Skip to main content
Top
Published in: Annals of Surgical Oncology 8/2020

01-08-2020 | Cancer Biomarker | Hepatobiliary Tumors

The Impact of Preoperative CA19-9 and CEA on Outcomes of Patients with Intrahepatic Cholangiocarcinoma

Authors: Amika Moro, MD, Rittal Mehta, MPH, BDS, Kota Sahara, MD, Diamantis I. Tsilimigras, MD, Anghela Z. Paredes, MD, MS, Ayesha Farooq, MBBS, J. Madison Hyer, MD, Itaru Endo, MD, PhD, Feng Shen, MD, Alfredo Guglielmi, MD, Luca Aldrighetti, MD, Matthew Weiss, MD, Todd W. Bauer, MD, Sorin Alexandrescu, MD, George A. Poultsides, MD, Shishir K. Maithel, MD, Hugo P. Marques, MD, Guillaume Martel, MD, Carlo Pulitano, MD, Olivier Soubrane, MD, Bas G. Koerkamp, MD, Kazunari Sasaki, MD, Timothy M. Pawlik, MD, MPH, PhD, FACS

Published in: Annals of Surgical Oncology | Issue 8/2020

Login to get access

Abstract

Background

The objective of the current study was to assess the impact of serum CA19-9 and CEA and their combination on survival among patients undergoing surgery for intrahepatic cholangiocarcinoma (ICC).

Methods

Patients who underwent curative-intent resection of ICC between 1990 and 2016 were identified using a multi-institutional database. Patients were categorized into four groups based on combinations of serum CA19-9 and CEA (low vs. high). Factors associated with 1-year mortality after hepatectomy were examined.

Results

Among 588 patients, 5-year OS was considerably better among patients with low CA19-9/low CEA (54.5%) compared with low CA19-9/high CEA (14.6%), high CA19-9/low CEA (10.0%), or high CA19-9/high CEA (0%) (P < 0.001). No difference in 1-year OS existed between patients who had either high CA19-9 (high CA19-9/low CEA: 70.4%) or high CEA levels (low CA19-9/high CEA: 72.5%) (P = 0.92). Although patients with the most favorable tumor marker profile (low CA19-9/low CEA) had the best 1-year survival (87.9%), 15.1% (n = 39) still died within a year of surgery. Among patients with low CA19-9/low CEA, a high neutrophil-to-lymphocyte ratio (NLR) (odds ratio 1.09; 95% confidence interval 1.03-1.64) and large size tumor (odds ratio 3.34; 95% confidence interval 1.40–8.10) were associated with 1-year mortality (P < 0.05).

