MRI radiomics in head and neck cancer from reproducibility to combined approaches.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
24 Apr 2024
Historique:
received: 30 12 2023
accepted: 17 04 2024
medline: 25 4 2024
pubmed: 25 4 2024
entrez: 24 4 2024
Statut: epublish

Résumé

The clinical applicability of radiomics in oncology depends on its transferability to real-world settings. However, the absence of standardized radiomics pipelines combined with methodological variability and insufficient reporting may hamper the reproducibility of radiomic analyses, impeding its translation to clinics. This study aimed to identify and replicate published, reproducible radiomic signatures based on magnetic resonance imaging (MRI), for prognosis of overall survival in head and neck squamous cell carcinoma (HNSCC) patients. Seven signatures were identified and reproduced on 58 HNSCC patients from the DB2Decide Project. The analysis focused on: assessing the signatures' reproducibility and replicating them by addressing the insufficient reporting; evaluating their relationship and performances; and proposing a cluster-based approach to combine radiomic signatures, enhancing the prognostic performance. The analysis revealed key insights: (1) despite the signatures were based on different features, high correlations among signatures and features suggested consistency in the description of lesion properties; (2) although the uncertainties in reproducing the signatures, they exhibited a moderate prognostic capability on an external dataset; (3) clustering approaches improved prognostic performance compared to individual signatures. Thus, transparent methodology not only facilitates replication on external datasets but also advances the field, refining prognostic models for potential personalized medicine applications.

Identifiants

pubmed: 38658630
doi: 10.1038/s41598-024-60009-6
pii: 10.1038/s41598-024-60009-6
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

9451

Subventions

Organisme : National Plan for NRRP Complementary Investments
ID : PNC0000003

Informations de copyright

© 2024. The Author(s).

