Radiomics of Intrahepatic Cholangiocarcinoma and Peritumoral Tissue Predicts Postoperative Survival: Development of a CT-Based Clinical-Radiomic Model.

Computed tomography Intrahepatic cholangiocarcinoma Liver surgery Peritumoral tissue Prognosis Radiomics Survival

Journal

Annals of surgical oncology
ISSN: 1534-4681
Titre abrégé: Ann Surg Oncol
Pays: United States
ID NLM: 9420840

Informations de publication

Date de publication:
26 May 2024
Historique:
received: 07 02 2024
accepted: 28 04 2024
medline: 27 5 2024
pubmed: 27 5 2024
entrez: 26 5 2024
Statut: aheadofprint

Résumé

For many tumors, radiomics provided a relevant prognostic contribution. This study tested whether the computed tomography (CT)-based textural features of intrahepatic cholangiocarcinoma (ICC) and peritumoral tissue improve the prediction of survival after resection compared with the standard clinical indices. All consecutive patients affected by ICC who underwent hepatectomy at six high-volume centers (2009-2019) were considered for the study. The arterial and portal phases of CT performed fewer than 60 days before surgery were analyzed. A manual segmentation of the tumor was performed (Tumor-VOI). A 5-mm volume expansion then was applied to identify the peritumoral tissue (Margin-VOI). The study enrolled 215 patients. After a median follow-up period of 28 months, the overall survival (OS) rate was 57.0%, and the progression-free survival (PFS) rate was 34.9% at 3 years. The clinical predictive model of OS had a C-index of 0.681. The addition of radiomic features led to a progressive improvement of performances (C-index of 0.71, including the portal Tumor-VOI, C-index of 0.752 including the portal Tumor- and Margin-VOI, C-index of 0.764, including all VOIs of the portal and arterial phases). The latter model combined clinical variables (CA19-9 and tumor pattern), tumor indices (density, homogeneity), margin data (kurtosis, compacity, shape), and GLRLM indices. The model had performance equivalent to that of the postoperative clinical model including the pathology data (C-index of 0.765). The same results were observed for PFS. The radiomics of ICC and peritumoral tissue extracted from preoperative CT improves the prediction of survival. Both the portal and arterial phases should be considered. Radiomic and clinical data are complementary and achieve a preoperative estimation of prognosis equivalent to that achieved in the postoperative setting.

Sections du résumé

BACKGROUND BACKGROUND
For many tumors, radiomics provided a relevant prognostic contribution. This study tested whether the computed tomography (CT)-based textural features of intrahepatic cholangiocarcinoma (ICC) and peritumoral tissue improve the prediction of survival after resection compared with the standard clinical indices.
METHODS METHODS
All consecutive patients affected by ICC who underwent hepatectomy at six high-volume centers (2009-2019) were considered for the study. The arterial and portal phases of CT performed fewer than 60 days before surgery were analyzed. A manual segmentation of the tumor was performed (Tumor-VOI). A 5-mm volume expansion then was applied to identify the peritumoral tissue (Margin-VOI).
RESULTS RESULTS
The study enrolled 215 patients. After a median follow-up period of 28 months, the overall survival (OS) rate was 57.0%, and the progression-free survival (PFS) rate was 34.9% at 3 years. The clinical predictive model of OS had a C-index of 0.681. The addition of radiomic features led to a progressive improvement of performances (C-index of 0.71, including the portal Tumor-VOI, C-index of 0.752 including the portal Tumor- and Margin-VOI, C-index of 0.764, including all VOIs of the portal and arterial phases). The latter model combined clinical variables (CA19-9 and tumor pattern), tumor indices (density, homogeneity), margin data (kurtosis, compacity, shape), and GLRLM indices. The model had performance equivalent to that of the postoperative clinical model including the pathology data (C-index of 0.765). The same results were observed for PFS.
CONCLUSIONS CONCLUSIONS
The radiomics of ICC and peritumoral tissue extracted from preoperative CT improves the prediction of survival. Both the portal and arterial phases should be considered. Radiomic and clinical data are complementary and achieve a preoperative estimation of prognosis equivalent to that achieved in the postoperative setting.

Identifiants

pubmed: 38797789
doi: 10.1245/s10434-024-15457-9
pii: 10.1245/s10434-024-15457-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Associazione Italiana per la Ricerca sul Cancro
ID : #2019-23822

Informations de copyright

© 2024. Society of Surgical Oncology.