Conclusions

Patients with either a high CA19-9 and/or high CEA had poor 1-year survival. High NLR and large tumor size were associated with a greater risk of 1-year mortality among patients with favorable tumor marker profile.
Literature
1.
go back to reference Lafaro KJ, Cosgrove D, Geschwind JF, Kamel I, Herman JM, Pawlik TM. Multidisciplinary care of patients with intrahepatic cholangiocarcinoma: updates in management. Gastroenterol Res Pract. 2015;2015:860861.PubMedPubMedCentralCrossRef Lafaro KJ, Cosgrove D, Geschwind JF, Kamel I, Herman JM, Pawlik TM. Multidisciplinary care of patients with intrahepatic cholangiocarcinoma: updates in management. Gastroenterol Res Pract. 2015;2015:860861.PubMedPubMedCentralCrossRef
2.
go back to reference Wu L, Tsilimigras DI, Paredes AZ, et al. Trends in the incidence, treatment and outcomes of patients with intrahepatic cholangiocarcinoma in the USA: facility type is associated with margin status, use of lymphadenectomy and overall survival. World J Surg. 2019. Wu L, Tsilimigras DI, Paredes AZ, et al. Trends in the incidence, treatment and outcomes of patients with intrahepatic cholangiocarcinoma in the USA: facility type is associated with margin status, use of lymphadenectomy and overall survival. World J Surg. 2019.
3.
go back to reference Bridgewater J, Galle PR, Khan SA, et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J Hepatol. 2014;60(6):1268–89.PubMedCrossRef Bridgewater J, Galle PR, Khan SA, et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. J Hepatol. 2014;60(6):1268–89.PubMedCrossRef
4.
go back to reference Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM. Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: systematic review and meta-analysistreatment of intrahepatic cholangiocarcinomatreatment of intrahepatic cholangiocarcinoma. JAMA Surg. 2014;149(6):565–74.PubMedCrossRef Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM. Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: systematic review and meta-analysistreatment of intrahepatic cholangiocarcinomatreatment of intrahepatic cholangiocarcinoma. JAMA Surg. 2014;149(6):565–74.PubMedCrossRef
5.
go back to reference Amini N, Ejaz A, Spolverato G, Kim Y, Herman JM, Pawlik TM. Temporal trends in liver-directed therapy of patients with intrahepatic cholangiocarcinoma in the United States: a population-based analysis. J Surg Oncol. 2014;110(2):163–70.PubMedCrossRef Amini N, Ejaz A, Spolverato G, Kim Y, Herman JM, Pawlik TM. Temporal trends in liver-directed therapy of patients with intrahepatic cholangiocarcinoma in the United States: a population-based analysis. J Surg Oncol. 2014;110(2):163–70.PubMedCrossRef
6.
go back to reference Weber SM, Ribero D, O’Reilly EM, Kokudo N, Miyazaki M, Pawlik TM. Intrahepatic cholangiocarcinoma: expert consensus statement. HPB. 2015;17(8):669–80.PubMedPubMedCentralCrossRef Weber SM, Ribero D, O’Reilly EM, Kokudo N, Miyazaki M, Pawlik TM. Intrahepatic cholangiocarcinoma: expert consensus statement. HPB. 2015;17(8):669–80.PubMedPubMedCentralCrossRef
7.
go back to reference Zhang XF, Beal EW, Bagante F, et al. Early versus late recurrence of intrahepatic cholangiocarcinoma after resection with curative intent. Br J Surg. 2018;105(7):848–56.PubMedCrossRef Zhang XF, Beal EW, Bagante F, et al. Early versus late recurrence of intrahepatic cholangiocarcinoma after resection with curative intent. Br J Surg. 2018;105(7):848–56.PubMedCrossRef
8.
go back to reference Poultsides GA, Zhu AX, Choti MA, Pawlik TM. Intrahepatic cholangiocarcinoma. Surg Clin N Am. 2010;90(4):817–37.PubMedCrossRef Poultsides GA, Zhu AX, Choti MA, Pawlik TM. Intrahepatic cholangiocarcinoma. Surg Clin N Am. 2010;90(4):817–37.PubMedCrossRef
