Delta Radiomic Features Predict Resection Margin Status and Overall Survival in Neoadjuvant-Treated Pancreatic Cancer Patients.


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:
27 Dec 2023
Historique:
received: 08 08 2023
accepted: 06 12 2023
medline: 28 12 2023
pubmed: 28 12 2023
entrez: 27 12 2023
Statut: aheadofprint

Résumé

Neoadjuvant therapy (NAT) emerged as the standard of care for patients with pancreatic ductal adenocarcinoma (PDAC) who undergo surgery; however, surgery is morbid, and tools to predict resection margin status (RMS) and prognosis in the preoperative setting are needed. Radiomic models, specifically delta radiomic features (DRFs), may provide insight into treatment dynamics to improve preoperative predictions. We retrospectively collected clinical, pathological, and surgical data (patients with resectable, borderline, locally advanced, and metastatic disease), and pre/post-NAT contrast-enhanced computed tomography (CT) scans from PDAC patients at the University of Texas Southwestern Medical Center (UTSW; discovery) and Humanitas Hospital (validation cohort). Gross tumor volume was contoured from CT scans, and 257 radiomics features were extracted. DRFs were calculated by direct subtraction of pre/post-NAT radiomic features. Cox proportional models and binary prediction models, including/excluding clinical variables, were constructed to predict overall survival (OS), disease-free survival (DFS), and RMS. The discovery and validation cohorts comprised 58 and 31 patients, respectively. Both cohorts had similar clinical characteristics, apart from differences in NAT (FOLFIRINOX vs. gemcitabine/nab-paclitaxel; p < 0.05) and type of surgery resections (pancreatoduodenectomy, distal or total pancreatectomy; p < 0.05). The model that combined clinical variables (pre-NAT carbohydrate antigen (CA) 19-9, the change in CA19-9 after NAT (∆CA19-9), and resectability status) and DRFs outperformed the clinical feature-based models and other radiomics feature-based models in predicting OS (UTSW: 0.73; Humanitas: 0.66), DFS (UTSW: 0.75; Humanitas: 0.64), and RMS (UTSW 0.73; Humanitas: 0.69). Our externally validated, predictive/prognostic delta-radiomics models, which incorporate clinical variables, show promise in predicting the risk of predicting RMS in NAT-treated PDAC patients and their OS or DFS.

Sections du résumé

BACKGROUND BACKGROUND
Neoadjuvant therapy (NAT) emerged as the standard of care for patients with pancreatic ductal adenocarcinoma (PDAC) who undergo surgery; however, surgery is morbid, and tools to predict resection margin status (RMS) and prognosis in the preoperative setting are needed. Radiomic models, specifically delta radiomic features (DRFs), may provide insight into treatment dynamics to improve preoperative predictions.
METHODS METHODS
We retrospectively collected clinical, pathological, and surgical data (patients with resectable, borderline, locally advanced, and metastatic disease), and pre/post-NAT contrast-enhanced computed tomography (CT) scans from PDAC patients at the University of Texas Southwestern Medical Center (UTSW; discovery) and Humanitas Hospital (validation cohort). Gross tumor volume was contoured from CT scans, and 257 radiomics features were extracted. DRFs were calculated by direct subtraction of pre/post-NAT radiomic features. Cox proportional models and binary prediction models, including/excluding clinical variables, were constructed to predict overall survival (OS), disease-free survival (DFS), and RMS.
RESULTS RESULTS
The discovery and validation cohorts comprised 58 and 31 patients, respectively. Both cohorts had similar clinical characteristics, apart from differences in NAT (FOLFIRINOX vs. gemcitabine/nab-paclitaxel; p < 0.05) and type of surgery resections (pancreatoduodenectomy, distal or total pancreatectomy; p < 0.05). The model that combined clinical variables (pre-NAT carbohydrate antigen (CA) 19-9, the change in CA19-9 after NAT (∆CA19-9), and resectability status) and DRFs outperformed the clinical feature-based models and other radiomics feature-based models in predicting OS (UTSW: 0.73; Humanitas: 0.66), DFS (UTSW: 0.75; Humanitas: 0.64), and RMS (UTSW 0.73; Humanitas: 0.69).
CONCLUSIONS CONCLUSIONS
Our externally validated, predictive/prognostic delta-radiomics models, which incorporate clinical variables, show promise in predicting the risk of predicting RMS in NAT-treated PDAC patients and their OS or DFS.