Références

Bray, F. et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA. Cancer J. Clin. 68, 394–424 (2018).
doi: 10.3322/caac.21492 pubmed: 30207593
Mody, M. D., Rocco, J. W., Yom, S. S., Haddad, R. I. & Saba, N. F. Head and neck cancer. Lancet 398, 2289–2299 (2021).
doi: 10.1016/S0140-6736(21)01550-6 pubmed: 34562395
Machiels, J.-P. et al. Squamous cell carcinoma of the oral cavity, larynx, oropharynx and hypopharynx: EHNS–ESMO–ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 31, 1462–1475 (2020).
doi: 10.1016/j.annonc.2020.07.011 pubmed: 33239190
Zanoni, D. K., Patel, S. G. & Shah, J. P. Changes in the 8th Edition of the American Joint Committee on Cancer (AJCC) staging of head and neck cancer: Rationale and implications. Curr. Oncol. Rep. 21, 52 (2019).
doi: 10.1007/s11912-019-0799-x pubmed: 30997577 pmcid: 6528815
Bera, K., Braman, N., Gupta, A., Velcheti, V. & Madabhushi, A. Predicting cancer outcomes with radiomics and artificial intelligence in radiology. Nat. Rev. Clin. Oncol. 19, 132–146 (2022).
doi: 10.1038/s41571-021-00560-7 pubmed: 34663898
Bruixola, G. et al. Radiomics and radiogenomics in head and neck squamous cell carcinoma: Potential contribution to patient management and challenges. Cancer Treat. Rev. 99, 102263 (2021).
doi: 10.1016/j.ctrv.2021.102263 pubmed: 34343892
Tanadini-Lang, S. et al. Radiomic biomarkers for head and neck squamous cell carcinoma. Strahlenther. Onkol. 196, 868–878 (2020).
doi: 10.1007/s00066-020-01638-4 pubmed: 32495038
Peng, Z. et al. Application of radiomics and machine learning in head and neck cancers. Int. J. Biol. Sci. 17, 475–486 (2021).
doi: 10.7150/ijbs.55716 pubmed: 33613106 pmcid: 7893590
Tortora, M. et al. Radiomics applications in head and neck tumor imaging: A narrative review. Cancers Basel. 15, 1174 (2023).
doi: 10.3390/cancers15041174 pubmed: 36831517 pmcid: 9954362
Pfaehler, E. et al. A systematic review and quality of reporting checklist for repeatability and reproducibility of radiomic features. Phys. Imaging Radiat. Oncol. 20, 69–75 (2021).
doi: 10.1016/j.phro.2021.10.007 pubmed: 34816024 pmcid: 8591412
Traverso, A., Wee, L., Dekker, A. & Gillies, R. Repeatability and reproducibility of radiomic features: A systematic review. Int. J. Radiat. Oncol. Biol. Phys. 102, 1143–1158 (2018).
doi: 10.1016/j.ijrobp.2018.05.053 pubmed: 30170872 pmcid: 6690209
Zwanenburg, A. et al. The image biomarker standardization initiative: Standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology 295, 328–338 (2020).
doi: 10.1148/radiol.2020191145 pubmed: 32154773
Collins, G. S., Reitsma, J. B., Altman, D. G. & Moons, K. G. M. Transparent reporting of a multivariable prediction model for individual prognosis or diagnosis (TRIPOD): The TRIPOD statement. BMJ 350, g7594 (2015).
doi: 10.1136/bmj.g7594 pubmed: 25569120
Clark, K. et al. The Cancer Imaging Archive (TCIA): Maintaining and operating a public information repository. J. Digit. Imaging 26, 1045–1057 (2013).
doi: 10.1007/s10278-013-9622-7 pubmed: 23884657 pmcid: 3824915
Lambin, P. et al. Radiomics: The bridge between medical imaging and personalized medicine. Nat. Rev. Clin. Oncol. 14, 749–762 (2017).
doi: 10.1038/nrclinonc.2017.141 pubmed: 28975929
Park, J. E. et al. Quality of science and reporting of radiomics in oncologic studies: Room for improvement according to radiomics quality score and TRIPOD statement. Eur. Radiol. 30, 523–536 (2020).
doi: 10.1007/s00330-019-06360-z pubmed: 31350588
Cavalieri, S. et al. Development of a multiomics database for personalized prognostic forecasting in head and neck cancer: The Big Data to Decide EU Project. Head Neck 43, 601–612 (2021).
doi: 10.1002/hed.26515 pubmed: 33107152
Corti, A. et al. MRI-based radiomic prognostic signature for locally advanced oral cavity squamous cell carcinoma: Development, testing and comparison with genomic prognostic signatures. Biomark. Res. 11, 69 (2023).
doi: 10.1186/s40364-023-00494-5 pubmed: 37455307 pmcid: 10350277
Bologna, M. et al. Prognostic radiomic signature for head and neck cancer: Development and validation on a multi-centric MRI dataset. Radiother. Oncol. J. Eur. Soc. Ther. Radiol. Oncol. 183, 109638 (2023).
doi: 10.1016/j.radonc.2023.109638
Jung, F., Steger, S., Knapp, O., Noll, M. & Wesarg, S. COSMO—coupled shape model for radiation therapy planning of head and neck cancer. In Clinical Image-Based Procedures. Translational Research in Medical Imaging. CLIP 2014. Lecture Notes in Computer Science (ed. Linguraru, M. et al.) 25–32 (Springer, 2014).
Tustison, N. J., Cook, P. A. & Gee, J. C. N4ITK: Improved N3 bias correction. IEEE Trans. Med. Imaging 29, 1310–1320 (2010).
doi: 10.1109/TMI.2010.2046908 pubmed: 20378467 pmcid: 3071855
Leijenaar, R. T. et al. Development and validation of a radiomic signature to predict HPV (p16) status from standard CT imaging: A multicenter study. Br. J. Radiol. 91, 20170498 (2018).
doi: 10.1259/bjr.20170498 pubmed: 29451412 pmcid: 6223271
Pyradiomics features description. Available online: https://pyradiomics.readthedocs.io/en/v3.1.0/features.html .
van Griethuysen, J. J. M. et al. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 77, e104–e107 (2017).
doi: 10.1158/0008-5472.CAN-17-0339 pubmed: 29092951 pmcid: 5672828
Kaplan, E. L. & Meier, P. Nonparametric estimation from incomplete samples. J. Am. Stat. Assoc. 73, 457–481 (1958).
doi: 10.1080/01621459.1958.10501452
Peto, R. & Peto, J. Asymptotically efficient rank invariant test procedures. J. R. Stat. Soc. 135, 185–207 (1972).
Harrell, F. E., Kerry, L. L. & Mark, D. B. Tutorial in biostatistics multivariable prognostic models: Issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat. Med. 15, 361–387 (1996).
doi: 10.1002/(SICI)1097-0258(19960229)15:4<361::AID-SIM168>3.0.CO;2-4 pubmed: 8668867
Park, H.-S. & Jun, C.-H. A simple and fast algorithm for K-medoids clustering. Expert Syst. Appl. 36, 3336–3341 (2009).
doi: 10.1016/j.eswa.2008.01.039
Bos, P. et al. Improved outcome prediction of oropharyngeal cancer by combining clinical and MRI features in machine learning models. Eur. J. Radiol. 139, 109701 (2021).
doi: 10.1016/j.ejrad.2021.109701 pubmed: 33865064
Chen, J. et al. An MRI-based radiomics-clinical nomogram for the overall survival prediction in patients with hypopharyngeal squamous cell carcinoma: A multi-cohort study. Eur. Radiol. 32, 1548–1557 (2022).
doi: 10.1007/s00330-021-08292-z pubmed: 34665315
Alfieri, S. et al. Prognostic role of pre-treatment magnetic resonance imaging (MRI)-based radiomic analysis in effectively cured head and neck squamous cell carcinoma (HNSCC) patients. Acta Oncol. 60, 1192–1200 (2021).
doi: 10.1080/0284186X.2021.1924401 pubmed: 34038324
Siow, T. Y. et al. MRI radiomics for predicting survival in patients with locally advanced hypopharyngeal cancer treated with concurrent chemoradiotherapy. Cancers Basel. 14, 6119 (2022).
doi: 10.3390/cancers14246119 pubmed: 36551604 pmcid: 9775984
Mossinelli, C. et al. The role of radiomics in tongue cancer: A new tool for prognosis prediction. Head Neck 45, 849–861 (2023).
doi: 10.1002/hed.27299 pubmed: 36779382
Lawrence, M. S. et al. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature 517, 576–582 (2015).
doi: 10.1038/nature14129
Tonella, L., Giannoccaro, M., Alfieri, S., Canevari, S. & De Cecco, L. Gene expression signatures for head and neck cancer patient stratification: Are results ready for clinical application?. Curr. Treat. Options Oncol. 18, 32 (2017).
doi: 10.1007/s11864-017-0472-2 pubmed: 28474265
Sun, F., Sun, J. & Zhao, Q. A deep learning method for predicting metabolite-disease associations via graph neural network. Brief. Bioinform. 23, 4 (2022).
doi: 10.1093/bib/bbac266
Liu, Z. et al. Radiogenomics: A key component of precision cancer medicine. Br. J. Cancer 129, 741–753 (2023).
doi: 10.1038/s41416-023-02317-8 pubmed: 37414827
Li, X. et al. Caspase-1 and gasdermin D afford the optimal targets with distinct switching strategies in NLRP1b inflammasome-induced cell death. Res. Washington, D. C. 2022, 9838341 (2022).
Philip, M. M., Welch, A., McKiddie, F. & Nath, M. A systematic review and meta-analysis of predictive and prognostic models for outcome prediction using positron emission tomography radiomics in head and neck squamous cell carcinoma patients. Cancer Med. 12, 16181–16194 (2023).
doi: 10.1002/cam4.6278 pubmed: 37353996 pmcid: 10469753
Li, L. et al. A meta-analysis of MRI-based radiomic features for predicting lymph node metastasis in patients with cervical cancer. Eur. J. Radiol. 151, 110243 (2022).
doi: 10.1016/j.ejrad.2022.110243 pubmed: 35366583
Spadarella, G. et al. Systematic review of the radiomics quality score applications: An EuSoMII Radiomics Auditing Group Initiative. Eur. Radiol. 33, 1884–1894 (2023).
doi: 10.1007/s00330-022-09187-3 pubmed: 36282312

