Abstract
Purpose
To assess the efficacy of radiomics features obtained by T2-weighted sequences to predict clinical outcomes following liver resection in colorectal liver metastases patients.
Methods
This retrospective analysis was approved by the local Ethical Committee board and radiological databases were interrogated, from January 2018 to May 2021, to select patients with liver metastases with pathological proof and MRI study in pre-surgical setting. The cohort of patients included a training set and an external validation set. The internal training set included 51 patients with 61 years of median age and 121 liver metastases. The validation cohort consisted a total of 30 patients with single lesion with 60 years of median age. For each volume of interest, 851 radiomics features were extracted as median values using PyRadiomics. Nonparametric test, intraclass correlation, receiver operating characteristic (ROC) analysis, linear regression modelling and pattern recognition methods (support vector machine (SVM), k-nearest neighbours (KNN), artificial neural network (NNET) and decision tree (DT)) were considered.
Results
The best predictor to discriminate expansive versus infiltrative front of tumour growth was obtained by wavelet_LHL_gldm_DependenceNonUniformityNormalized with an accuracy of 82%; to discriminate high grade versus low grade or absent was the wavelet_LLH_glcm_Imc1 with accuracy of 88%; to differentiate the mucinous type of tumour was the wavelet_LLH_glcm_JointEntropy with accuracy of 92% while to identify tumour recurrence was the wavelet_LLL_glcm_Correlation with accuracy of 85%. Linear regression model increased the performance obtained with respect to the univariate analysis exclusively in the discrimination of expansive versus infiltrative front of tumour growth reaching an accuracy of 90%, a sensitivity of 95% and a specificity of 80%. Considering significant texture metrics tested with pattern recognition approaches, the best performance was reached by the KNN in the discrimination of the tumour budding considering the four textural predictors obtaining an accuracy of 93%, a sensitivity of 81% and a specificity of 97%.
Conclusions
Ours results confirmed the capacity of radiomics to identify as biomarkers, several prognostic features that could affect the treatment choice in patients with liver metastases, in order to obtain a more personalized approach.
Similar content being viewed by others
Data Availability
Data are available at the link https://zenodo.org/record/6374234#.YjjY3erMK3A.
References
Granata V, Fusco R, Avallone A, De Stefano A, Ottaiano A, Sbordone C, Brunese L, Izzo F, Petrillo A (2021) Radiomics-Derived Data by Contrast Enhanced Magnetic Resonance in RAS Mutations Detection in Colorectal Liver Metastases. Cancers (Basel) 25;13(3):453. doi: https://doi.org/10.3390/cancers13030453.
Granata V, Fusco R, Risi C, Ottaiano A, Avallone A, De Stefano A, Grimm R, Grassi R, Brunese L, Izzo F, Petrillo A (2020) Diffusion-Weighted MRI and Diffusion Kurtosis Imaging to Detect RAS Mutation in Colorectal Liver Metastasis. Cancers (Basel) 26;12(9):2420. doi: https://doi.org/10.3390/cancers12092420.
Granata V, Fusco R, Barretta ML, Picone C, Avallone A, Belli A, Patrone R, Ferrante M, Cozzi D, Grassi R, Grassi R, Izzo F, Petrillo A (2021) Radiomics in hepatic metastasis by colorectal cancer. Infect Agent Cancer 2;16(1):39. doi: https://doi.org/10.1186/s13027-021-00379-y.
Granata V, Fusco R, Costa M, Picone C, Cozzi D, Moroni C, La Casella GV, Montanino A, Monti R, Mazzoni F, Grassi R, Malagnino VG, Cappabianca S, Grassi R, Miele V, Petrillo A (2021). Preliminary Report on Computed Tomography Radiomics Features as Biomarkers to Immunotherapy Selection in Lung Adenocarcinoma Patients. Cancers (Basel) 7;13(16):3992. doi: https://doi.org/10.3390/cancers13163992. Fusco R, Piccirillo A, Sansone M, Granata V, Rubulotta MR, Petrosino T, Barretta ML, Vallone P, Di Giacomo R, Esposito E, Di Bonito M, Petrillo A (2021) Radiomics and Artificial Intelligence Analysis with Textural Metrics Extracted by Contrast-Enhanced Mammography in the Breast Lesions Classification. Diagnostics (Basel) 30;11(5):815. doi: https://doi.org/10.3390/diagnostics11050815.