Identifiants

pubmed: 38151623
doi: 10.1245/s10434-023-14805-5
pii: 10.1245/s10434-023-14805-5
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIH HHS
ID : 5R37CA242070
Pays : United States

Informations de copyright

© 2023. The Author(s).

Références

Sung H, Ferlay J, Siegel RL, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49. https://doi.org/10.3322/caac.21660 .
doi: 10.3322/caac.21660 pubmed: 33538338
Rahib L, Smith BD, Aizenberg R, Rosenzweig AB, Fleshman JM, Matrisian LM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74(11):2913–21. https://doi.org/10.1158/0008-5472.CAN-14-0155 .
doi: 10.1158/0008-5472.CAN-14-0155 pubmed: 24840647
Demir IE, Jäger C, Schlitter AM, et al. R0 versus R1 resection matters after pancreaticoduodenectomy, and less after distal or total pancreatectomy for pancreatic cancer. Ann Surg. 2018;268(6):1058–68.
doi: 10.1097/SLA.0000000000002345 pubmed: 28692477
Kaltenmeier C, Nassour I, Hoehn RS, et al. Impact of Resection margin status in patients with pancreatic cancer: a national cohort study. J Gastrointest Surg. 2021;25(9):2307–16. https://doi.org/10.1007/s11605-020-04870-6 .
doi: 10.1007/s11605-020-04870-6 pubmed: 33269460
Ferrone CR, Marchegiani G, Hong TS, et al. Radiological and surgical implications of neoadjuvant treatment with FOLFIRINOX for locally advanced and borderline resectable pancreatic cancer. Ann Surg. 2015;261(1):12–7. https://doi.org/10.1097/sla.0000000000000867 .
doi: 10.1097/sla.0000000000000867 pubmed: 25599322
Perri G, Prakash L, Wang H, et al. Radiographic and serologic predictors of pathologic major response to preoperative therapy for pancreatic cancer. Ann Surg. 2021;273(4):806–13.
doi: 10.1097/SLA.0000000000003442 pubmed: 31274655
Khristenko E, Shrainer I, Setdikova G, Palkina O, Sinitsyn V, Lyadov V. Preoperative CT-based detection of extrapancreatic perineural invasion in pancreatic cancer. Sci Rep. 2021;11(1):1–11.
doi: 10.1038/s41598-021-81322-4
Zhang Y, Huang Z-X, Song B. Role of imaging in evaluating the response after neoadjuvant treatment for pancreatic ductal adenocarcinoma. World J Gastroenterol. 2021;27(22):3037.
doi: 10.3748/wjg.v27.i22.3037 pubmed: 34168406 pmcid: 8192284
Janssen BV, Verhoef S, Wesdorp NJ, et al. Imaging-based machine-learning models to predict clinical outcomes and identify biomarkers in pancreatic cancer: a scoping review. Ann Surg. 2022;275(3):560–7.
doi: 10.1097/SLA.0000000000005349 pubmed: 34954758
Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2016;278(2):563–77. https://doi.org/10.1148/radiol.2015151169 .
doi: 10.1148/radiol.2015151169 pubmed: 26579733
Healy GM, Salinas-Miranda E, Jain R, et al. Pre-operative radiomics model for prognostication in resectable pancreatic adenocarcinoma with external validation. Eur Radiol. 2022;32(4):2492–505.
doi: 10.1007/s00330-021-08314-w pubmed: 34757450
Parr E, Du Q, Zhang C, et al. Radiomics-based outcome prediction for pancreatic cancer following stereotactic body radiotherapy. Cancers. 2020;12(4):1051.
doi: 10.3390/cancers12041051 pubmed: 32344538 pmcid: 7226523
Kim BR, Kim JH, Ahn SJ, et al. CT prediction of resectability and prognosis in patients with pancreatic ductal adenocarcinoma after neoadjuvant treatment using image findings and texture analysis. Eur Radiol. 2019;29(1):362–72.
doi: 10.1007/s00330-018-5574-0 pubmed: 29931561
Jeon SH, Song C, Chie EK, et al. Delta-radiomics signature predicts treatment outcomes after preoperative chemoradiotherapy and surgery in rectal cancer. Radiat Oncol. 2019;14(1):1–10.
doi: 10.1186/s13014-019-1246-8
Nasief H, Hall W, Zheng C, et al. Improving treatment response prediction for chemoradiation therapy of pancreatic cancer using a combination of delta-radiomics and the clinical biomarker CA19-9. Front Oncol. 2020;9:1464.
doi: 10.3389/fonc.2019.01464 pubmed: 31970088 pmcid: 6960122
Tomaszewski M, Latifi K, Boyer E, et al. Delta radiomics analysis of magnetic resonance guided radiotherapy imaging data can enable treatment response prediction in pancreatic cancer. Radiat Oncol. 2021;16(1):1–11.
doi: 10.1186/s13014-021-01957-5
