Abstract
Objective
This study evaluates the ability of several machine learning (ML) algorithms, developed using volumetric and texture data extracted from baseline 18F-FDG PET/CT studies performed initial staging of patient with esophageal cancer (EC), to predict survival and histopathology.
Methods
The initial staging 18F-FDG PET/CT images obtained on newly diagnosed EC patients between January 2008 and June 2019 were evaluated using LIFEx software. A region of interest (ROI) of the primary tumor was created and volumetric and textural features were obtained. A significant relationship between these features and pathological subtypes, 1-year, and 5-year survival was investigated. Due to the nonhomogeneity of the data, nonparametric test (The Mann–Whitney U test) was used for each feature, in pairwise comparisons of independent variables. A p value of < 0.05 was considered significant. Receiver operating curve (ROC) analysis was performed for features with p < 0.05. Correlation between the significant features was evaluated with Spearman correlation test; features with correlation coefficient < 0.8 were evaluated with several ML algorithms.
Results
In predicting survival in a 1-year follow-up J48 was obtained as the most successful algorithm (AUC: 0.581, PRC: 0.565, MCC: 0.258, acc: 64.29%). 5-year survival results were more promising than 1-year survival results with (AUC: 0.820, PRC: 0.860, MCC: 271, acc: 81.36%) by logistic regression. It is revealed that the most successful algorithm was naive bayes (AUC: 0.680 PRC: 0.776, MCC: 0.298, acc: 82.66%) in the histopathological discrimination.
Conclusion
Texture analysis with ML algorithms could be predictive of overall survival and discriminating histopathological subtypes of EC.
Similar content being viewed by others
References
Thrumurthy SG, Chaudry MA, Thrumurthy SSD, Mughal M. Oesophageal cancer: risks, prevention, and diagnosis. BMJ. 2019;366:l4373.
Martin-Richard M, DíazBeveridge R, Arrazubi V, Alsina M, Galan Guzmán M, Custodio AB, et al. SEOM Clinical Guideline for the diagnosis and treatment of esophageal cancer. Clin Transl Oncol. 2016;18:1179–86.
Bedard PL, Hansen AR, Ratain MJ, Siu LL. Tumour heterogeneity in the clinic. Nature. 2013;501:355–64.
Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, et al. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6.
Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2016;278:563–77.
Kim SJ, Pak K, Chang S. Determination of regional lymph node status using 18F-FDG PET/CT parameters in oesophageal cancer patients: comparison of SUV, volumetric parameters and intratumoral heterogeneity. Br J Radiol. 2016;89:20150673.
Coroller TP, Agrawal V, Huynh E, Narayan V, Lee SW, Mak RH, et al. Radiomic-based pathological response prediction from primary tumors and lymph nodes in NSCLC. J Thorac Oncol. 2017;12:467–76.
Orlhac F, Soussan M, Maisonobe JA, Garcia CA, Vanderlinden B, Buvat I. Tumor texture analysis in 18F-FDG PET: relationships between texture parameters, histogram indices, standardized uptake values, metabolic volumes, and total lesion glycolysis. J Nucl Med. 2014;55:414–22.
Hatt M, Majdoub M, Vallières M, Tixier F, Le Rest CC, Groheux D, et al. 18F-FDG PET uptake characterization through texture analysis: investigating the complementary nature of heterogeneity and functional tumor volume in a multi-cancer site patient cohort. J Nucl Med. 2015;56:38–44.
van Rossum PS, Fried DV, Zhang L, Hofstetter WL, van Vulpen M, Meijer GJ, Court LE, et al. The incremental value of subjective and quantitative assessment of 18F-FDG PET for the prediction of pathologic complete response to preoperative chemoradiotherapy in esophageal cancer. J Nucl Med. 2016;57:691–700.
Wheeler JM, Warren BF, Mortensen NJ, Ekanyaka N, Kulacoglu H, Jones AC, et al. Quantification of histologic regression of rectal cancer after irradiation: a proposal for a modified staging system. Dis Colon Rectum. 2002;45:1051–6.
Nioche C, Orlhac F, Boughdad S, Reuze S, Goya-Outi J, Robert C, et al. LIFEx: a freeware for radiomic feature calculation in multimodality imaging to accelerate advances in the characterization of tumor heterogeneity. Cancer Res. 2018;78:4786–9.
Orlhac F, Thézé B, Soussan M, Boisgard R, Buvat I. Multiscale texture analysis: from 18F-FDG PET images to histologic images. J Nucl Med. 2016;57:1823–8.
Saito T, Rehmsmeier M. The precision-recall plot is more informative than the ROC plot when evaluating binary classifiers on imbalanced datasets. PLoS ONE. 2015;10:e0118432.