Fusco R, Granata V, Mazzei MA, Meglio ND, Roscio DD, Moroni C, Monti R, Cappabianca C, Picone C, Neri E, Coppola F, Montanino A, Grassi R, Petrillo A, Miele V (2021) Quantitative imaging decision support (QIDS™) tool consistency evaluation and radiomic analysis by means of 594 metrics in lung carcinoma on chest CT scan. Cancer Control 28:1073274820985786. https://doi.org/10.1177/1073274820985786 PetraliaG, SummersPE, AgostiniA, AmbrosiniR, CianciR, CristelG, CalistriL, ColagrandeS (2020) Dynamiccontrast-enhancedMRIinoncology:howwedoit.RadiolMed125,1288-1300, https://doi.org/10.1007/s11547-020-01220-z
Ria F, Samei E (2020) Is regulatory compliance enough to ensure excellence in medicine? Radiol Med 125:904–905. https://doi.org/10.1007/s11547-020-01171-5
Zhang A, Song J, Ma Z, Chen T (2020) Combined dynamic contrast-enhanced magnetic resonance imaging and diffusion-weighted imaging to predict neoadjuvant chemotherapy effect in FIGO stage IB2-IIA2 cervical cancers. Radiol Med 125:1233–1242. https://doi.org/10.1007/s11547-020-01214-x
Crimì F, Capelli G, Spolverato G, Bao QR, Florio A, Milite Rossi S, Cecchin D, Albertoni L, Campi C, Pucciarelli S, Stramare R (2020) MRI T2-weighted sequences-based texture analysis (TA) as a predictor of response to neoadjuvant chemo-radiotherapy (nCRT) in patients with locally advanced rectal cancer (LARC). Radiol Med 125:1216–1224. https://doi.org/10.1007/s11547-020-01215-w
Kirienko M, Ninatti G, Cozzi L, Voulaz E, Gennaro N, Barajon I, Ricci F, Carlo-Stella C, Zucali P, Sollini M, Balzarini L, Chiti A (2020) Computed tomography (CT)-derived radiomic features differentiate prevascular mediastinum masses as thymic neoplasms versus lymphomas. Radiol Med 125:951–960. https://doi.org/10.1007/s11547-020-01188-w
Zhang L, Kang L, Li G, Zhang X, Ren J, Shi Z, Li J, Yu S (2020) Computed tomography-based radiomics model for discriminating the risk stratification of gastrointestinal stromal tumors. Radiol Med 125:465–473. https://doi.org/10.1007/s11547-020-01138-6
Gurgitano M, Angileri SA, Rodà GM, Liguori A, Pandolfi M, Ierardi AM, Wood BJ, Carrafiello G (2021) Interventional Radiology ex-machina: impact of Artificial Intelligence on practice. Radiol Med 126(7):998–1006. https://doi.org/10.1007/s11547-021-01351-x
Scapicchio C, Gabelloni M, Barucci A, Cioni D, Saba L, Neri E (2021) A deep look into radiomics. Radiol Med 126(10):1296–1311. https://doi.org/10.1007/s11547-021-01389-x
Wei J, Jiang H, Gu D, Niu M, Fu F, Han Y, Song B, Tian J (2020) Radiomics in liver diseases: Current progress and future opportunities. Liver Int Sep;40(9):2050–2063. doi: https://doi.org/10.1111/liv.14555.
Saini A, Breen I, Pershad Y, Naidu S, Knuttinen MG, Alzubaidi S, Sheth R, Albadawi H, Kuo M, Oklu R. Radiogenomics and Radiomics in Liver Cancers (2018) Diagnostics (Basel) 27;9(1):4. doi: https://doi.org/10.3390/diagnostics9010004.
de la Pinta C, Castillo ME, Collado M, Galindo-Pumariño C, Peña C (2021) Radiogenomics: Hunting Down Liver Metastasis in Colorectal Cancer Patients. Cancers (Basel) 5;13(21):5547. doi: https://doi.org/10.3390/cancers13215547.
