Abstract
Purpose
This study aimed to establish a nomogram based on preoperative magnetic resonance imaging (MRI) features to predict the very early recurrence (VER, less than 6 months) of intrahepatic mass-forming cholangiocarcinoma (IMCC) after R0 resection.
Methods
This study enrolled a group of 193 IMCC patients from our institution between March 2010 and January 2022. Patients were allocated into the development cohort (n = 137) and the validation cohort (n = 56), randomly, and the preoperative clinical and MRI features were collected. Univariate and multivariate stepwise logistic regression assessments were adopted to assess predictors of VER. Nomogram was constructed and certificated in the validation cohort. The performance of the prediction nomogram was evaluated by its discrimination, calibration, and clinical utility. The performance of the nomogram was compared with the T stage of the American Joint Committee on Cancer (AJCC) 8th edition staging system.
Results
Fifty-three patients (27.5%) experienced VER of the tumor and 140 patients (72.5%) with non-VER, during the follow-up period. After multivariate stepwise logistic regression, number of lesions, diffuse hypoenhancement on arterial phase, necorsis and suspicious lymph nodes were independently associated with VER. The nomogram demonstrated significantly higher area under the curve (AUC) of 0.813 than T stage (AUC = 0.666, P = 0.006) in the development cohort, whereas in the validation cohort, the nomogram showed better discrimination performance, with an AUC of 0.808 than T stage (0.705) with no significantly difference (P = 0.230). Decision curve analysis reflected the clinical net benefit of the nomogram.
Conclusion
The nomogram based on preoperative MRI features is a reliable tool to predict VER for patients with IMCC after R0 resection. This nomogram will be helpful to improve survival prediction and individualized treatment.
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Abbreviations
- AFP:
-
Alpha-fetoprotein
- AJCC:
-
American Joint Committee on Cancer
- AP:
-
Arterial phase
- AUC:
-
Area under the curve
- CA 19-9:
-
Cancer antigen 19-9
- CEA:
-
Carcinoembryonic antigen
- CI:
-
Confidence interval
- IMCC:
-
Intrahepatic mass-forming cholangiocarcinoma
- NT:
-
Neoadjuvant therapy
- OR:
-
Odds ratio
- ROC:
-
Receiver operating characteristic
Reference
Bertuccio P, Malvezzi M, Carioli G, Hashim D, Boffetta P, El-Serag H B, La Vecchia C and Negri E, Global trends in mortality from intrahepatic and extrahepatic cholangiocarcinoma. J Hepatol 2019; 71: 104-114.
Kendall T, Verheij J, Gaudio E, Evert M, Guido M, Goeppert B and Carpino G, Anatomical, histomorphological and molecular classification of cholangiocarcinoma. Liver Int 2019; 39 Suppl 1: 7-18.
Littau M J, Kim P, Kulshrestha S, Bunn C, Tonelli C, Abdelsattar Z M, Luchette F A and Baker M S, Resectable intrahepatic and hilar cholangiocarcinoma: Is margin status associated with survival? Surgery 2022; 171: 703-710.
Mazzaferro V, Gorgen A, Roayaie S, Dit Busset M D and Sapisochin G, Liver resection and transplantation for intrahepatic cholangiocarcinoma. J Hepatol 2020; 72: 364-377.
Zhang X F, Beal E W, Bagante F, Chakedis J, Weiss M, Popescu I, Marques H P, Aldrighetti L, Maithel S K, Pulitano C, Bauer T W, Shen F, Poultsides G A, Soubrane O, Martel G, Koerkamp B G, Itaru E and Pawlik T M, Early versus late recurrence of intrahepatic cholangiocarcinoma after resection with curative intent. Br J Surg 2018; 105: 848-856.
Zhao L, Ma X, Liang M, Li D, Ma P, Wang S, Wu Z and Zhao X, Prediction for early recurrence of intrahepatic mass-forming cholangiocarcinoma: quantitative magnetic resonance imaging combined with prognostic immunohistochemical markers. Cancer Imaging 2019; 19: 49.
Tsilimigras D I, Sahara K, Wu L, Moris D, Bagante F, Guglielmi A et al., Very Early Recurrence After Liver Resection for Intrahepatic Cholangiocarcinoma: Considering Alternative Treatment Approaches. JAMA Surg 2020; 155: 823-831.
Tsilimigras D I and Pawlik T M, Preoperative Model and Patient Selection for Neoadjuvant Therapy for Intrahepatic Cholangiocarcinoma-Reply. JAMA Surg 2021; 156: 395-396.
Yadav S, Xie H, Bin-Riaz I, Sharma P, Durani U, Goyal G, Borah B, Borad M J, Smoot R L, Roberts L R, Go R S, McWilliams R R and Mahipal A, Neoadjuvant vs. adjuvant chemotherapy for cholangiocarcinoma: A propensity score matched analysis. Eur J Surg Oncol 2019; 45: 1432-1438.
