Skip to main content
Top
Published in: BMC Cancer 1/2023

Open Access 01-12-2023 | Cholangiocarcinoma | Research

Using immunovascular characteristics to predict very early recurrence and prognosis of resectable intrahepatic cholangiocarcinoma

Authors: Ying Xu, Zhuo Li, Yanzhao Zhou, Yi Yang, Jingzhong Ouyang, Lu Li, Zhen Huang, Feng Ye, Jianming Ying, Hong Zhao, Jinxue Zhou, Xinming Zhao

Published in: BMC Cancer | Issue 1/2023

Login to get access

Abstract

Objective

To predict the very early recurrence (VER) of patients with intrahepatic cholangiocarcinoma (ICC) based on TLSs and MVI status, and further perform prognosis stratifications.

Methods

A total of 160, 51 ICC patients from two institutions between May 2012 and July 2022 were retrospectively included as training, external validation cohort. Clinical, radiological and pathological variables were evaluated and collected. Univariate and multivariate analysis were applied to select the significant factors related to VER of ICC. The factors selected were combined to perform stratification of overall survival (OS) using the Kaplan-Meier method with the log-rank test.

Results

Overall, 39 patients (24.4%) had VER, whereas 121 (75.6%) did not (non-VER group). In the training cohort, the median OS was 40.5 months (95% CIs: 33.2–47.7 months). The VER group showed significantly worse OS than the non-VER group (median OS: 14.8, 95% CI:11.6–18.0 months vs. 53.4, 34.3–72.6 months; p<0.001), and it was confirmed in the validation cohort (median OS: 22.1, 95% CI: 8.8–35.4 months vs. 40.1, 21.2–59.0 months; p = 0.003). According to the univariate analysis, four variables were significantly different between the VER group and non-VER group (TLSs status, p = 0.028; differentiation, p = 0.023; MVI status, p = 0.012; diameter, p = 0.028). According to the multivariate analysis, MVI-positive status was independently associated with a higher probability of VER (odds ratio [OR], 2.5; 95% CIs,1.16–5.18; p = 0.018), whereas intra-tumoral TLSs-positive status was associated with lower odds of VER (OR, 0.43; 95% CIs, 0.19–0.97; p = 0.041). Based on the TLSs and MVI status, patients of ICC were categorized into four groups: TLSs-positive and MVI-negative (TP/MN); TLSs-negative and MVI-negative (TN/MN); TLSs-positive and MVI-positive (TP/MP), TLSs-negative and MVI-positive groups (TN/MP). In the training cohort, the four groups could be correlated with OS significantly (p<0.001), and it was confirmed in the validation cohort (p<0.001).