Nardone V, Reginelli A, Grassi R, Boldrini L, Vacca G, D’Ippolito E, Annunziata S, Farchione A, Belfiore MP, Desideri I, Cappabianca S (2021) Delta radiomics: a systematic review. Radiol Med 126(12):1571–1583. https://doi.org/10.1007/s11547-021-01436-7
Brunese L, Brunese MC, Carbone M, Ciccone V, Mercaldo F, Santone A (2021) Automatic PI-RADS assignment by means of formal methods. Radiol Med. https://doi.org/10.1007/s11547-021-01431-y
van der Lubbe MFJA, Vaidyanathan A, de Wit M, van den Burg EL, Postma AA, Bruintjes TD, Bilderbeek-Beckers MAL, Dammeijer PFM, Bossche SV, Van Rompaey V, Lambin P, van Hoof M, van de Berg R (2021) A non-invasive, automated diagnosis of Menière’s disease using radiomics and machine learning on conventional magnetic resonance imaging: A multicentric, case-controlled feasibility study. Radiol Med. https://doi.org/10.1007/s11547-021-01425-w
Granata V, Fusco R, Avallone A, Cassata A, Palaia R, Delrio P, Grassi R, Tatangelo F, Grazzini G, Izzo F, Petrillo A (2020) Abbreviated MRI protocol for colorectal liver metastases: How the radiologist could work in pre surgical setting. PLoS One 19;15(11):e0241431. doi: https://doi.org/10.1371/journal.pone.0241431.
Granata V, Fusco R, Venanzio Setola S, Mattace Raso M, Avallone A, De Stefano A, Nasti G, Palaia R, Delrio P, Petrillo A, Izzo F (2019) Liver radiologic findings of chemotherapy-induced toxicity in liver colorectal metastases patients. Eur Rev Med Pharmacol Sci 23(22):9697–9706. https://doi.org/10.26355/eurrev_201911_19531
Granata V, Fusco R, Maio F, Avallone A, Nasti G, Palaia R, Albino V, Grassi R, Izzo F, Petrillo A (2019) Qualitative assessment of EOB-GD-DTPA and Gd-BT-DO3A MR contrast studies in HCC patients and colorectal liver metastases. Infect Agent Cancer 27(14):40. https://doi.org/10.1186/s13027-019-0264-3
Granata V, Fusco R, de Lutio di Castelguidone E, Avallone A, Palaia R, Delrio P, Tatangelo F, Botti G, Grassi R, Izzo F, Petrillo A, (2019) Diagnostic performance of gadoxetic acid-enhanced liver MRI versus multidetector CT in the assessment of colorectal liver metastases compared to hepatic resection. BMC Gastroenterol 19(1):129. https://doi.org/10.1186/s12876-019-1036-7
Zwanenburg A, Vallières M, Abdalah MA, Aerts HJWL, Andrearczyk V, Apte A, Ashrafinia S, Bakas S, Beukinga RJ, Boellaard R, Bogowicz M, Boldrini L, Buvat I, Cook GJR, Davatzikos C, Depeursinge A, Desseroit MC, Dinapoli N, Dinh CV, Echegaray S, El Naqa I, Fedorov AY, Gatta R, Gillies RJ, Goh V, Götz M, Guckenberger M, Ha SM, Hatt M, Isensee F, Lambin P, Leger S, Leijenaar RTH, Lenkowicz J, Lippert F, Losnegård A, Maier-Hein KH, Morin O, Müller H, Napel S, Nioche C, Orlhac F, Pati S, Pfaehler EAG, Rahmim A, Rao AUK, Scherer J, Siddique MM, Sijtsema NM, Socarras Fernandez J, Spezi E, Steenbakkers RJHM, Tanadini-Lang S, Thorwarth D, Troost EGC, Upadhaya T, Valentini V, van Dijk LV, van Griethuysen J, van Velden FHP, Whybra P, Richter C, Löck S (2020) The Image Biomarker Standardization Initiative: Standardized Quantitative Radiomics for High-Throughput Im-age-based Phenotyping. Radiology 295:328–338. https://doi.org/10.1148/radiol.2020191145
Granata V, Fusco R, Avallone A, Catalano O, Piccirillo M, Palaia R, Nasti G, Petrillo A, Izzo F (2018) A radiologist’s point of view in the presurgical and intraoperative setting of colorectal liver metastases. Future Oncol 14(21):2189–2206. https://doi.org/10.2217/fon-2018-0080
Granata V, Fusco R, Catalano O, Avallone A, Palaia R, Botti G, Tatangelo F, Granata F, Cascella M, Izzo F, Petrillo A (2017) Diagnostic accuracy of magnetic resonance, computed tomography and contrast enhanced ultrasound in radiological multimodality assessment of peribiliary liver metastases. PLoS ONE 12(6):e0179951. https://doi.org/10.1371/journal.pone.0179951