9.
go back to reference Fang T, Wang H, Wang Y, Lin X, Cui Y, Wang Z. Clinical significance of preoperative serum CEA, CA125, and CA19-9 levels in predicting the resectability of cholangiocarcinoma. Dis Markers. 2019;2019:6016931.PubMedPubMedCentral Fang T, Wang H, Wang Y, Lin X, Cui Y, Wang Z. Clinical significance of preoperative serum CEA, CA125, and CA19-9 levels in predicting the resectability of cholangiocarcinoma. Dis Markers. 2019;2019:6016931.PubMedPubMedCentral
10.
go back to reference Amin MB, Greene FL, Edge SB, et al. 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(2):93–9. Amin MB, Greene FL, Edge SB, et al. 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(2):93–9.
11.
go back to reference Sasaki K, Margonis GA, Andreatos N, et al. Serum tumor markers enhance the predictive power of the AJCC and LCSGJ staging systems in resectable intrahepatic cholangiocarcinoma. HPB. 2018;20(10):956–65.PubMedCrossRef Sasaki K, Margonis GA, Andreatos N, et al. Serum tumor markers enhance the predictive power of the AJCC and LCSGJ staging systems in resectable intrahepatic cholangiocarcinoma. HPB. 2018;20(10):956–65.PubMedCrossRef
12.
go back to reference Loosen SH, Roderburg C, Kauertz KL, et al. CEA but not CA19-9 is an independent prognostic factor in patients undergoing resection of cholangiocarcinoma. Scientific Rep. 2017;7(1):16975.CrossRef Loosen SH, Roderburg C, Kauertz KL, et al. CEA but not CA19-9 is an independent prognostic factor in patients undergoing resection of cholangiocarcinoma. Scientific Rep. 2017;7(1):16975.CrossRef
13.
go back to reference Wang Y, Li J, Xia Y, et al. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol. 2013;31(9):1188–95.PubMedCrossRef Wang Y, Li J, Xia Y, et al. Prognostic nomogram for intrahepatic cholangiocarcinoma after partial hepatectomy. J Clin Oncol. 2013;31(9):1188–95.PubMedCrossRef
14.
go back to reference Das V, Kalita J, Pal M. Predictive and prognostic biomarkers in colorectal cancer: a systematic review of recent advances and challenges. Biomed Pharmacother. 2017;87:8–19.PubMedCrossRef Das V, Kalita J, Pal M. Predictive and prognostic biomarkers in colorectal cancer: a systematic review of recent advances and challenges. Biomed Pharmacother. 2017;87:8–19.PubMedCrossRef
15.
go back to reference Mattiucci GC, Morganti AG, Cellini F, et al. Prognostic impact of presurgical ca19-9 level in pancreatic adenocarcinoma: a pooled analysis. Transl Oncol. 2019;12(1):1–7.PubMedCrossRef Mattiucci GC, Morganti AG, Cellini F, et al. Prognostic impact of presurgical ca19-9 level in pancreatic adenocarcinoma: a pooled analysis. Transl Oncol. 2019;12(1):1–7.PubMedCrossRef
16.
go back to reference Uson Junior PLS, Callegaro-Filho D, Bugano DDG, Moura F, Maluf FC. predictive value of serum carbohydrate antigen 19-9 (CA19-9) for early mortality in advanced pancreatic cancer. J Gastrointest Cancer. 2018;49(4):481–6.PubMedCrossRef Uson Junior PLS, Callegaro-Filho D, Bugano DDG, Moura F, Maluf FC. predictive value of serum carbohydrate antigen 19-9 (CA19-9) for early mortality in advanced pancreatic cancer. J Gastrointest Cancer. 2018;49(4):481–6.PubMedCrossRef
17.
go back to reference Margonis GA, Sasaki K, Gholami S, et al. Genetic And Morphological Evaluation (GAME) score for patients with colorectal liver metastases. Br J Surg. 2018;105(9):1210–20.PubMedCrossRef Margonis GA, Sasaki K, Gholami S, et al. Genetic And Morphological Evaluation (GAME) score for patients with colorectal liver metastases. Br J Surg. 2018;105(9):1210–20.PubMedCrossRef