Foley KG, Hills RK, Berthon B, Marshall C, Parkinson C, Lewis WG, et al. Development and validation of a prognostic model incorporating texture analysis derived from standardised segmentation of PET in patients with oesophageal cancer. Eur Radiol. 2018;28:428–36.
Cao Q, Li Y, Li Z, An D, Li B, Lin Q. Development and validation of a radiomics signature on differentially expressed features of 18F-FDG PET to predict treatment response of concurrent chemoradiotherapy in thoracic esophagus squamous cell carcinoma. Radiother Oncol. 2020;146:9–15.
Zhang C, Shi Z, Kalendralis P, Whybra P, Parkinson C, Berbee M, et al. Prediction of lymph node metastases using pre-treatment PET radiomics of the primary tumour in esophageal adenocarcinoma: an external validation study. Br J Radiol. 2021;94:20201042.
Beukinga RJ, Hulshoff JB, Mul VEM, Noordzij W, Kats-Ugurlu G, Slart RHJA, et al. Prediction of response to neoadjuvant chemotherapy and radiation therapy with baseline and restaging 18F-FDG PET imaging biomarkers in patients with esophageal cancer. Radiology. 2018;287:983–92.
Tan S, Kligerman S, Chen W, Lu M, Kim G, Feigenberg S, et al. Spatial-temporal 18F-FDG-PET features for predicting pathologic response of esophageal cancer to neoadjuvant chemoradiation therapy. Int J Radiat Oncol Biol Phys. 2013;85:1375–82.
Nakajo M, Jinguji M, Nakabeppu Y, Nakajo M, Higashi R, Fukukura Y, et al. Texture analysis of 18F-FDG PET/CT to predict tumour response and prognosis of patients with esophageal cancer treated by chemoradiotherapy. Eur J Nucl Med Mol Imaging. 2017;44:206–14.
Paul D, Su R, Romain M, Sébastien V, Pierre V, Isabelle G. Feature selection for outcome prediction in oesophageal cancer using genetic algorithm and random forest classifier. Comput Med Imaging Graph. 2017;60:42–9.
Yip SS, Coroller TP, Sanford NN, Mamon H, Aerts HJ, Berbeco RI. Relationship between the temporal changes in positron-emission-tomography-imaging-based textural features and pathologic response and survival in esophageal cancer patients. Front Oncol. 2016;6:72.
Zhang YH, Herlin G, Rouvelas I, Nilsson M, Lundell L, Brismar TB. Texture analysis of computed tomography data using morphologic and metabolic delineation of esophageal cancer-relation to tumor type and neoadjuvant therapy response. Dis Esophagus. 2019;32:doy096.
DomperArnal MJ, Ferrández Arenas Á, Lanas AÁ. Esophageal cancer: risk factors, screening and endoscopic treatment in Western and Eastern countries. World J Gastroenterol. 2015;21:7933–43.
Cook GJR, Azad G, Owczarczyk K, Owczarczyk K, Siddique M, Goh V. Challenges and promises of PET radiomics. Int J Radiat Oncol Biol Phys. 2018;102:1083–9.
Ha S, Choi H, Paeng JC, Cheon GJ. Radiomics in oncological PET/CT: a methodological overview. Nucl Med Mol Imaging. 2019;53:14–29.
Hatt M, Tixier F, Pierce L, Kinahan PE, Le Rest CC, Visvikis D. Characterization of PET/CT images using texture analysis: the past, the present… any future? Eur J Nucl Med Mol Imaging. 2017;44:151–65.
Liberini V, De Santi B, Rampado O, Gallio E, Dionisi B, Ceci F, et al. Impact of segmentation and discretization on radiomic features in 68Ga-DOTA-TOC PET/CT images of neuroendocrine tumor. EJNMMI Phys. 2021;8:21.
Belli ML, Mori M, Broggi S, Cattaneo GM, Bettinardi V, Dell’Oca I, et al. Quantifying the robustness of 18F-FDG-PET/CT radiomic features with respect to tumor delineation in head and neck and pancreatic cancer patients. Phys Med. 2018;49:105–11.
Leijenaar RT, Carvalho S, Velazquez ER, van Elmpt WJ, Parmar C, Hoekstra OS, et al. Stability of FDG-PET Radiomics features: an integrated analysis of test-retest and inter-observer variability. Acta Oncol. 2013;52:1391–7.
Acknowledgements
The authors declared that there is no conflict of interest concerning this manuscript. This study did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Funding
The authors received no financial support for the research and/or authorship of this article.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No potential conflicts of interest were disclosed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Karahan Şen, N.P., Aksu, A. & Çapa Kaya, G. A different overview of staging PET/CT images in patients with esophageal cancer: the role of textural analysis with machine learning methods. Ann Nucl Med 35, 1030–1037 (2021). https://doi.org/10.1007/s12149-021-01638-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12149-021-01638-z