiology 303:533–541
McNitt-Gray M, Napel S, Jaggi A et al (2020) Standardization in quantitative imaging: a multicenter comparison of radiomic features from different software Packages on digital reference objects and patient data sets. Tomography 6:118–128
Yip SS, Aerts HJ (2016) Applications and limitations of radiomics. Phys Med Biol 61:R150-166
Welch ML, McIntosh C, Haibe-Kains B et al (2019) Vulnerabilities of radiomic signature development: The need for safeguards. Radiother Oncol 130:2–9
Branchini M, Zorz A, Zucchetta P et al (2019) Impact of acquisition count statistics reduction and SUV discretization on PET radiomic features in pediatric 18F-FDG-PET/MRI examinations. Phys Med 59:117–126
Li Y, Tan G, Vangel M, Hall J, Cai W (2020) Influence of feature calculating parameters on the reproducibility of CT radiomic features: a thoracic phantom study. Quant Imaging Med Surg 10:1775–1785
Hanchuan P, Fuhui L, Ding C (2005) Feature selection based on mutual information criteria of max-dependency, max-relevance, and min-redundancy. IEEE Trans Pattern Anal Mach Intell 27:1226–1238
Winship C, Mare RD (1984) Regression models with ordinal variables. Am Sociol Rev 49:512–525
Ananth CV, Kleinbaum DG (1997) Regression models for ordinal responses: a review of methods and applications. Int J Epidemiol 26:1323–1333
Liu X (2009) Ordinal regression analysis: fitting the proportional odds model using Stata, SAS and SPSS. J Mod Appl Stat Methods 8:632–642
Pan W (2001) Akaike’s information criterion in generalized estimating equations. Biometrics 57:120–125
Brant R (1990) Assessing proportionality in the proportional odds model for ordinal logistic regression. Biometrics 46:1171–1178
Yoo W, Mayberry R, Bae S, Singh K, Peter He Q, Lillard JW Jr (2014) A study of effects of multicollinearity in the multivariable analysis. Int J Appl Sci Technol 4:9–19
MacMahon H, Naidich DP, Goo JM et al (2017) Guidelines for management of incidental pulmonary nodules detected on CT images: from the Fleischner Society 2017. Radiology 284:228–243
Fagerland M, Hosmer D (2016) Tests for goodness of fit in ordinal logistic regression models. J Stat Comput Simul 86:1–21
Fagerland MW, Hosmer DW (2017) How to test for goodness of fit in ordinal logistic regression models. Stand Genomic Sci 17:668–686
DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845
Newcombe RG (1998) Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med 17:857–872
Hintze JL (2019) Test for multiple correlated proportions: McNemar-Bowker test of symmetry. NCSS PASS. Available via https://ncss-wpengine.netdna-ssl.com/wp-content/themes/ncss/pdf/Procedures/PASS/Tests_for_Multiple_Correlated_Proportions-McNemar-Bowker_Test_of_Symmetry.pdf. Accessed 8 May 2022
Moons KG, Altman DG, Reitsma JB et al (2015) Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): explanation and elaboration. Ann Intern Med 162:W1-73
Zhao Y, Wang R, Shen X et al (2016) Minor components of micropapillary and solid subtypes in lung adenocarcinoma are predictors of lymph node metastasis and poor prognosis. Ann Surg Oncol 23:2099–2105
Nitadori J, Bograd AJ, Kadota K et al (2013) Impact of micropapillary histologic subtype in selecting limited resection vs lobectomy for lung adenocarcinoma of 2cm or smaller. J Natl Cancer Inst 105:1212–1220
Hong JH, Park S, Kim H et al (2021) Volume and mass doubling time of lung adenocarcinoma according to WHO histologic classification. Korean J Radiol 22:464–475
Song SH, Park H, Lee G et al (2017) Imaging phenotyping using radiomics to predict micropapillary pattern within lung adenocarcinoma. J Thorac Oncol 12:624–632
Wang X, Zhang L, Yang X et al (2020) Deep learning combined with radiomics may optimize the prediction in differentiating high-grade lung adenocarcinomas in ground glass opacity lesions on CT scans. Eur J Radiol 129:109150
Chen LW, Yang SM, Wang HJ et al (2021) Prediction of micropapillary and solid pattern in lung adenocarcinoma using radiomic values extracted from near-pure histopathological subtypes. Eur Radiol 31:5127–5138
He B, Song Y, Wang L et al (2021) A machine learning-based prediction of the micropapillary/solid growth pattern in invasive lung adenocarcinoma with radiomics. Transl Lung Cancer Res 10:955–964
Warner P (2008) Ordinal logistic regression. J Fam Plann Reprod Health Care 34:169–170
Fujikawa R, Muraoka Y, Kashima J et al (2022) Clinicopathologic and genotypic features of lung adenocarcinoma characterized by the International Association for the Study of Lung Cancer Grading System. J Thorac Oncol 17:700–707
Takahashi S, Tanaka N, Okimoto T et al (2012) Long term follow-up for small pure ground-glass nodules: implications of determining an optimum follow-up period and high-resolution CT findings to predict the growth of nodules. Jpn J Radiol 30:206–217
Nakazono T, Sakao Y, Yamaguchi K, Imai S, Kumazoe H, Kudo S (2005) Subtypes of peripheral adenocarcinoma of the lung: differentiation by thin-section CT. Eur Radiol 15:1563–1568
Aerts HJ (2016) The potential of radiomic-based phenotyping in precision medicine: a review. JAMA Oncol 2:1636–1642
Tomaszewski MR, Gillies RJ (2021) The biological meaning of radiomic features. Radiology 298:505–516
Yip SSF, Liu Y, Parmar C et al (2017) Associations between radiologist-defined semantic and automatically computed radiomic features in non-small cell lung cancer. Sci Rep 7:3519
Mackin D, Fave X, Zhang L et al (2015) Measuring computed tomography scanner variability of radiomics features. Invest Radiol 50:757–765
Berenguer R, Pastor-Juan MDR, Canales-Vázquez J et al (2018) Radiomics of CT features may be nonreproducible and redundant: influence of CT acquisition parameters. Radiology 288:407–415
Funding
This study has received funding from the National Natural Science Foundation of China (82202141), the Sichuan Science and Technology Program (2021YFS0075, 2021YFS0225), and the Chengdu Science and Technology Program (2021-YF05-01507-SN).
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The scientific guarantor of this publication is Peng Zhou.
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Li, Y., Liu, J., Yang, X. et al. An ordinal radiomic model to predict the differentiation grade of invasive non-mucinous pulmonary adenocarcinoma based on low-dose computed tomography in lung cancer screening. Eur Radiol 33, 3072–3082 (2023). https://doi.org/10.1007/s00330-023-09453-y
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DOI: https://doi.org/10.1007/s00330-023-09453-y