18.
go back to reference Sasaki K, Margonis GA, Andreatos N, et al. Pre-hepatectomy carcinoembryonic antigen (CEA) levels among patients undergoing resection of colorectal liver metastases: do CEA levels still have prognostic implications? HPB: the official journal of the International Hepato Pancreato Biliary Association. Dec 2016;18(12):1000–9.CrossRef Sasaki K, Margonis GA, Andreatos N, et al. Pre-hepatectomy carcinoembryonic antigen (CEA) levels among patients undergoing resection of colorectal liver metastases: do CEA levels still have prognostic implications? HPB: the official journal of the International Hepato Pancreato Biliary Association. Dec 2016;18(12):1000–9.CrossRef
19.
go back to reference Yamamoto Y, Sugiura T, Todaka A, et al. Surgical indication for advanced intrahepatic cholangiocarcinoma according to the optimal preoperative carbohydrate antigen 19-9 cutoff value. World J Surg. 2018;42(10):3331–40.PubMedCrossRef Yamamoto Y, Sugiura T, Todaka A, et al. Surgical indication for advanced intrahepatic cholangiocarcinoma according to the optimal preoperative carbohydrate antigen 19-9 cutoff value. World J Surg. 2018;42(10):3331–40.PubMedCrossRef
20.
go back to reference He C, Zhang Y, Song Y, et al. Preoperative CEA levels are supplementary to CA19-9 levels in predicting prognosis in patients with resectable intrahepatic cholangiocarcinoma. J Cancer. 2018;9(17):3117–28.PubMedPubMedCentralCrossRef He C, Zhang Y, Song Y, et al. Preoperative CEA levels are supplementary to CA19-9 levels in predicting prognosis in patients with resectable intrahepatic cholangiocarcinoma. J Cancer. 2018;9(17):3117–28.PubMedPubMedCentralCrossRef
21.
go back to reference Yamada T, Nakanishi Y, Okamura K, et al. Impact of serum carbohydrate antigen 19-9 level on prognosis and prediction of lymph node metastasis in patients with intrahepatic cholangiocarcinoma. J Gastroenterol Hepatol. 2018. Yamada T, Nakanishi Y, Okamura K, et al. Impact of serum carbohydrate antigen 19-9 level on prognosis and prediction of lymph node metastasis in patients with intrahepatic cholangiocarcinoma. J Gastroenterol Hepatol. 2018.
22.
go back to reference Buettner S, Spolverato G, Kimbrough CW, et al. The impact of neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio among patients with intrahepatic cholangiocarcinoma. Surgery. 2018;164(3):411–8.PubMedCrossRef Buettner S, Spolverato G, Kimbrough CW, et al. The impact of neutrophil-to-lymphocyte ratio and platelet-to-lymphocyte ratio among patients with intrahepatic cholangiocarcinoma. Surgery. 2018;164(3):411–8.PubMedCrossRef
23.
go back to reference Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepato-biliary-pancreatic Surg. 2005;12(5):351–5.CrossRef Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepato-biliary-pancreatic Surg. 2005;12(5):351–5.CrossRef
24.
go back to reference L Camp R, Dolled-Filhart M, L Rimm D. X-Tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Vol 102004. L Camp R, Dolled-Filhart M, L Rimm D. X-Tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Vol 102004.
25.
go back to reference Camp RL, Dolled-Filhart M, Rimm DL. X-Tile. A New Bio-Informatics Tool for Biomarker Assessment and Outcome-Based Cut-Point Optimization. 2004;10(21):7252–9. Camp RL, Dolled-Filhart M, Rimm DL. X-Tile. A New Bio-Informatics Tool for Biomarker Assessment and Outcome-Based Cut-Point Optimization. 2004;10(21):7252–9.
26.