Chun Y S, Pawlik T M and Vauthey J N, 8th Edition of the AJCC Cancer Staging Manual: Pancreas and Hepatobiliary Cancers. Ann Surg Oncol 2018; 25: 845-847.
Sasaki K, Margonis G A, Andreatos N, Chen Q, Barbon C, Bagante F et al., Serum tumor markers enhance the predictive power of the AJCC and LCSGJ staging systems in resectable intrahepatic cholangiocarcinoma. HPB (Oxford) 2018; 20: 956-965.
Buettner S, Galjart B, van Vugt J L A, Bagante F, Alexandrescu S, Marques H P et al., Performance of prognostic scores and staging systems in predicting long-term survival outcomes after surgery for intrahepatic cholangiocarcinoma. J Surg Oncol 2017; 116: 1085-1095.
Granata V, Grassi R, Fusco R, Setola S V, Belli A, Ottaiano A, Nasti G, La Porta M, Danti G, Cappabianca S, Cutolo C, Petrillo A and Izzo F, Intrahepatic cholangiocarcinoma and its differential diagnosis at MRI: how radiologist should assess MR features. Radiol Med 2021; 126: 1584-1600.
Jhaveri K S and Hosseini-Nik H, MRI of cholangiocarcinoma. J Magn Reson Imaging 2015; 42: 1165-79.
Min J H, Kim Y K, Choi S Y, Kang T W, Lee S J, Kim J M, Ahn S and Cho H, Intrahepatic Mass-forming Cholangiocarcinoma: Arterial Enhancement Patterns at MRI and Prognosis. Radiology 2019; 290: 691-699.
Promsorn J, Eurboonyanun K, Chadbunchachai P, Apivatanasiri C, Wirasorn K, Chindaprasirt J, Sookprasert A and Harisinghani M, Diffusion-weighted imaging as an imaging biomarker for assessing survival of patients with intrahepatic mass-forming cholangiocarcinoma. Abdom Radiol (NY) 2022; 47: 2811-2821.
Liang W, Xu L, Yang P, Zhang L, Wan D, Huang Q, Niu T and Chen F, Novel Nomogram for Preoperative Prediction of Early Recurrence in Intrahepatic Cholangiocarcinoma. Front Oncol 2018; 8: 360.
Sheng R, Huang X, Jin K, Gao S, Zeng M, Wu D and Shi G, Contrast-enhanced MRI could predict response of systemic therapy in advanced intrahepatic cholangiocarcinoma. Eur Radiol 2022; 32: 5156-5165.
Lee A J and Chun Y S, Intrahepatic cholangiocarcinoma: the AJCC/UICC 8th edition updates. Chin Clin Oncol 2018; 7: 52.
Hallgren K A, Computing Inter-Rater Reliability for Observational Data: An Overview and Tutorial. Tutor Quant Methods Psychol 2012; 8: 23-34.
Balachandran V P, Gonen M, Smith J J and DeMatteo R P, Nomograms in oncology: more than meets the eye. Lancet Oncol 2015; 16: e173-80.
Wu Y, Liu H, Zeng J, Chen Y, Fang G, Zhang J, Zhou W, Zeng Y and Liu J, Development and validation of nomogram to predict very early recurrence of combined hepatocellular-cholangiocarcinoma after hepatic resection: a multi-institutional study. World J Surg Oncol 2022; 20: 60.
Hirokawa F, Hayashi M, Asakuma M, Shimizu T, Inoue Y and Uchiyama K, Risk factors and patterns of early recurrence after curative hepatectomy for hepatocellular carcinoma. Surg Oncol 2016; 25: 24-9.
Mason M C, Massarweh N N, Tzeng C D, Chiang Y J, Chun Y S, Aloia T A, Javle M, Vauthey J N and Tran Cao H S, Time to Rethink Upfront Surgery for Resectable Intrahepatic Cholangiocarcinoma? Implications from the Neoadjuvant Experience. Ann Surg Oncol 2021; 28: 6725-6735.
Utuama O, Permuth J B, Dagne G, Sanchez-Anguiano A, Alman A, Kumar A, Denbo J, Kim R, Fleming J B and Anaya D A, Neoadjuvant Chemotherapy for Intrahepatic Cholangiocarcinoma: A Propensity Score Survival Analysis Supporting Use in Patients with High-Risk Disease. Ann Surg Oncol 2021; 28: 1939-1949.
Jin K P, Sheng R F, Yang C and Zeng M S, Combined arterial and delayed enhancement patterns of MRI assist in prognostic prediction for intrahepatic mass-forming cholangiocarcinoma (IMCC). Abdom Radiol (NY) 2022; 47: 640-650.