Zwanenburg A, Vallières M, Abdalah MA, et al. The image biomarker standardization initiative: standardized quantitative radiomics for high-throughput image-based phenotyping. Radiology. 2020;295(2):328–38.
doi: 10.1148/radiol.2020191145 pubmed: 32154773
Zwanenburg A. Radiomics in nuclear medicine: robustness, reproducibility, standardization, and how to avoid data analysis traps and replication crisis. Eur J Nucl Med Mol Imaging. 2019;46(13):2638–55.
doi: 10.1007/s00259-019-04391-8 pubmed: 31240330
Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749–62. https://doi.org/10.1038/nrclinonc.2017.141 .
doi: 10.1038/nrclinonc.2017.141 pubmed: 28975929
Kocak B, Baessler B, Bakas S, et al. CheckList for EvaluAtion of Radiomics research (CLEAR): a step-by-step reporting guideline for authors and reviewers endorsed by ESR and EuSoMII. Insights Imaging. 2023;14(1):75. https://doi.org/10.1186/s13244-023-01415-8 .
doi: 10.1186/s13244-023-01415-8 pubmed: 37142815 pmcid: 10160267
Hall WA, Heerkens HD, Paulson ES, et al. Pancreatic gross tumor volume contouring on computed tomography (CT) compared with magnetic resonance imaging (MRI): results of an international contouring conference. Pract Radiat Oncol. 2018;8(2):107–15. https://doi.org/10.1016/j.prro.2017.11.005 .
doi: 10.1016/j.prro.2017.11.005 pubmed: 29426692
Oar A, Lee M, Le H, et al. Australasian Gastrointestinal Trials Group (AGITG) and Trans-Tasman Radiation Oncology Group (TROG) guidelines for pancreatic stereotactic body radiation therapy (SBRT). Pract Radiat Oncol. 2020;10(3):e136–46. https://doi.org/10.1016/j.prro.2019.07.018 .
doi: 10.1016/j.prro.2019.07.018 pubmed: 31761541
Cellini F, Arcelli A, Simoni N, et al. Basics and frontiers on pancreatic cancer for radiation oncology: target delineation, SBRT, SIB technique, MRgRT, particle therapy, immunotherapy and clinical guidelines. Cancers (Basel). 2020. https://doi.org/10.3390/cancers12071729 .
doi: 10.3390/cancers12071729 pubmed: 32610592
Vallieres M, Kay-Rivest E, Perrin LJ, et al. Radiomics strategies for risk assessment of tumour failure in head-and-neck cancer. Sci Rep. 2017;7(1):10117. https://doi.org/10.1038/s41598-017-10371-5 .
doi: 10.1038/s41598-017-10371-5 pubmed: 28860628 pmcid: 5579274
D’Onofrio M, Ciaravino V, Cardobi N, et al. CT enhancement and 3D texture analysis of pancreatic neuroendocrine neoplasms. Sci Rep. 2019;9(1):2176. https://doi.org/10.1038/s41598-018-38459-6 .
doi: 10.1038/s41598-018-38459-6 pubmed: 30778137 pmcid: 6379382
Jeon SH, Song C, Chie EK, et al. Delta-radiomics signature predicts treatment outcomes after preoperative chemoradiotherapy and surgery in rectal cancer. Radiat Oncol. 2019;14(1):43. https://doi.org/10.1186/s13014-019-1246-8 .
doi: 10.1186/s13014-019-1246-8 pubmed: 30866965 pmcid: 6417065
Fave X, Zhang LF, Yang JZ, et al. Delta-radiomics features for the prediction of patient outcomes in non-small cell lung cancer. Sci Rep. 2017;7(1):588. https://doi.org/10.1038/s41598-017-00665-z .
doi: 10.1038/s41598-017-00665-z pubmed: 28373718 pmcid: 5428827
Chiesa S, Bartoli FB, Longo S, et al. Delta radiomics features analysis for the prediction of patients outcomes in glioblastoma multiforme: the generating hypothesis phase of GLIFA project. Int J Radiat Oncol. 2018;102(3):S213–S213. https://doi.org/10.1016/j.ijrobp.2018.07.128 .
doi: 10.1016/j.ijrobp.2018.07.128
Palumbo D, Mori M, Prato F, et al. Prediction of early distant recurrence in upfront resectable pancreatic adenocarcinoma: a multidisciplinary, machine learning-based approach. Cancers (Basel). 2021;13:19. https://doi.org/10.3390/cancers13194938 .
doi: 10.3390/cancers13194938
Nasief H, Zheng C, Schott D, et al. A machine learning based delta-radiomics process for early prediction of treatment response of pancreatic cancer. NPJ Precis Oncol. 2019;3:25. https://doi.org/10.1038/s41698-019-0096-z .
doi: 10.1038/s41698-019-0096-z pubmed: 31602401 pmcid: 6778189
Cozzi L, Comito T, Fogliata A, et al. Computed tomography based radiomic signature as predictive of survival and local control after stereotactic body radiation therapy in pancreatic carcinoma. PLoS ONE. 2019;14(1):e0210758. https://doi.org/10.1371/journal.pone.0210758 .