go back to reference Facciabene A, Peng X, Hagemann IS, et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature. 2011;475(7355):226–30.PubMedCrossRef Facciabene A, Peng X, Hagemann IS, et al. Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and T(reg) cells. Nature. 2011;475(7355):226–30.PubMedCrossRef
27.
go back to reference Mahmoud SM, Paish EC, Powe DG, et al. Tumor-infiltrating CD8 + lymphocytes predict clinical outcome in breast cancer. J Clin Oncol. 2011;29(15):1949–55.PubMedCrossRef Mahmoud SM, Paish EC, Powe DG, et al. Tumor-infiltrating CD8 + lymphocytes predict clinical outcome in breast cancer. J Clin Oncol. 2011;29(15):1949–55.PubMedCrossRef
28.
go back to reference Zhang J-X, Song W, Chen Z-H, et al. Prognostic and predictive value of a microRNA signature in stage II colon cancer: a microRNA expression analysis. The Lancet Oncology. 2013/12/01/2013;14(13):1295–306. Zhang J-X, Song W, Chen Z-H, et al. Prognostic and predictive value of a microRNA signature in stage II colon cancer: a microRNA expression analysis. The Lancet Oncology. 2013/12/01/2013;14(13):1295–306.
29.
go back to reference Le Roy B, Gelli M, Pittau G, et al. Neoadjuvant chemotherapy for initially unresectable intrahepatic cholangiocarcinoma. Br J Surg. 2018;105(7):839–47.PubMedCrossRef Le Roy B, Gelli M, Pittau G, et al. Neoadjuvant chemotherapy for initially unresectable intrahepatic cholangiocarcinoma. Br J Surg. 2018;105(7):839–47.PubMedCrossRef
30.
go back to reference Konstantinidis IT, Groot Koerkamp B, Do RK, et al. Unresectable intrahepatic cholangiocarcinoma: Systemic plus hepatic arterial infusion chemotherapy is associated with longer survival in comparison with systemic chemotherapy alone. Cancer. 2016;122(5):758–65.PubMedCrossRef Konstantinidis IT, Groot Koerkamp B, Do RK, et al. Unresectable intrahepatic cholangiocarcinoma: Systemic plus hepatic arterial infusion chemotherapy is associated with longer survival in comparison with systemic chemotherapy alone. Cancer. 2016;122(5):758–65.PubMedCrossRef
31.
go back to reference Bergquist JR, Ivanics T, Storlie CB, et al. Implications of CA19-9 elevation for survival, staging, and treatment sequencing in intrahepatic cholangiocarcinoma: a national cohort analysis. J Surg Oncol. 2016;114(4):475–82.PubMedPubMedCentralCrossRef Bergquist JR, Ivanics T, Storlie CB, et al. Implications of CA19-9 elevation for survival, staging, and treatment sequencing in intrahepatic cholangiocarcinoma: a national cohort analysis. J Surg Oncol. 2016;114(4):475–82.PubMedPubMedCentralCrossRef
32.
go back to reference Sahara K, Tsilimigras DI, Mehta R, 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. Sahara K, Tsilimigras DI, Mehta R, 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.
33.
go back to reference Yoh T, Seo S, Hatano E, et al. A novel biomarker-based preoperative prognostic grading system for predicting survival after surgery for intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2017;24(5):1351–7.PubMedCrossRef Yoh T, Seo S, Hatano E, et al. A novel biomarker-based preoperative prognostic grading system for predicting survival after surgery for intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2017;24(5):1351–7.PubMedCrossRef
34.
go back to reference Ferrone CR, Finkelstein DM, Thayer SP, Muzikansky A, Fernandez-delCastillo C, Warshaw AL. Perioperative CA19-9 levels can predict stage and survival in patients with resectable pancreatic adenocarcinoma. J Clin Oncol. 2006;24(18):2897–902.PubMedCrossRef Ferrone CR, Finkelstein DM, Thayer SP, Muzikansky A, Fernandez-delCastillo C, Warshaw AL. Perioperative CA19-9 levels can predict stage and survival in patients with resectable pancreatic adenocarcinoma. J Clin Oncol. 2006;24(18):2897–902.PubMedCrossRef