Références

Banales JM, Cardinale V, Carpino G, et al. Expert consensus document: cholangiocarcinoma: current knowledge and future perspectives consensus statement from the European network for the study of cholangiocarcinoma (ENS-CCA). Nat Rev Gastroenterol Hepatol. 2016;13:261–80.
pubmed: 27095655 doi: 10.1038/nrgastro.2016.51
Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM. Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: systematic review and meta-analysis. JAMA Surg. 2014;149:565–74.
pubmed: 24718873 doi: 10.1001/jamasurg.2013.5137
Kelley RK, Bridgewater J, Gores GJ, Zhu AX. Systemic therapies for intrahepatic cholangiocarcinoma. J Hepatol. 2020;72:353–63.
pubmed: 31954497 doi: 10.1016/j.jhep.2019.10.009
Javle M, Roychowdhury S, Kelley RK, et al. Infigratinib (BGJ398) in previously treated patients with advanced or metastatic cholangiocarcinoma with FGFR2 fusions or rearrangements: mature results from a multicentre, open-label, single-arm, phase 2 study. Lancet Gastroenterol Hepatol. 2021;6:803–15.
pubmed: 34358484 doi: 10.1016/S2468-1253(21)00196-5
Mazzaferro V, Gorgen A, Roayaie S, Droz Dit Busset M, Sapisochin G. Liver resection and transplantation for intrahepatic cholangiocarcinoma. J Hepatol. 2020;72:364–77.
pubmed: 31954498 doi: 10.1016/j.jhep.2019.11.020
Torzilli G, Vigano L, Fontana A, et al. Oncological outcome of R1 vascular margin for mass-forming cholangiocarcinoma: a single-center observational cohort analysis. HPB Oxf. 2020;22:570–7.
doi: 10.1016/j.hpb.2019.08.015
Doussot A, Gonen M, Wiggers JK, et al. Recurrence patterns and disease-free survival after resection of intrahepatic cholangiocarcinoma: preoperative and postoperative prognostic models. J Am Coll Surg. 2016;223:493–505.
pubmed: 27296525 pmcid: 5003652 doi: 10.1016/j.jamcollsurg.2016.05.019
de Jong MC, Nathan H, Sotiropoulos GC, et al. Intrahepatic cholangiocarcinoma: an international multi-institutional analysis of prognostic factors and lymph node assessment. J Clin Oncol. 2011;29:3140–5.
pubmed: 21730269 doi: 10.1200/JCO.2011.35.6519
Conci S, Ruzzenente A, Vigano L, et al. Patterns of distribution of hepatic nodules (single, satellites or multifocal) in intrahepatic cholangiocarcinoma: prognostic impact after surgery. Ann Surg Oncol. 2018;25:3719–27.
pubmed: 30088126 doi: 10.1245/s10434-018-6669-1
Job S, Rapoud D, Dos Santos A, et al. Identification of four immune subtypes characterized by distinct composition and functions of tumor microenvironment in intrahepatic cholangiocarcinoma. Hepatology. 2020;72:965–81.
pubmed: 31875970 doi: 10.1002/hep.31092
Fabris L, Sato K, Alpini G, Strazzabosco M. The tumor microenvironment in cholangiocarcinoma progression. Hepatology. 2021;73(Suppl 1):75–85.
pubmed: 32500550 doi: 10.1002/hep.31410
Vigano L, Soldani C, Franceschini B, et al. Tumor-infiltrating lymphocytes and macrophages in intrahepatic cholangiocellular carcinoma. Impact on prognosis after complete surgery. J Gastrointest Surg. 2019;23:2216–24.
pubmed: 30843133 doi: 10.1007/s11605-019-04111-5
Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14:749–62.
pubmed: 28975929 doi: 10.1038/nrclinonc.2017.141