Conclusion

Intra-tumoral TLSs and MVI status are independent predictive factors of VER after surgery, based on which immunovascular stratifications are constructed and associated with OS significantly of resectable intrahepatic cholangiocarcinoma.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bertuccio P, Malvezzi M, Carioli G, Hashim D, Boffetta P, El-Serag HB, La Vecchia C, Negri E. Global trends in mortality from intrahepatic and extrahepatic cholangiocarcinoma. J Hepatol. 2019;71(1):104–14.CrossRefPubMed Bertuccio P, Malvezzi M, Carioli G, Hashim D, Boffetta P, El-Serag HB, La Vecchia C, Negri E. Global trends in mortality from intrahepatic and extrahepatic cholangiocarcinoma. J Hepatol. 2019;71(1):104–14.CrossRefPubMed
2.
go back to reference Forner A, Vidili G, Rengo M, Bujanda L, Ponz-Sarvise M, Lamarca A. Clinical presentation, diagnosis and staging of cholangiocarcinoma. Liver Int. 2019;39(Suppl 1):98–107.CrossRefPubMed Forner A, Vidili G, Rengo M, Bujanda L, Ponz-Sarvise M, Lamarca A. Clinical presentation, diagnosis and staging of cholangiocarcinoma. Liver Int. 2019;39(Suppl 1):98–107.CrossRefPubMed
3.
go back to reference Zhang XF, Beal EW, Bagante F, Chakedis J, Weiss M, Popescu I, Marques HP, Aldrighetti L, Maithel SK, Pulitano C, et al. Early versus late recurrence of intrahepatic cholangiocarcinoma after resection with curative intent. Br J Surg. 2018;105(7):848–56.CrossRefPubMed Zhang XF, Beal EW, Bagante F, Chakedis J, Weiss M, Popescu I, Marques HP, Aldrighetti L, Maithel SK, Pulitano C, et al. Early versus late recurrence of intrahepatic cholangiocarcinoma after resection with curative intent. Br J Surg. 2018;105(7):848–56.CrossRefPubMed
4.
go back to reference Tsilimigras DI, Sahara K, Wu L, Moris D, Bagante F, Guglielmi A, Aldrighetti L, Weiss M, Bauer TW, Alexandrescu S, et al. Very early recurrence after liver resection for Intrahepatic Cholangiocarcinoma: considering Alternative Treatment Approaches. JAMA Surg. 2020;155(9):823–31.CrossRefPubMed Tsilimigras DI, Sahara K, Wu L, Moris D, Bagante F, Guglielmi A, Aldrighetti L, Weiss M, Bauer TW, Alexandrescu S, et al. Very early recurrence after liver resection for Intrahepatic Cholangiocarcinoma: considering Alternative Treatment Approaches. JAMA Surg. 2020;155(9):823–31.CrossRefPubMed
5.
go back to reference Doussot A, Gonen M, Wiggers JK, Groot-Koerkamp B, DeMatteo RP, Fuks D, Allen PJ, Farges O, Kingham TP, Regimbeau JM, et al. Recurrence patterns and Disease-Free Survival after Resection of Intrahepatic Cholangiocarcinoma: preoperative and postoperative prognostic models. J Am Coll Surg. 2016;223(3):493–505e492.CrossRefPubMedPubMedCentral Doussot A, Gonen M, Wiggers JK, Groot-Koerkamp B, DeMatteo RP, Fuks D, Allen PJ, Farges O, Kingham TP, Regimbeau JM, et al. Recurrence patterns and Disease-Free Survival after Resection of Intrahepatic Cholangiocarcinoma: preoperative and postoperative prognostic models. J Am Coll Surg. 2016;223(3):493–505e492.CrossRefPubMedPubMedCentral
6.
go back to reference Fabris L, Sato K, Alpini G, Strazzabosco M. The Tumor Microenvironment in Cholangiocarcinoma Progression. Hepatology. 2021;73(Suppl 1):75–85.CrossRefPubMed Fabris L, Sato K, Alpini G, Strazzabosco M. The Tumor Microenvironment in Cholangiocarcinoma Progression. Hepatology. 2021;73(Suppl 1):75–85.CrossRefPubMed
7.
go back to reference Job S, Rapoud D, Dos Santos A, Gonzalez P, Desterke C, Pascal G, Elarouci N, Ayadi M, Adam R, Azoulay D, et al. Identification of four Immune Subtypes characterized by distinct composition and functions of Tumor Microenvironment in Intrahepatic Cholangiocarcinoma. Hepatology. 2020;72(3):965–81.CrossRefPubMed Job S, Rapoud D, Dos Santos A, Gonzalez P, Desterke C, Pascal G, Elarouci N, Ayadi M, Adam R, Azoulay D, et al. Identification of four Immune Subtypes characterized by distinct composition and functions of Tumor Microenvironment in Intrahepatic Cholangiocarcinoma. Hepatology. 2020;72(3):965–81.CrossRefPubMed