Granata V, Fusco R, Catalano O, Filice S, Amato DM, Nasti G, Avallone A, Izzo F, Petrillo A (2015) Early Assessment of Colorectal Cancer Patients with Liver Metastases Treated with Antiangiogenic Drugs: The Role of Intravoxel Incoherent Motion in Diffusion-Weighted Imaging. PLoS ONE 10(11):e0142876. https://doi.org/10.1371/journal.pone.0142876
Beckers RCJ, Trebeschi S, Maas M, Schnerr RS, Sijmons JML, Beets GL, Houwers JB, Beets-Tan RGH, Lambregts DMJ (2018) CT texture analysis in colorectal liver metastases and the surrounding liver parenchyma and its potential as an imaging biomarker of disease aggressiveness, response and survival. Eur J Radiol 102:15–21. https://doi.org/10.1016/j.ejrad.2018.02.031
Andersen IR, Thorup K, Andersen MB, Olesen R, Mortensen FV, Nielsen DT, Rasmussen F (2019) Texture in the monitoring of regorafenib therapy in patients with colorectal liver metastases. Acta Radiol 60(9):1084–1093. https://doi.org/10.1177/0284185118817940
Zhang H, Li W, Hu F, Sun Y, Hu T, Tong T (2019) MR texture analysis: potential imaging biomarker for predicting the chemotherapeutic response of patients with colorectal liver metastases. Abdom Radiol (NY) 44(1):65–71. https://doi.org/10.1007/s00261-018-1682-1
Lubner MG, Stabo N, Lubner SJ, del Rio AM, Song C, Halberg RB, Pickhardt PJ (2015) CT textural analysis of hepatic metastatic colorectal cancer: pre-treatment tumor heterogeneity correlates with pathology and clinical outcomes. Abdom Imaging 40(7):2331–2337. https://doi.org/10.1007/s00261-015-0438-4
Simpson AL, Doussot A, Creasy JM, Adams LB, Allen PJ, DeMatteo RP, Gönen M, Kemeny NE, Kingham TP, Shia J, Jarnagin WR, Do RKG, D’Angelica MI (2017) Computed Tomography Image Texture: A Noninvasive Prognostic Marker of Hepatic Recurrence After Hepatectomy for Metastatic Colorectal Cancer. Ann Surg Oncol 24(9):2482–2490. https://doi.org/10.1245/s10434-017-5896-1
Ganeshan B, Miles KA, Young RC, Chatwin CR. Hepatic enhancement in colorectal cancer: texture analysis correlates with hepatic hemodynamics and patient survival (2007) Acad Radiol 14(12):1520–30. doi: https://doi.org/10.1016/j.acra.2007.06.028.
Rahmim A, Bak-Fredslund KP, Ashrafinia S, Lu L, Schmidtlein CR, Subramaniam RM, Morsing A, Keiding S, Horsager J, Munk OL (2019) Prognostic modeling for patients with colorectal liver metastases incorporating FDG PET radiomic features. Eur J Radiol 113:101–109. https://doi.org/10.1016/j.ejrad.2019.02.006
Dercle L, Lu L, Schwartz LH, Qian M, Tejpar S, Eggleton P, Zhao B, Piessevaux H (2020) Radiomics Response Signature for Identification of Metastatic Colorectal Cancer Sensitive to Therapies Targeting EGFR Pathway. J Natl Cancer Inst 112:902–912. https://doi.org/10.1093/jnci/djaa017
Ravanelli M, Agazzi GM, Tononcelli E, Roca E, Cabassa P, Baiocchi G, Berruti A, Maroldi R (2019) Farina D (2019) Texture features of colorectal liver metastases on pretreatment contrast-enhanced CT may predict response and prognosis in patients treated with bevacizumab-containing chemotherapy: a pilot study including comparison with standard chemotherapy. Radiol Med 124(9):877–886. https://doi.org/10.1007/s11547-019-01046-4
Taghavi M, Staal FC, Simões R, Hong EK, Lambregts DM, van der Heide UA, Beets-Tan RG, Maas M (2021) CT radiomics models are unable to predict new liver metastasis after successful thermal ablation of colorectal liver metastases. Acta Radiol 17:2841851211060437. https://doi.org/10.1177/02841851211060437
Rizzetto F, Calderoni F, De Mattia C, Defeudis A, Giannini V, Mazzetti S, Vassallo L, Ghezzi S, Sartore-Bianchi A, Marsoni S, Siena S, Regge D, Torresin A, Vanzulli A (2020) Impact of inter-reader contouring variability on textural radiomics of colorectal liver metastases. Eur. Radiol. Exp 10;4(1):62. doi: https://doi.org/10.1186/s41747-020-00189-8.