Sollini M, Antunovic L, Chiti A, Kirienko M. Towards clinical application of image mining: a systematic review on artificial intelligence and radiomics. Eur J Nucl Med Mol Imaging. 2019;46:2656–72.
pubmed: 31214791 pmcid: 6879445 doi: 10.1007/s00259-019-04372-x
Zwanenburg A, Vallieres M, Abdalah MA, et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology. 2020;295:328–38.
pubmed: 32154773 doi: 10.1148/radiol.2020191145
Fiz F, Vigano L, Gennaro N, et al. Radiomics of liver metastases: a systematic review. Cancers. 2020;12:2881.
pubmed: 33036490 pmcid: 7600822 doi: 10.3390/cancers12102881
Wakabayashi T, Ouhmich F, Gonzalez-Cabrera C, et al. Radiomics in hepatocellular carcinoma: a quantitative review. Hepatol Int. 2019;13:546–59.
pubmed: 31473947 doi: 10.1007/s12072-019-09973-0
Fiz F, Jayakody Arachchige VS, Gionso M, et al. Radiomics of biliary tumors: a systematic review of current evidence. Diagnostics. 2022;12:826.
pubmed: 35453878 pmcid: 9024804 doi: 10.3390/diagnostics12040826
Mosconi C, Cucchetti A, Bruno A, et al. Radiomics of cholangiocarcinoma on pretreatment CT can identify patients who would best respond to radioembolisation. Eur Radiol. 2020;30:4534–44.
pubmed: 32227266 doi: 10.1007/s00330-020-06795-9
Xu L, Wan Y, Luo C, et al. Integrating intratumoral and peritumoral features to predict tumor recurrence in intrahepatic cholangiocarcinoma. Phys Med Biol. 2021;66:125001.
doi: 10.1088/1361-6560/ac01f3
Park HJ, Park B, Park SY, et al. Preoperative prediction of postsurgical outcomes in mass-forming intrahepatic cholangiocarcinoma based on clinical, radiologic, and radiomics features. Eur Radiol. 2021;31:8638–48.
pubmed: 33890153 doi: 10.1007/s00330-021-07926-6
Yang Y, Zou X, Zhou W, et al. Multiparametric MRI-based radiomic signature for preoperative evaluation of overall survival in intrahepatic cholangiocarcinoma after partial hepatectomy. J Magn Reson Imaging. 2022;56:739–51.
pubmed: 35049076 doi: 10.1002/jmri.28071
Fiz F, Rossi N, Langella S, et al. Radiomic analysis of intrahepatic cholangiocarcinoma: non-invasive prediction of pathology data: a multicenter study to develop a clinical-radiomic model. Cancers. 2023;15:4204.
pubmed: 37686480 pmcid: 10486795 doi: 10.3390/cancers15174204
Nioche C, Orlhac F, Boughdad S, 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.
pubmed: 29959149 doi: 10.1158/0008-5472.CAN-18-0125
Baheti AD, Tirumani SH, Shinagare AB, et al. Correlation of CT patterns of primary intrahepatic cholangiocarcinoma at the time of presentation with the metastatic spread and clinical outcomes: retrospective study of 92 patients. Abdom Imaging. 2014;39:1193–201.
pubmed: 24869789 doi: 10.1007/s00261-014-0167-0
Amin MB, Edge SB, Greene FL, et al. AJCC cancer staging manual. vol 1024, Berlin: Springer; 2017.
Wienke A. Frailty models in survival analysis. 1st edn. London: Chapman and Hall/CRC; 2010.
doi: 10.1201/9781420073911
Jin KP, Sheng RF, Yang C, Zeng MS. Combined arterial and delayed enhancement patterns of MRI assist in prognostic prediction for intrahepatic mass-forming cholangiocarcinoma (IMCC). Abdom Radiol. 2022;47:640–50.
doi: 10.1007/s00261-021-03292-5
Vigano L, Branciforte B, Laurenti V, et al. The histopathological growth pattern of colorectal liver metastases impacts local recurrence risk and the adequate width of the surgical margin. Ann Surg Oncol. 2022;29:5515–24.