8.
go back to reference Yugawa K, Itoh S, Yoshizumi T, Iseda N, Tomiyama T, Toshima T, Harada N, Kohashi K, Oda Y, Mori M. Prognostic impact of tumor microvessels in intrahepatic cholangiocarcinoma: association with tumor-infiltrating lymphocytes. Mod Pathol. 2021;34(4):798–807.CrossRefPubMed Yugawa K, Itoh S, Yoshizumi T, Iseda N, Tomiyama T, Toshima T, Harada N, Kohashi K, Oda Y, Mori M. Prognostic impact of tumor microvessels in intrahepatic cholangiocarcinoma: association with tumor-infiltrating lymphocytes. Mod Pathol. 2021;34(4):798–807.CrossRefPubMed
9.
go back to reference Lauss M, Donia M, Svane IM, Jonsson G. B cells and tertiary lymphoid structures: friends or foes in Cancer Immunotherapy? Clin Cancer Res. 2022;28(9):1751–8.CrossRefPubMed Lauss M, Donia M, Svane IM, Jonsson G. B cells and tertiary lymphoid structures: friends or foes in Cancer Immunotherapy? Clin Cancer Res. 2022;28(9):1751–8.CrossRefPubMed
10.
go back to reference Ding GY, Ma JQ, Yun JP, Chen X, Ling Y, Zhang S, Shi JY, Chang YQ, Ji Y, Wang XY, et al. Distribution and density of tertiary lymphoid structures predict clinical outcome in intrahepatic cholangiocarcinoma. J Hepatol. 2022;76(3):608–18.CrossRefPubMed Ding GY, Ma JQ, Yun JP, Chen X, Ling Y, Zhang S, Shi JY, Chang YQ, Ji Y, Wang XY, et al. Distribution and density of tertiary lymphoid structures predict clinical outcome in intrahepatic cholangiocarcinoma. J Hepatol. 2022;76(3):608–18.CrossRefPubMed
11.
go back to reference Chen Y, Liu H, Zhang J, Wu Y, Zhou W, Cheng Z, Lou J, Zheng S, Bi X, Wang J, et al. Prognostic value and predication model of microvascular invasion in patients with intrahepatic cholangiocarcinoma: a multicenter study from China. BMC Cancer. 2021;21(1):1299.CrossRefPubMedPubMedCentral Chen Y, Liu H, Zhang J, Wu Y, Zhou W, Cheng Z, Lou J, Zheng S, Bi X, Wang J, et al. Prognostic value and predication model of microvascular invasion in patients with intrahepatic cholangiocarcinoma: a multicenter study from China. BMC Cancer. 2021;21(1):1299.CrossRefPubMedPubMedCentral
12.
go back to reference Tang Z, Liu W-R, Zhou P-Y, Ding Z-B, Jiang X-F, Wang H, Tian M-X, Tao C-Y, Fang Y, Qu W-F, et al. Prognostic Value and Predication Model of Microvascular Invasion in patients with Intrahepatic Cholangiocarcinoma. J Cancer. 2019;10(22):5575–84.CrossRefPubMedPubMedCentral Tang Z, Liu W-R, Zhou P-Y, Ding Z-B, Jiang X-F, Wang H, Tian M-X, Tao C-Y, Fang Y, Qu W-F, et al. Prognostic Value and Predication Model of Microvascular Invasion in patients with Intrahepatic Cholangiocarcinoma. J Cancer. 2019;10(22):5575–84.CrossRefPubMedPubMedCentral
13.
go back to reference Sun Z, Han X, You W, Tang J, Xu J, Ye B, Li T, Zhang Y, Chen K, Ding Y et al. Adjuvant therapy for cholangiocarcinoma after surgery and prognosis factors for cholangiocarcinoma: a single-center retrospective cohort study. Front Oncol 2023, 13. Sun Z, Han X, You W, Tang J, Xu J, Ye B, Li T, Zhang Y, Chen K, Ding Y et al. Adjuvant therapy for cholangiocarcinoma after surgery and prognosis factors for cholangiocarcinoma: a single-center retrospective cohort study. Front Oncol 2023, 13.
14.
go back to reference Kurebayashi Y, Matsuda K, Ueno A, Tsujikawa H, Yamazaki K, Masugi Y, Kwa WT, Effendi K, Hasegawa Y, Yagi H, et al. Immunovascular classification of HCC reflects reciprocal interaction between immune and angiogenic tumor microenvironments. Hepatology. 2022;75(5):1139–53.CrossRefPubMed Kurebayashi Y, Matsuda K, Ueno A, Tsujikawa H, Yamazaki K, Masugi Y, Kwa WT, Effendi K, Hasegawa Y, Yagi H, et al. Immunovascular classification of HCC reflects reciprocal interaction between immune and angiogenic tumor microenvironments. Hepatology. 2022;75(5):1139–53.CrossRefPubMed