35.
go back to reference Liu F, Hu HJ, Ma WJ, Yang Q, Wang JK, Li FY. Prognostic significance of neutrophil-lymphocyte ratio and carbohydrate antigen 19-9 in patients with gallbladder carcinoma. Medicine. 2019;98(8):e14550.PubMedPubMedCentralCrossRef Liu F, Hu HJ, Ma WJ, Yang Q, Wang JK, Li FY. Prognostic significance of neutrophil-lymphocyte ratio and carbohydrate antigen 19-9 in patients with gallbladder carcinoma. Medicine. 2019;98(8):e14550.PubMedPubMedCentralCrossRef
36.
go back to reference Vestergaard EM, Hein HO, Meyer H, et al. Reference values and biological variation for tumor marker CA 19-9 in serum for different lewis and secretor genotypes and evaluation of secretor and lewis genotyping in a caucasian population. Clin Chem. 1999;45(1):54–61.PubMed Vestergaard EM, Hein HO, Meyer H, et al. Reference values and biological variation for tumor marker CA 19-9 in serum for different lewis and secretor genotypes and evaluation of secretor and lewis genotyping in a caucasian population. Clin Chem. 1999;45(1):54–61.PubMed
37.
go back to reference Jing CY, Fu YP, Shen HJ, et al. Albumin to gamma-glutamyltransferase ratio as a prognostic indicator in intrahepatic cholangiocarcinoma after curative resection. Oncotarget. 2017;8(8):13293–303.PubMedCrossRef Jing CY, Fu YP, Shen HJ, et al. Albumin to gamma-glutamyltransferase ratio as a prognostic indicator in intrahepatic cholangiocarcinoma after curative resection. Oncotarget. 2017;8(8):13293–303.PubMedCrossRef
38.
go back to reference Sun KY, Xu JB, Chen SL, et al. Novel immunological and nutritional-based prognostic index for gastric cancer. World J Gastroenterol. 2015;21(19):5961–71.PubMedPubMedCentralCrossRef Sun KY, Xu JB, Chen SL, et al. Novel immunological and nutritional-based prognostic index for gastric cancer. World J Gastroenterol. 2015;21(19):5961–71.PubMedPubMedCentralCrossRef
39.
go back to reference Akgul O, Bagante F, Olsen G, et al. Preoperative prognostic nutritional index predicts survival of patients with intrahepatic cholangiocarcinoma after curative resection. J Surg Oncol. 2018;118(3):422–30.PubMed Akgul O, Bagante F, Olsen G, et al. Preoperative prognostic nutritional index predicts survival of patients with intrahepatic cholangiocarcinoma after curative resection. J Surg Oncol. 2018;118(3):422–30.PubMed
40.
go back to reference Bagante F, Tran TB, Postlewait LM, et al. Neutrophil-lymphocyte and platelet-lymphocyte ratio as predictors of disease specific survival after resection of adrenocortical carcinoma. J Surg Oncol. 2015;112(2):164–72.PubMedPubMedCentralCrossRef Bagante F, Tran TB, Postlewait LM, et al. Neutrophil-lymphocyte and platelet-lymphocyte ratio as predictors of disease specific survival after resection of adrenocortical carcinoma. J Surg Oncol. 2015;112(2):164–72.PubMedPubMedCentralCrossRef
41.
go back to reference Spolverato G, Maqsood H, Kim Y, et al. Neutrophil-lymphocyte and platelet-lymphocyte ratio in patients after resection for hepato-pancreatico-biliary malignancies. J Surg Oncol. 2015;111(7):868–74.PubMedCrossRef Spolverato G, Maqsood H, Kim Y, et al. Neutrophil-lymphocyte and platelet-lymphocyte ratio in patients after resection for hepato-pancreatico-biliary malignancies. J Surg Oncol. 2015;111(7):868–74.PubMedCrossRef
42.
go back to reference Borazan E, Balik AA, Bozdag Z, et al. Assessment of the relationship between neutrophil lymphocyte ratio and prognostic factors in non-metastatic colorectal cancer. Turkish J Surg. 2017;33(3):185–9.CrossRef Borazan E, Balik AA, Bozdag Z, et al. Assessment of the relationship between neutrophil lymphocyte ratio and prognostic factors in non-metastatic colorectal cancer. Turkish J Surg. 2017;33(3):185–9.CrossRef
43.
go back to reference Tang H, Lu W, Li B, Li C, Xu Y, Dong J. Prognostic significance of neutrophil-to-lymphocyte ratio in biliary tract cancers: a systematic review and meta-analysis. Oncotarget. 2017;8(22):36857–68.PubMedPubMedCentralCrossRef Tang H, Lu W, Li B, Li C, Xu Y, Dong J. Prognostic significance of neutrophil-to-lymphocyte ratio in biliary tract cancers: a systematic review and meta-analysis. Oncotarget. 2017;8(22):36857–68.PubMedPubMedCentralCrossRef
44.
go back to reference Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev. 2013;13(11):759–71.CrossRef Elinav E, Nowarski R, Thaiss CA, Hu B, Jin C, Flavell RA. Inflammation-induced cancer: crosstalk between tumours, immune cells and microorganisms. Nat Rev. 2013;13(11):759–71.CrossRef
45.
go back to reference Templeton AJ, McNamara MG, Seruga B, et al. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst. 2014;106(6):dju124. Templeton AJ, McNamara MG, Seruga B, et al. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J Natl Cancer Inst. 2014;106(6):dju124.
46.
go back to reference Petrie HT, Klassen LW, Kay HD. Inhibition of human cytotoxic T lymphocyte activity in vitro by autologous peripheral blood granulocytes. Journal of immunology (Baltimore, Md.: 1950). 1985;134(1):230–4. Petrie HT, Klassen LW, Kay HD. Inhibition of human cytotoxic T lymphocyte activity in vitro by autologous peripheral blood granulocytes. Journal of immunology (Baltimore, Md.: 1950). 1985;134(1):230–4.
47.
go back to reference Coffelt SB, Wellenstein MD, de Visser KE. Neutrophils in cancer: neutral no more. Nat Rev. 2016;16(7):431–46.CrossRef Coffelt SB, Wellenstein MD, de Visser KE. Neutrophils in cancer: neutral no more. Nat Rev. 2016;16(7):431–46.CrossRef
48.
go back to reference el-Hag A, Clark RA. Immunosuppression by activated human neutrophils. Dependence on the myeloperoxidase system. J Immunol (Baltimore, Md.: 1950). 1987;139(7):2406–13. el-Hag A, Clark RA. Immunosuppression by activated human neutrophils. Dependence on the myeloperoxidase system. J Immunol (Baltimore, Md.: 1950). 1987;139(7):2406–13.
49.
go back to reference Sia D, Hoshida Y, Villanueva A, et al. Integrative molecular analysis of intrahepatic cholangiocarcinoma reveals 2 classes that have different outcomes. Gastroenterology. 2013;144(4):829–40.PubMedPubMedCentralCrossRef Sia D, Hoshida Y, Villanueva A, et al. Integrative molecular analysis of intrahepatic cholangiocarcinoma reveals 2 classes that have different outcomes. Gastroenterology. 2013;144(4):829–40.PubMedPubMedCentralCrossRef
Metadata
Title
The Impact of Preoperative CA19-9 and CEA on Outcomes of Patients with Intrahepatic Cholangiocarcinoma
Authors
Amika Moro, MD
Rittal Mehta, MPH, BDS
Kota Sahara, MD
Diamantis I. Tsilimigras, MD
Anghela Z. Paredes, MD, MS
Ayesha Farooq, MBBS
J. Madison Hyer, MD
Itaru Endo, MD, PhD
Feng Shen, MD
Alfredo Guglielmi, MD
Luca Aldrighetti, MD
Matthew Weiss, MD
Todd W. Bauer, MD
Sorin Alexandrescu, MD
George A. Poultsides, MD
Shishir K. Maithel, MD
Hugo P. Marques, MD
Guillaume Martel, MD
Carlo Pulitano, MD
Olivier Soubrane, MD
Bas G. Koerkamp, MD
Kazunari Sasaki, MD
Timothy M. Pawlik, MD, MPH, PhD, FACS
Publication date
01-08-2020
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 8/2020
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-020-08350-8

Other articles of this Issue 8/2020

Annals of Surgical Oncology 8/2020 Go to the issue