King M J, Hectors S, Lee K M, Omidele O, Babb J S, Schwartz M, Tabrizian P, Taouli B and Lewis S, Outcomes assessment in intrahepatic cholangiocarcinoma using qualitative and quantitative imaging features. Cancer Imaging 2020; 20: 43.
Baheti A D, Tirumani S H, Rosenthal M H, Shinagare A B and Ramaiya N H, Diagnosis and management of intrahepatic cholangiocarcinoma: a comprehensive update for the radiologist. Clin Radiol 2014; 69: e463-70.
Sulpice L, Rayar M, Desille M, Turlin B, Fautrel A, Boucher E, Llamas-Gutierrez F, Meunier B, Boudjema K, Clément B and Coulouarn C, Molecular profiling of stroma identifies osteopontin as an independent predictor of poor prognosis in intrahepatic cholangiocarcinoma. Hepatology 2013; 58: 1992-2000.
Atanasov G, Dietel C, Feldbrügge L, Benzing C, Krenzien F, Brandl A, Mann E, Englisch J P, Schierle K, Robson S C, Splith K, Morgul M H, Reutzel-Selke A, Jonas S, Pascher A, Bahra M, Pratschke J and Schmelzle M, Tumor necrosis and infiltrating macrophages predict survival after curative resection for cholangiocarcinoma. Oncoimmunology 2017; 6: e1331806.
Atanasov G, Schierle K, Hau H M, Dietel C, Krenzien F, Brandl A, Wiltberger G, Englisch J P, Robson S C, Reutzel-Selke A, Pascher A, Jonas S, Pratschke J, Benzing C and Schmelzle M, Prognostic Significance of Tumor Necrosis in Hilar Cholangiocarcinoma. Ann Surg Oncol 2017; 24: 518-525.
Tsilimigras D I, Ejaz A, Cloyd J, Guglielmi A, Aldrighetti L, Weiss M, Bauer T W, Alexandrescu S, Poultsides G A, Maithel S K, Marques H P, Martel G, Pulitano C, Shen F, Soubrane O, Koerkamp B G, Endo I and Pawlik T M, Tumor Necrosis Impacts Prognosis of Patients Undergoing Resection for T1 Intrahepatic Cholangiocarcinoma. Ann Surg Oncol 2022. https://doi.org/10.1245/s10434-022-11462-y
Wang Y, Li J, Xia Y, Gong R, Wang K, Yan Z, Wan X, Liu G, Wu D, Shi L, Lau W, Wu M and Shen F, Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol 2013; 31: 1188-95.
Hyder O, Marques H, Pulitano C, Marsh J W, Alexandrescu S, Bauer T W, Gamblin T C, Sotiropoulos G C, Paul A, Barroso E, Clary B M, Aldrighetti L, Ferrone C R, Zhu A X, Popescu I, Gigot J F, Mentha G, Feng S and Pawlik T M, A nomogram to predict long-term survival after resection for intrahepatic cholangiocarcinoma: an Eastern and Western experience. JAMA Surg 2014; 149: 432-8.
Amin M B, Greene F L, Edge S B, Compton C C, Gershenwald J E, Brookland R K, Meyer L, Gress D M, Byrd D R and Winchester D P, The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more "personalized" approach to cancer staging. CA Cancer J Clin 2017; 67: 93-99.
Zhou S N, Lu S S, Ju D W, Yu L X, Liang X X, Xiang X, Liangpunsakul S, Roberts L R, Lu Y Y and Zhang N, A New Prognostic Model Covering All Stages of Intrahepatic Cholangiocarcinoma. J Clin Transl Hepatol 2022; 10: 254-262.
Rhee H, Choi S H, Park J H, Cho E S, Yeom S K, Park S, Han K, Lee S S and Park M S, Preoperative magnetic resonance imaging-based prognostic model for mass-forming intrahepatic cholangiocarcinoma. Liver Int 2022; 42: 930-941.
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Study concepts/study design: SC, HZ; data acquisition or data analysis/interpretation: LW, RZ, WP; statistical analysis: SC, LW, RZ; drafting the article or revising it critically for important intellectual content: SC, SZ, HZ; final approval of the version to be submitted: SC, LW, RZ, WP, SZ, HZ authors.
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Chen, S., Wan, L., Zhao, R. et al. Preoperative MRI features predicting very early recurrence of intrahepatic mass-forming cholangiocarcinoma after R0 resection: a comparison with the AJCC 8th edition staging system. Abdom Radiol 49, 21–33 (2024). https://doi.org/10.1007/s00261-023-04038-1
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DOI: https://doi.org/10.1007/s00261-023-04038-1