15.
go back to reference Wang Y, Li J, Xia Y, Gong R, Wang K, Yan Z, Wan X, Liu G, Wu D, Shi L, et al. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol. 2013;31(9):1188–95.CrossRefPubMed Wang Y, Li J, Xia Y, Gong R, Wang K, Yan Z, Wan X, Liu G, Wu D, Shi L, et al. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol. 2013;31(9):1188–95.CrossRefPubMed
16.
go back to reference Hyder O, Marques H, Pulitano C, Marsh JW, Alexandrescu S, Bauer TW, Gamblin TC, Sotiropoulos GC, Paul A, Barroso E, et al. A nomogram to predict long-term survival after resection for intrahepatic cholangiocarcinoma: an eastern and western experience. JAMA Surg. 2014;149(5):432–8.CrossRefPubMed Hyder O, Marques H, Pulitano C, Marsh JW, Alexandrescu S, Bauer TW, Gamblin TC, Sotiropoulos GC, Paul A, Barroso E, et al. A nomogram to predict long-term survival after resection for intrahepatic cholangiocarcinoma: an eastern and western experience. JAMA Surg. 2014;149(5):432–8.CrossRefPubMed
17.
go back to reference Doussot A, Groot-Koerkamp B, Wiggers JK, Chou J, Gonen M, DeMatteo RP, Allen PJ, Kingham TP, D’Angelica MI, Jarnagin WR. Outcomes after resection of Intrahepatic Cholangiocarcinoma: external validation and comparison of Prognostic Models. J Am Coll Surg. 2015;221(2):452–61.CrossRefPubMedPubMedCentral Doussot A, Groot-Koerkamp B, Wiggers JK, Chou J, Gonen M, DeMatteo RP, Allen PJ, Kingham TP, D’Angelica MI, Jarnagin WR. Outcomes after resection of Intrahepatic Cholangiocarcinoma: external validation and comparison of Prognostic Models. J Am Coll Surg. 2015;221(2):452–61.CrossRefPubMedPubMedCentral
18.
go back to reference Li T, Qin LX, Zhou J, Sun HC, Qiu SJ, Ye QH, Wang L, Tang ZY, Fan J. Staging, prognostic factors and adjuvant therapy of intrahepatic cholangiocarcinoma after curative resection. Liver Int. 2014;34(6):953–60.CrossRefPubMed Li T, Qin LX, Zhou J, Sun HC, Qiu SJ, Ye QH, Wang L, Tang ZY, Fan J. Staging, prognostic factors and adjuvant therapy of intrahepatic cholangiocarcinoma after curative resection. Liver Int. 2014;34(6):953–60.CrossRefPubMed
19.
go back to reference Zhang X, Li J, Shen F, Lau WY. Significance of presence of microvascular invasion in specimens obtained after surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol. 2018;33(2):347–54.CrossRefPubMed Zhang X, Li J, Shen F, Lau WY. Significance of presence of microvascular invasion in specimens obtained after surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol. 2018;33(2):347–54.CrossRefPubMed
20.
go back to reference Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg. 2005;12(5):351–5.CrossRefPubMed Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg. 2005;12(5):351–5.CrossRefPubMed
21.
go back to reference Calderaro J, Petitprez F, Becht E, Laurent A, Hirsch TZ, Rousseau B, Luciani A, Amaddeo G, Derman J, Charpy C, et al. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J Hepatol. 2019;70(1):58–65.CrossRefPubMed Calderaro J, Petitprez F, Becht E, Laurent A, Hirsch TZ, Rousseau B, Luciani A, Amaddeo G, Derman J, Charpy C, et al. Intra-tumoral tertiary lymphoid structures are associated with a low risk of early recurrence of hepatocellular carcinoma. J Hepatol. 2019;70(1):58–65.CrossRefPubMed
22.