pubmed: 35687176 doi: 10.1245/s10434-022-11717-8
Fernández Moro C, Bozóky B, Gerling M. Growth patterns of colorectal cancer liver metastases and their impact on prognosis: a systematic review. BMJ Open Gastroenterol. 2018;5:e000217.
pubmed: 30073092 pmcid: 6067357 doi: 10.1136/bmjgast-2018-000217
Fiz F, Masci C, Costa G, et al. PET/CT-based radiomics of mass-forming intrahepatic cholangiocarcinoma improves prediction of pathology data and survival. Eur J Nucl Med Mol Imaging. 2022;49:3387–400.
pubmed: 35347437 doi: 10.1007/s00259-022-05765-1
Yugawa K, Itoh S, Iseda N, et al. Obesity is a risk factor for intrahepatic cholangiocarcinoma progression associated with alterations of metabolic activity and immune status. Sci Rep. 2021;11:5845.
pubmed: 33712681 pmcid: 7955092 doi: 10.1038/s41598-021-85186-6
Min JH, Kim YK, Choi SY, et al. Intrahepatic mass-forming cholangiocarcinoma: arterial enhancement patterns at MRI and prognosis. Radiology. 2019;290:691–9.
pubmed: 30620253 doi: 10.1148/radiol.2018181485
Jiao CY, Zhang H, Ji GW, et al. CT-based clinico-radiological nomograms for prognosis prediction in patients with intrahepatic mass-forming cholangiocarcinoma: a multi-institutional study. Eur Radiol. 2022;32:8326–38.
pubmed: 35708837 doi: 10.1007/s00330-022-08914-0
Fujita N, Asayama Y, Nishie A, et al. Mass-forming intrahepatic cholangiocarcinoma: enhancement patterns in the arterial phase of dynamic hepatic CT: correlation with clinicopathological findings. Eur Radiol. 2017;27:498–506.
pubmed: 27165138 doi: 10.1007/s00330-016-4386-3
Viganò L, Lleo A, Muglia R, et al. Intrahepatic cholangiocellular carcinoma with radiological enhancement patterns mimicking hepatocellular carcinoma. Updates Surg. 2020;72:413–21.
pubmed: 32323164 doi: 10.1007/s13304-020-00750-5
Nakanishi R, Oki E, Hasuda H, et al. Radiomics texture analysis for the identification of colorectal liver metastases sensitive to first-line oxaliplatin-based chemotherapy. Ann Surg Oncol. 2021;28:2975–85.
pubmed: 33454878 doi: 10.1245/s10434-020-09581-5
Viganò L, Ammirabile A, Zwanenburg A. Radiomics in liver surgery: defining the path toward clinical application. Updates Surg. 2023;75:1387–90.
pubmed: 37543527 doi: 10.1007/s13304-023-01620-6
Goldenholz DM, Sun H, Ganglberger W, Westover MB. Sample size analysis for machine learning clinical validation studies. Biomedicines. 2023;11:685.
pubmed: 36979665 pmcid: 10045793 doi: 10.3390/biomedicines11030685
Rajput D, Wang WJ, Chen CC. Evaluation of a decided sample size in machine learning applications. BMC Bioinform. 2023;24:48.
doi: 10.1186/s12859-023-05156-9
Bodalal Z, Trebeschi S, Nguyen-Kim TDL, Schats W, Beets-Tan R. Radiogenomics: bridging imaging and genomics. Abdom Radiol. 2019;44:1960–84.
doi: 10.1007/s00261-019-02028-w
Costa G, Cavinato L, Fiz F, et al. Mapping tumor heterogeneity via local entropy assessment: making biomarkers visible. J Digit Imaging. 2023;36:1038–48.
pubmed: 36849835 pmcid: 10287605 doi: 10.1007/s10278-023-00799-9
Gumbs AA, Croner R, Abu-Hilal M, et al. Surgomics and the artificial intelligence, radiomics, genomics, oncopathomics and surgomics (AiRGOS) project. Artif Intell Surg. 2023;3:180–5.
doi: 10.20517/ais.2023.24

Auteurs

Francesco Fiz (F)

Nuclear Medicine Unit, Department of Diagnostic Imaging, Ente Ospedaliero "Ospedali Galliera", Genoa, Italy.
Department of Nuclear Medicine and Clinical Molecular Imaging, University Hospital, Tübingen, Germany.

Noemi Rossi (N)

MOX Laboratory, Department of Mathematics, Politecnico di Milano, Milan, Italy.

Serena Langella (S)

Department of Digestive and Hepatobiliary Surgery, Mauriziano Umberto I Hospital, Turin, Italy.

Simone Conci (S)

Division of General and Hepatobiliary Surgery, Department of Surgical Sciences, Dentistry, Gynaecology and Pediatrics, University Hospital G.B. Rossi, University of Verona, Verona, Italy.

Matteo Serenari (M)

General Surgery and Transplant Unit, IRCCS, Azienda Ospedaliero-Universitaria di Bologna, Sant'Orsola-Malpighi Hospital, Bologna, Italy.
Department of Medical and Surgical Sciences, Alma Mater Studiorum, University of Bologna, Bologna, Italy.

Francesco Ardito (F)

Hepatobiliary Surgery Unit, A. Gemelli Hospital, Università Cattolica del Sacro Cuore, Rome, Italy.

Alessandro Cucchetti (A)

Department of Medical and Surgical Sciences, Alma Mater Studiorum, University of Bologna, Bologna, Italy.
Department of General Surgery, Morgagni-Pierantoni Hospital, Forlì, Italy.

Teresa Gallo (T)

Department of Radiology, Mauriziano Umberto I Hospital, Turin, Italy.

Giulia A Zamboni (GA)

Department of Radiology, University Hospital G.B. Rossi, University of Verona, Verona, Italy.

Cristina Mosconi (C)

Department of Radiology, IRCCS, Azienda Ospedaliero-Universitaria di Bologna, Sant'Orsola-Malpighi Hospital, Bologna, Italy.

Luca Boldrini (L)

Department of Radiology, Radiation Oncology and Hematology, Fondazione Policlinico Universitario "A. Gemelli" IRCCS, Rome, Italy.

Mariateresa Mirarchi (M)

Department of General Surgery, Morgagni-Pierantoni Hospital, Forlì, Italy.

Stefano Cirillo (S)

Department of Radiology, Mauriziano Umberto I Hospital, Turin, Italy.

Andrea Ruzzenente (A)

Division of General and Hepatobiliary Surgery, Department of Surgical Sciences, Dentistry, Gynaecology and Pediatrics, University Hospital G.B. Rossi, University of Verona, Verona, Italy.

Ilaria Pecorella (I)

Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy.

Nadia Russolillo (N)

Department of Digestive and Hepatobiliary Surgery, Mauriziano Umberto I Hospital, Turin, Italy.

Martina Borzi (M)

Department of Radiology, University Hospital G.B. Rossi, University of Verona, Verona, Italy.

Giulio Vara (G)

Department of Radiology, IRCCS, Azienda Ospedaliero-Universitaria di Bologna, Sant'Orsola-Malpighi Hospital, Bologna, Italy.

Caterina Mele (C)

Hepatobiliary Surgery Unit, A. Gemelli Hospital, Università Cattolica del Sacro Cuore, Rome, Italy.

Giorgio Ercolani (G)

Department of Medical and Surgical Sciences, Alma Mater Studiorum, University of Bologna, Bologna, Italy.
Department of General Surgery, Morgagni-Pierantoni Hospital, Forlì, Italy.

Felice Giuliante (F)

Hepatobiliary Surgery Unit, A. Gemelli Hospital, Università Cattolica del Sacro Cuore, Rome, Italy.

Matteo Cescon (M)

General Surgery and Transplant Unit, IRCCS, Azienda Ospedaliero-Universitaria di Bologna, Sant'Orsola-Malpighi Hospital, Bologna, Italy.
Department of Medical and Surgical Sciences, Alma Mater Studiorum, University of Bologna, Bologna, Italy.

Alfredo Guglielmi (A)

Division of General and Hepatobiliary Surgery, Department of Surgical Sciences, Dentistry, Gynaecology and Pediatrics, University Hospital G.B. Rossi, University of Verona, Verona, Italy.

Alessandro Ferrero (A)

Department of Digestive and Hepatobiliary Surgery, Mauriziano Umberto I Hospital, Turin, Italy.

Martina Sollini (M)

Department of Nuclear Medicine, IRCCS San Raffaele, Milan, Italy.
Faculty of Medicine, Università Vita-Salute San Raffaele, Milan, Italy.

Arturo Chiti (A)

Department of Nuclear Medicine, IRCCS San Raffaele, Milan, Italy.
Faculty of Medicine, Università Vita-Salute San Raffaele, Milan, Italy.

Guido Torzilli (G)

Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy.
Division of Hepatobiliary and General Surgery, Department of Surgery, IRCCS Humanitas Research Hospital, Rozzano, Milan, Italy.

Francesca Ieva (F)

MOX Laboratory, Department of Mathematics, Politecnico di Milano, Milan, Italy.
CHDS - Center for Health Data Science, Human Technopole, Milan, Italy.

Luca Viganò (L)

Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Milan, Italy. luca.vigano@hunimed.eu.
Hepatobiliary Unit, Department of Minimally Invasive General and Oncologic Surgery, Humanitas Gavazzeni University Hospital, Bergamo, Italy. luca.vigano@hunimed.eu.

Classifications MeSH