Coppola F, Giannini V, Gabelloni M, Panic J, Defeudis A, Lo Monaco S, Cattabriga A, Cocozza MA, Pastore LV, Polici M, Caruso D, Laghi A, Regge D, Neri E, Golfieri R, Faggioni L (2021) Radiomics and Magnetic Resonance Imaging of Rectal Cancer: From Engineering to Clinical Practice. Diagnostics (Basel) 11(5):756. https://doi.org/10.3390/diagnostics11050756
Esposito A, Buscarino V, Raciti D, Casiraghi E, Manini M, Biondetti P, Forzenigo L (2020) Characterization of liver nodules in patients with chronic liver disease by MRI: performance of the Liver Imaging Reporting and Data System (LI-RADS vol 2018) scale and its comparison with the Likert scale. Radiol Med 125(1):15–23. https://doi.org/10.1007/s11547-019-01092-y
Bozkurt M, Eldem G, Bozbulut UB, Bozkurt MF, Kılıçkap S, Peynircioğlu B, Çil B, Lay Ergün E, Volkan–Salanci B (2021) Factors affecting the response to Y-90 microsphere therapy in the cholangiocarcinoma patients. Radiol Med 126(2):323–333. https://doi.org/10.1007/s11547-020-01240-9
Granata V, Grassi R, Fusco R, Setola SV, Belli A, Ottaiano A, Nasti G, La Porta M, Danti G, Cappabianca S, Cutolo C, Petrillo A (2021) Izzo F (2021) Intrahepatic cholangiocarcinoma and its differential diagnosis at MRI: how radiologist should assess MR features. Radiol Med 126(12):1584–1600. https://doi.org/10.1007/s11547-021-01428-7
Cusumano D, Meijer G, Lenkowicz J, Chiloiro G, Boldrini L, Masciocchi C, Dinapoli N, Gatta R, Casà C, Damiani A, Barbaro B, Gambacorta MA, Azario L, De Spirito M, Intven M, Valentini V (2021) A field strength independent MR radiomics model to predict pathological complete response in locally advanced rectal cancer. Radiol Med 126(3):421–429. https://doi.org/10.1007/s11547-020-01266-z
Bertocchi E, Barugola G, Nicosia L, Mazzola R, Ricchetti F, Dell’Abate P, Alongi F, Ruffo G (2020) A comparative analysis between radiation dose intensification and conventional fractionation in neoadjuvant locally advanced rectal cancer: a monocentric prospective observational study. Radiol Med 125:990–998. https://doi.org/10.1007/s11547-020-01189-9
Fornell-Perez R, Vivas-Escalona V, Aranda-Sanchez J, Gonzalez-Dominguez MC, Rubio-Garcia J, Aleman-Flores P, Lozano-Rodriguez A, Porcel-de-Peralta G, Loro-Ferrer JF (2020) Primary and post-chemoradiotherapy MRI detection of extramural venous invasion in rectal cancer: the role of diffusion-weighted imaging. Radiol Med 125(6):522–530. https://doi.org/10.1007/s11547-
Schicchi N, Fogante M, Palumbo P, Agliata G, Esposto Pirani P, Di Cesare E, Giovagnoni A (2020) The sub-millisievert era in CTCA: the technical basis of the new radiation dose approach. Radiol Med 125(11):1024020–01137–7.
Park SH, Kim YS, Choi J. Dosimetric analysis of the effects of a temporary tissue expander on the radiotherapy technique. Radiol Med 126(3):437–444. doi: https://doi.org/10.1007/s11547-020-01297-6.
Acknowledgements
The authors are grateful to Alessandra Trocino, librarian at the National Cancer Institute of Naples, Italy. Moreover, for the collaboration, authors are grateful for the research support to Paolo Pariate, Martina Totaro and Andrea Esposito of Radiology Division, “Istituto Nazionale Tumori IRCCS Fondazione Pascale – IRCCS di Napoli”, Naples, I-80131, Italy
Funding
The authors have not disclosed any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No conflicts of interest.
Research involving human participants and/or animals
The research was conducted in accordance with the principles embodied in the Declaration of Helsinki and in accordance with local statutory requirements.
Informed consent
Local Ethical Committee board accepted this retrospective study renouncing to the patient consent signature for nature of the study.
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
Granata, V., Fusco, R., De Muzio, F. et al. Radiomics textural features by MR imaging to assess clinical outcomes following liver resection in colorectal liver metastases. Radiol med 127, 461–470 (2022). https://doi.org/10.1007/s11547-022-01477-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11547-022-01477-6