go back to reference Finkin S, Yuan D, Stein I, Taniguchi K, Weber A, Unger K, Browning JL, Goossens N, Nakagawa S, Gunasekaran G, et al. Ectopic lymphoid structures function as microniches for tumor progenitor cells in hepatocellular carcinoma. Nat Immunol. 2015;16(12):1235–44.CrossRefPubMedPubMedCentral Finkin S, Yuan D, Stein I, Taniguchi K, Weber A, Unger K, Browning JL, Goossens N, Nakagawa S, Gunasekaran G, et al. Ectopic lymphoid structures function as microniches for tumor progenitor cells in hepatocellular carcinoma. Nat Immunol. 2015;16(12):1235–44.CrossRefPubMedPubMedCentral
23.
go back to reference Yang SL, Luo YY, Chen M, Zhou YP, Lu FR, Deng DF, Wu YR. A systematic review and meta-analysis comparing the prognosis of multicentric occurrence and vs. intrahepatic metastasis in patients with recurrent hepatocellular carcinoma after hepatectomy. HPB (Oxford). 2017;19(10):835–42.CrossRefPubMed Yang SL, Luo YY, Chen M, Zhou YP, Lu FR, Deng DF, Wu YR. A systematic review and meta-analysis comparing the prognosis of multicentric occurrence and vs. intrahepatic metastasis in patients with recurrent hepatocellular carcinoma after hepatectomy. HPB (Oxford). 2017;19(10):835–42.CrossRefPubMed
24.
go back to reference Bagante F, Spolverato G, Merath K, Weiss M, Alexandrescu S, Marques HP, Aldrighetti L, Maithel SK, Pulitano C, Bauer TW, et al. Intrahepatic cholangiocarcinoma tumor burden: a classification and regression tree model to define prognostic groups after resection. Surgery. 2019;166(6):983–90.CrossRefPubMed Bagante F, Spolverato G, Merath K, Weiss M, Alexandrescu S, Marques HP, Aldrighetti L, Maithel SK, Pulitano C, Bauer TW, et al. Intrahepatic cholangiocarcinoma tumor burden: a classification and regression tree model to define prognostic groups after resection. Surgery. 2019;166(6):983–90.CrossRefPubMed
25.
go back to reference Sahara K, Tsilimigras DI, Mehta R, Bagante F, Guglielmi A, Aldrighetti L, Alexandrescu S, Marques HP, Shen F, Koerkamp BG, et al. A novel online prognostic tool to predict long-term survival after liver resection for intrahepatic cholangiocarcinoma: the metro-ticket paradigm. J Surg Oncol. 2019;120(2):223–30.CrossRefPubMed Sahara K, Tsilimigras DI, Mehta R, Bagante F, Guglielmi A, Aldrighetti L, Alexandrescu S, Marques HP, Shen F, Koerkamp BG, et al. A novel online prognostic tool to predict long-term survival after liver resection for intrahepatic cholangiocarcinoma: the metro-ticket paradigm. J Surg Oncol. 2019;120(2):223–30.CrossRefPubMed
26.
go back to reference Benson AB, D’Angelica MI, Abbott DE, Anaya DA, Anders R, Are C, Bachini M, Borad M, Brown D, Burgoyne A, et al. Hepatobiliary cancers, Version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2021;19(5):541–65.CrossRefPubMed Benson AB, D’Angelica MI, Abbott DE, Anaya DA, Anders R, Are C, Bachini M, Borad M, Brown D, Burgoyne A, et al. Hepatobiliary cancers, Version 2.2021, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2021;19(5):541–65.CrossRefPubMed
27.
go back to reference Oh DY, Lee KH, Lee DW, Yoon J, Kim TY, Bang JH, Nam AR, Oh KS, Kim JM, Lee Y, et al. Gemcitabine and cisplatin plus durvalumab with or without tremelimumab in chemotherapy-naive patients with advanced biliary tract cancer: an open-label, single-centre, phase 2 study. Lancet Gastroenterol Hepatol. 2022;7(6):522–32.CrossRefPubMed Oh DY, Lee KH, Lee DW, Yoon J, Kim TY, Bang JH, Nam AR, Oh KS, Kim JM, Lee Y, et al. Gemcitabine and cisplatin plus durvalumab with or without tremelimumab in chemotherapy-naive patients with advanced biliary tract cancer: an open-label, single-centre, phase 2 study. Lancet Gastroenterol Hepatol. 2022;7(6):522–32.CrossRefPubMed
28.