doi: 10.1371/journal.pone.0210758 pubmed: 30657785 pmcid: 6338357
Rizzo S, Botta F, Raimondi S, et al. Radiomics: the facts and the challenges of image analysis. Eur Radiol Exp. 2018;2(1):36. https://doi.org/10.1186/s41747-018-0068-z .
doi: 10.1186/s41747-018-0068-z pubmed: 30426318 pmcid: 6234198
Song J, Yin Y, Wang H, Chang Z, Liu Z, Cui L. A review of original articles published in the emerging field of radiomics. Eur J Radiol. 2020;127:108991. https://doi.org/10.1016/j.ejrad.2020.108991 .
doi: 10.1016/j.ejrad.2020.108991 pubmed: 32334372
Chen Y, Chen TW, Wu CQ, et al. Radiomics model of contrast-enhanced computed tomography for predicting the recurrence of acute pancreatitis. Eur Radiol. 2019;29(8):4408–17. https://doi.org/10.1007/s00330-018-5824-1 .
doi: 10.1007/s00330-018-5824-1 pubmed: 30413966
Dalal V, Carmicheal J, Dhaliwal A, Jain M, Kaur S, Batra SK. Radiomics in stratification of pancreatic cystic lesions: Machine learning in action. Cancer Lett. 2020;469:228–37. https://doi.org/10.1016/j.canlet.2019.10.023 .
doi: 10.1016/j.canlet.2019.10.023 pubmed: 31629933
Zhou ZG, Folkert M, Iyengar P, et al. Multi-objective radiomics model for predicting distant failure in lung SBRT. Phys Med Biol. 2017;62(11):4460–78. https://doi.org/10.1088/1361-6560/aa6ae5 .
doi: 10.1088/1361-6560/aa6ae5 pubmed: 28480871 pmcid: 8087147
Wang K, Zhou Z, Wang R, et al. A multi-objective radiomics model for the prediction of locoregional recurrence in head and neck squamous cell cancers. Med Phys. 2020;47(10):5392–400.
doi: 10.1002/mp.14388 pubmed: 32657426
Poruk KE, Gay DZ, Brown K, et al. The clinical utility of CA 19–9 in pancreatic adenocarcinoma: diagnostic and prognostic updates. Curr Mol Med. 2013;13(3):340–51.
pubmed: 23331006 pmcid: 4419808
Ahmad SA, Duong M, Sohal DP, et al. Surgical outcome results from SWOG S1505: a randomized clinical trial of mFOLFIRINOX vs. gemcitabine/nab-paclitaxel for perioperative treatment of resectable pancreatic ductal adenocarcinoma. Ann Surg. 2020;272(3):481.
doi: 10.1097/SLA.0000000000004155 pubmed: 32740235
Oettle H, Neuhaus P, Hochhaus A, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA. 2013;310(14):1473–81.
doi: 10.1001/jama.2013.279201 pubmed: 24104372
Neoptolemos JP, Stocken DD, Bassi C, et al. Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial. JAMA. 2010;304(10):1073–81.
doi: 10.1001/jama.2010.1275 pubmed: 20823433
Rigiroli F, Hoye J, Lerebours R, et al. Exploratory analysis of mesenteric-portal axis CT radiomic features for survival prediction of patients with pancreatic ductal adenocarcinoma. Eur Radiol. 2023;33(8):5779–91. https://doi.org/10.1007/s00330-023-09532-0 .
doi: 10.1007/s00330-023-09532-0 pubmed: 36894753
Khalvati F, Zhang Y, Baig S, et al. Prognostic value of CT radiomic features in resectable pancreatic ductal adenocarcinoma. Sci Rep. 2019. https://doi.org/10.1038/s41598-019-41728-7 .
doi: 10.1038/s41598-019-41728-7 pubmed: 31863034 pmcid: 6925141
Oikonomou A, Khalvati F, Tyrrell PN, et al. Radiomics analysis at PET/CT contributes to prognosis of recurrence and survival in lung cancer treated with stereotactic body radiotherapy. Sci Rep. 2018. https://doi.org/10.1038/s41598-018-22357-y .
doi: 10.1038/s41598-018-22357-y pubmed: 30341326 pmcid: 6195575
Lubner MG, Stabo N, Abel EJ, Del Rio AM, Pickhardt PJ. CT textural analysis of large primary renal cell carcinomas: pretreatment tumor heterogeneity correlates with histologic findings and clinical outcomes. Am J Roentgenol. 2016;207(1):96–105.
doi: 10.2214/AJR.15.15451
Lubner MG, Stabo N, Lubner SJ, et al. CT textural analysis of hepatic metastatic colorectal cancer: pre-treatment tumor heterogeneity correlates with pathology and clinical outcomes. Abdominal Imaging. 2015;40:2331–7.
doi: 10.1007/s00261-015-0438-4 pubmed: 25968046
Toyama Y, Hotta M, Motoi F, Takanami K, Minamimoto R, Takase K. Prognostic value of FDG-PET radiomics with machine learning in pancreatic cancer. Sci Rep. 2020. https://doi.org/10.1038/s41598-020-73237-3 .
doi: 10.1038/s41598-020-73237-3 pubmed: 33116238 pmcid: 7595182