Auteurs

Anna Corti (A)

Department of Electronics, Information and Bioengineering, Politecnico di Milano, Via Ponzio 34/5, 20133, Milan, Italy. anna.corti@polimi.it.

Stefano Cavalieri (S)

Head and Neck Medical Oncology Department, Fondazione IRCCS, Istituto Nazionale dei Tumori, Milan, Italy.
Department of Oncology and Hemato-Oncology, Università degli studi di Milano, Milan, Italy.

Giuseppina Calareso (G)

Radiology Department, Fondazione IRCCS, Istituto Nazionale dei Tumori, Milan, Italy.

Davide Mattavelli (D)

Unit of Otorhinolaryngology-Head and Neck Surgery, Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, ASST Spedali Civili of Brescia, University of Brescia, Brescia, Italy.

Marco Ravanelli (M)

Unit of Radiology, Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, ASST Spedali Civili of Brescia, University of Brescia, Brescia, Italy.

Tito Poli (T)

Maxillo-Facial Surgery Division, Head and Neck Department, University Hospital of Parma, Parma, Italy.

Lisa Licitra (L)

Head and Neck Medical Oncology Department, Fondazione IRCCS, Istituto Nazionale dei Tumori, Milan, Italy.
Department of Oncology and Hemato-Oncology, Università degli studi di Milano, Milan, Italy.

Valentina D A Corino (VDA)

Department of Electronics, Information and Bioengineering, Politecnico di Milano, Via Ponzio 34/5, 20133, Milan, Italy.
Cardiotech Lab, Centro Cardiologico Monzino IRCCS, Milan, Italy.

Luca Mainardi (L)

Department of Electronics, Information and Bioengineering, Politecnico di Milano, Via Ponzio 34/5, 20133, Milan, Italy.

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