go back to reference Zhou J, Jia F, Guo-Ming S, Xiao-Yong H, Dong W, Guo-Huan Y, Yuan J, Yi C, Fei L, Jia-Cheng L, et al. Gemox chemotherapy in combination with anti-PD1 antibody toripalimab and lenvatinib as first-line treatment for advanced intrahepatic cholangiocarcinoma: a phase 2 clinical trial. J Clin Oncol. 2021;39(15suppl):4094–4. Zhou J, Jia F, Guo-Ming S, Xiao-Yong H, Dong W, Guo-Huan Y, Yuan J, Yi C, Fei L, Jia-Cheng L, et al. Gemox chemotherapy in combination with anti-PD1 antibody toripalimab and lenvatinib as first-line treatment for advanced intrahepatic cholangiocarcinoma: a phase 2 clinical trial. J Clin Oncol. 2021;39(15suppl):4094–4.
29.
go back to reference Anthony BE-K, Zhenggang R, Hongjae C, Joon Oh P, Jin Won K, Tiziana P, Daneng L, Lyudmila Z, Ming-Huang C, Stephen Paul H, et al. IMbrave151: a phase 2, randomized, double-blind, placebo-controlled study of atezolizumab with or without bevacizumab in combination with cisplatin plus gemcitabine in patients with untreated, advanced biliary tract cancer. J Clin Oncol. 2023;41(4suppl):491–1. Anthony BE-K, Zhenggang R, Hongjae C, Joon Oh P, Jin Won K, Tiziana P, Daneng L, Lyudmila Z, Ming-Huang C, Stephen Paul H, et al. IMbrave151: a phase 2, randomized, double-blind, placebo-controlled study of atezolizumab with or without bevacizumab in combination with cisplatin plus gemcitabine in patients with untreated, advanced biliary tract cancer. J Clin Oncol. 2023;41(4suppl):491–1.
30.
go back to reference Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G, et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–92.CrossRefPubMedPubMedCentral Gu-Trantien C, Loi S, Garaud S, Equeter C, Libin M, de Wind A, Ravoet M, Le Buanec H, Sibille C, Manfouo-Foutsop G, et al. CD4(+) follicular helper T cell infiltration predicts breast cancer survival. J Clin Invest. 2013;123(7):2873–92.CrossRefPubMedPubMedCentral
31.
go back to reference Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8 + T cells. Cancer Res. 2014;74(3):705–15.CrossRefPubMed Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, Knockaert S, de Chaisemartin L, Ouakrim H, Becht E, Alifano M, et al. Dendritic cells in tumor-associated tertiary lymphoid structures signal a Th1 cytotoxic immune contexture and license the positive prognostic value of infiltrating CD8 + T cells. Cancer Res. 2014;74(3):705–15.CrossRefPubMed
32.
go back to reference Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are Associated with Tertiary lymphoid structures, cytolytic T-Cell responses, and Superior Prognosis in Ovarian Cancer. Clin Cancer Res. 2016;22(12):3005–15.CrossRefPubMed Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are Associated with Tertiary lymphoid structures, cytolytic T-Cell responses, and Superior Prognosis in Ovarian Cancer. Clin Cancer Res. 2016;22(12):3005–15.CrossRefPubMed
33.
go back to reference Hennequin A, Derangere V, Boidot R, Apetoh L, Vincent J, Orry D, Fraisse J, Causeret S, Martin F, Arnould L, et al. Tumor infiltration by tbet + effector T cells and CD20 + B cells is associated with survival in gastric cancer patients. Oncoimmunology. 2016;5(2):e1054598.CrossRefPubMed Hennequin A, Derangere V, Boidot R, Apetoh L, Vincent J, Orry D, Fraisse J, Causeret S, Martin F, Arnould L, et al. Tumor infiltration by tbet + effector T cells and CD20 + B cells is associated with survival in gastric cancer patients. Oncoimmunology. 2016;5(2):e1054598.CrossRefPubMed
34.
go back to reference Di Caro G, Bergomas F, Grizzi F, Doni A, Bianchi P, Malesci A, Laghi L, Allavena P, Mantovani A, Marchesi F. Occurrence of tertiary lymphoid tissue is associated with T-cell infiltration and predicts better prognosis in early-stage colorectal cancers. Clin Cancer Res. 2014;20(8):2147–58.CrossRefPubMed Di Caro G, Bergomas F, Grizzi F, Doni A, Bianchi P, Malesci A, Laghi L, Allavena P, Mantovani A, Marchesi F. Occurrence of tertiary lymphoid tissue is associated with T-cell infiltration and predicts better prognosis in early-stage colorectal cancers. Clin Cancer Res. 2014;20(8):2147–58.CrossRefPubMed