Auteurs

Kai Wang (K)

Department of Radiation Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

John D Karalis (JD)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Ahmed Elamir (A)

Department of Radiation Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Alessandro Bifolco (A)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Megan Wachsmann (M)

Department of Pathology, Veterans Affairs North Texas Health Care System, Dallas, TX, USA.

Giovanni Capretti (G)

Pancreatic Surgery Unit, IRCCS Humanitas Research Hospital, Rozzano, Italy.
Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy.

Paola Spaggiari (P)

Department of Pathology, IRCCS Humanitas Research Hospital, Rozzano, Italy.

Sebastian Enrico (S)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Kishore Balasubramanian (K)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Nafeesah Fatimah (N)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Giada Pontecorvi (G)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Martina Nebbia (M)

Pancreatic Surgery Unit, IRCCS Humanitas Research Hospital, Rozzano, Italy.

Adam Yopp (A)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Ravi Kaza (R)

Department of Radiology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Ivan Pedrosa (I)

Department of Radiology, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Herbert Zeh (H)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Patricio Polanco (P)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA.

Alessandro Zerbi (A)

Pancreatic Surgery Unit, IRCCS Humanitas Research Hospital, Rozzano, Italy.
Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, Italy.

Jing Wang (J)

Department of Radiation Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA. jing.wang@utsouthwestern.edu.

Todd Aguilera (T)

Department of Radiation Oncology, University of Texas Southwestern Medical Center, Dallas, TX, USA. todd.aguilera@utsouthwestern.edu.

Matteo Ligorio (M)

Department of Surgery, University of Texas Southwestern Medical Center, Dallas, TX, USA. matteo.ligorio@utsouthwestern.edu.

Classifications MeSH