35.
go back to reference Zhang J, Wu Z, Zhao J, Liu S, Zhang X, Yuan F, Shi Y, Song B. Intrahepatic cholangiocarcinoma: MRI texture signature as predictive biomarkers of immunophenotyping and survival. Eur Radiol. 2021;31(6):3661–72.CrossRefPubMed Zhang J, Wu Z, Zhao J, Liu S, Zhang X, Yuan F, Shi Y, Song B. Intrahepatic cholangiocarcinoma: MRI texture signature as predictive biomarkers of immunophenotyping and survival. Eur Radiol. 2021;31(6):3661–72.CrossRefPubMed
36.
go back to reference Liang W, Xu L, Yang P, Zhang L, Wan D, Huang Q, Niu T, Chen F. Novel nomogram for preoperative prediction of early recurrence in Intrahepatic Cholangiocarcinoma. Front Oncol. 2018;8:360.CrossRefPubMedPubMedCentral Liang W, Xu L, Yang P, Zhang L, Wan D, Huang Q, Niu T, Chen F. Novel nomogram for preoperative prediction of early recurrence in Intrahepatic Cholangiocarcinoma. Front Oncol. 2018;8:360.CrossRefPubMedPubMedCentral
37.
go back to reference Wang XH, Zhou QF, Wang CM, Xiang CL, Song YH, Li SQ, Chen MS, Xiang SL, Liu CJ, Mao XH. Adjuvant transarterial chemoembolization for intermediate-stage hepatocellular carcinoma with microvascular invasion. Br J Surg 2022. Wang XH, Zhou QF, Wang CM, Xiang CL, Song YH, Li SQ, Chen MS, Xiang SL, Liu CJ, Mao XH. Adjuvant transarterial chemoembolization for intermediate-stage hepatocellular carcinoma with microvascular invasion. Br J Surg 2022.
38.
go back to reference Li SH, Mei J, Cheng Y, Li Q, Wang QX, Fang CK, Lei QC, Huang HK, Cao MR, Luo R et al. Postoperative adjuvant hepatic arterial infusion Chemotherapy with FOLFOX in Hepatocellular Carcinoma with Microvascular Invasion: a Multicenter, Phase III, Randomized Study. J Clin Oncol 2022:JCO2201142. Li SH, Mei J, Cheng Y, Li Q, Wang QX, Fang CK, Lei QC, Huang HK, Cao MR, Luo R et al. Postoperative adjuvant hepatic arterial infusion Chemotherapy with FOLFOX in Hepatocellular Carcinoma with Microvascular Invasion: a Multicenter, Phase III, Randomized Study. J Clin Oncol 2022:JCO2201142.
39.
go back to reference Wang Z, Ren Z, Chen Y, Hu J, Yang G, Yu L, Yang X, Huang A, Zhang X, Zhou S, et al. Adjuvant Transarterial Chemoembolization for HBV-Related Hepatocellular Carcinoma after Resection: a randomized controlled study. Clin Cancer Res. 2018;24(9):2074–81.CrossRefPubMed Wang Z, Ren Z, Chen Y, Hu J, Yang G, Yu L, Yang X, Huang A, Zhang X, Zhou S, et al. Adjuvant Transarterial Chemoembolization for HBV-Related Hepatocellular Carcinoma after Resection: a randomized controlled study. Clin Cancer Res. 2018;24(9):2074–81.CrossRefPubMed
40.
go back to reference Peng Z, Chen S, Xiao H, Wang Y, Li J, Mei J, Chen Z, Zhou Q, Feng S, Chen M, et al. Microvascular Invasion as a predictor of response to treatment with Sorafenib and Transarterial Chemoembolization for Recurrent Intermediate-Stage Hepatocellular Carcinoma. Radiology. 2019;292(1):237–47.CrossRefPubMed Peng Z, Chen S, Xiao H, Wang Y, Li J, Mei J, Chen Z, Zhou Q, Feng S, Chen M, et al. Microvascular Invasion as a predictor of response to treatment with Sorafenib and Transarterial Chemoembolization for Recurrent Intermediate-Stage Hepatocellular Carcinoma. Radiology. 2019;292(1):237–47.CrossRefPubMed
Metadata
Title
Using immunovascular characteristics to predict very early recurrence and prognosis of resectable intrahepatic cholangiocarcinoma
Authors
Ying Xu
Zhuo Li
Yanzhao Zhou
Yi Yang
Jingzhong Ouyang
Lu Li
Zhen Huang
Feng Ye
Jianming Ying
Hong Zhao
Jinxue Zhou
Xinming Zhao
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2023
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/s12885-023-11476-z

Other articles of this Issue 1/2023

BMC Cancer 1/2023 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine