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Published in: Journal of Gastrointestinal Surgery 11/2019

Open Access 01-11-2019 | Metastasis | Original Article

Survival after Resection of Multiple Tumor Foci of Intrahepatic Cholangiocarcinoma

Authors: Stefan Buettner, David W. G. ten Cate, Fabio Bagante, Sorin Alexandrescu, Hugo P. Marques, Jorge Lamelas, Luca Aldrighetti, T. Clark Gamblin, Shishir K. Maithel, Carlo Pulitano, Georgios Antonios Margonis, Matthew Weiss, Todd W. Bauer, Feng Shen, George A. Poultsides, J. Wallis Marsh, Jan N. M. IJzermans, Timothy M. Pawlik, Bas Groot Koerkamp

Published in: Journal of Gastrointestinal Surgery | Issue 11/2019

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Abstract

Background

Multiple tumor foci of intrahepatic cholangiocarcinoma (ICC) are often considered a contra-indication for resection. We sought to define long-term outcomes after resection of ICC in patients with multiple foci.

Methods

Patients who underwent resection for ICC between 1990 and 2017 were identified from 12 major HPB centers. Outcomes of patients with solitary lesions, multiple lesions (ML), and oligometastases (OM) were compared. OM were defined as extrahepatic metastases spread to a single organ.

Results

One thousand thirteen patients underwent resection of ICC. On final pathology, 185 patients (18.4%) had ML and 27 (2.7%) had OM. Median survival of patients with a solitary tumor was 43.2 months, while the median survival of patients with 2 tumors was 21.2 months; the median survival of patients with 3 or more tumors was 15.3 months (p < 0.001). Five-year survival was 43.3%, 28.0%, and 8.6%, respectively. The median survival of patients without OM was 37.8 months versus 14.9 months among patients with OM (p < 0.001); estimated 5-year survival was 39.3% and 10.6%, respectively. In multivariable analysis, the presence of two lesions was not an independent poor prognostic factor for OS (HR 1.19; 95%CI 0.90–1.57; p = 0.229). However, the presence of three or more tumors was an independent poor prognostic factor for OS (HR 1.97; 95%CI 1.48–2.64; p < 0.001).

Conclusion

Resection of multiple liver tumors for patients with ICC did not preclude 5-year survival: in particular, estimated 5-year OS for resection of two tumors was 28.0%.
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Literature
1.
go back to reference Shin HR, Oh JK, Masuyer E, Curado MP, Bouvard V, Fang Y, et al. Comparison of incidence of intrahepatic and extrahepatic cholangiocarcinoma--focus on East and South-Eastern Asia. Asian Pac J Cancer Prev. 2010;11(5):1159–66.PubMed Shin HR, Oh JK, Masuyer E, Curado MP, Bouvard V, Fang Y, et al. Comparison of incidence of intrahepatic and extrahepatic cholangiocarcinoma--focus on East and South-Eastern Asia. Asian Pac J Cancer Prev. 2010;11(5):1159–66.PubMed
2.
go back to reference Singal AK, Vauthey JN, Grady JJ, Stroehlein JR. Intra-hepatic cholangiocarcinoma--frequency and demographic patterns: thirty-year data from the M.D. Anderson Cancer Center. J Cancer Res Clin Oncol. 2011;137(7):1071–8.PubMed Singal AK, Vauthey JN, Grady JJ, Stroehlein JR. Intra-hepatic cholangiocarcinoma--frequency and demographic patterns: thirty-year data from the M.D. Anderson Cancer Center. J Cancer Res Clin Oncol. 2011;137(7):1071–8.PubMed
3.
go back to reference Poultsides GA, Zhu AX, Choti MA, Pawlik TM. Intrahepatic cholangiocarcinoma. Surg Clin North Am. 2010;90(4):817–37.PubMed Poultsides GA, Zhu AX, Choti MA, Pawlik TM. Intrahepatic cholangiocarcinoma. Surg Clin North Am. 2010;90(4):817–37.PubMed
4.
go back to reference Cillo U, Spolverato G, Vitale A, Ejaz A, Lonardi S, Cosgrove D, et al. Liver Resection for Advanced Intrahepatic Cholangiocarcinoma: A Cost-Utility Analysis. World J Surg. 2015;39(10):2500–9.PubMed Cillo U, Spolverato G, Vitale A, Ejaz A, Lonardi S, Cosgrove D, et al. Liver Resection for Advanced Intrahepatic Cholangiocarcinoma: A Cost-Utility Analysis. World J Surg. 2015;39(10):2500–9.PubMed
5.
go back to reference Esnaola NF, Meyer JE, Karachristos A, Maranki JL, Camp ER, Denlinger CS. Evaluation and management of intrahepatic and extrahepatic cholangiocarcinoma. Cancer. 2016;122(9):1349–69.PubMed Esnaola NF, Meyer JE, Karachristos A, Maranki JL, Camp ER, Denlinger CS. Evaluation and management of intrahepatic and extrahepatic cholangiocarcinoma. Cancer. 2016;122(9):1349–69.PubMed
6.
go back to reference Welzel TM, Graubard BI, El-Serag HB, Shaib YH, Hsing AW, Davila JA, et al. Risk factors for intrahepatic and extrahepatic cholangiocarcinoma in the United States: a population-based case-control study. Clin Gastroenterol Hepatol. 2007;5(10):1221–8.PubMedPubMedCentral Welzel TM, Graubard BI, El-Serag HB, Shaib YH, Hsing AW, Davila JA, et al. Risk factors for intrahepatic and extrahepatic cholangiocarcinoma in the United States: a population-based case-control study. Clin Gastroenterol Hepatol. 2007;5(10):1221–8.PubMedPubMedCentral
7.
go back to reference Nakanuma Y CM, Franceschi S, Gores G, Paradis V, Sripa B. Intrahepatic cholangiocarcinoma. WHO classification of tumours of the digestive system. 4th ed. Lyon 2010. Nakanuma Y CM, Franceschi S, Gores G, Paradis V, Sripa B. Intrahepatic cholangiocarcinoma. WHO classification of tumours of the digestive system. 4th ed. Lyon 2010.
8.
go back to reference Malhi H, Gores GJ. Cholangiocarcinoma: modern advances in understanding a deadly old disease. J Hepatol. 2006;45(6):856–67.PubMedPubMedCentral Malhi H, Gores GJ. Cholangiocarcinoma: modern advances in understanding a deadly old disease. J Hepatol. 2006;45(6):856–67.PubMedPubMedCentral
9.
go back to reference Khan SA, Thomas HC, Davidson BR, Taylor-Robinson SD. Cholangiocarcinoma. Lancet. 2005;366(9493):1303–14.PubMed Khan SA, Thomas HC, Davidson BR, Taylor-Robinson SD. Cholangiocarcinoma. Lancet. 2005;366(9493):1303–14.PubMed
10.
go back to reference Blechacz B, Gores GJ. Cholangiocarcinoma: advances in pathogenesis, diagnosis, and treatment. Hepatology. 2008;48(1):308–21.PubMedPubMedCentral Blechacz B, Gores GJ. Cholangiocarcinoma: advances in pathogenesis, diagnosis, and treatment. Hepatology. 2008;48(1):308–21.PubMedPubMedCentral
11.
go back to reference Khan SA, Toledano MB, Taylor-Robinson SD. Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford). 2008;10(2):77–82.PubMedPubMedCentral Khan SA, Toledano MB, Taylor-Robinson SD. Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford). 2008;10(2):77–82.PubMedPubMedCentral
12.
go back to reference Amin MB, Edge SB, American Joint Committee on C. AJCC cancer staging manual. Eighth edition. Switzerland: Springer; 2017. Amin MB, Edge SB, American Joint Committee on C. AJCC cancer staging manual. Eighth edition. Switzerland: Springer; 2017.
13.
go back to reference Bridgewater J, Galle PR, Khan SA, Llovet JM, Park J-W, Patel T, et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. Journal of Hepatology.60(6):1268–89.PubMed Bridgewater J, Galle PR, Khan SA, Llovet JM, Park J-W, Patel T, et al. Guidelines for the diagnosis and management of intrahepatic cholangiocarcinoma. Journal of Hepatology.60(6):1268–89.PubMed
14.
go back to reference Jarnagin WR, Fong Y, DeMatteo RP, Gonen M, Burke EC, Bodniewicz BJ, et al. Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg. 2001;234(4):507–17; discussion 17-9.PubMedPubMedCentral Jarnagin WR, Fong Y, DeMatteo RP, Gonen M, Burke EC, Bodniewicz BJ, et al. Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg. 2001;234(4):507–17; discussion 17-9.PubMedPubMedCentral
15.
go back to reference Konstantinidis IT, Groot Koerkamp B, Do RK, Gonen M, Fong Y, Allen PJ, 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.PubMed Konstantinidis IT, Groot Koerkamp B, Do RK, Gonen M, Fong Y, Allen PJ, 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.PubMed
16.
go back to reference Nakeeb A, Tran KQ, Black MJ, Erickson BA, Ritch PS, Quebbeman EJ, et al. Improved survival in resected biliary malignancies. Surgery. 2002;132(4):555–63; discission 63-4.PubMed Nakeeb A, Tran KQ, Black MJ, Erickson BA, Ritch PS, Quebbeman EJ, et al. Improved survival in resected biliary malignancies. Surgery. 2002;132(4):555–63; discission 63-4.PubMed
17.
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.PubMed 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.PubMed
18.
go back to reference Buettner S, Gani F, Amini N, Spolverato G, Kim Y, Kilic A, et al. The relative effect of hospital and surgeon volume on failure to rescue among patients undergoing liver resection for cancer. Surgery. 2016;159(4):1004–12.PubMed Buettner S, Gani F, Amini N, Spolverato G, Kim Y, Kilic A, et al. The relative effect of hospital and surgeon volume on failure to rescue among patients undergoing liver resection for cancer. Surgery. 2016;159(4):1004–12.PubMed
19.
go back to reference Khan AS, Garcia-Aroz S, Ansari MA, Atiq SM, Senter-Zapata M, Fowler K, et al. Assessment and optimization of liver volume before major hepatic resection: Current guidelines and a narrative review. Int J Surg. 2018;52:74–81.PubMed Khan AS, Garcia-Aroz S, Ansari MA, Atiq SM, Senter-Zapata M, Fowler K, et al. Assessment and optimization of liver volume before major hepatic resection: Current guidelines and a narrative review. Int J Surg. 2018;52:74–81.PubMed
20.
go back to reference Lafaro K, Buettner S, Maqsood H, Wagner D, Bagante F, Spolverato G, et al. Defining Post Hepatectomy Liver Insufficiency: Where do We stand? J Gastrointest Surg. 2015;19(11):2079–92.PubMed Lafaro K, Buettner S, Maqsood H, Wagner D, Bagante F, Spolverato G, et al. Defining Post Hepatectomy Liver Insufficiency: Where do We stand? J Gastrointest Surg. 2015;19(11):2079–92.PubMed
21.
go back to reference Zhu AX, Knox JJ. Adjuvant therapy for intrahepatic cholangiocarcinoma: the debate continues. Oncologist. 2012;17(12):1504–7.PubMedPubMedCentral Zhu AX, Knox JJ. Adjuvant therapy for intrahepatic cholangiocarcinoma: the debate continues. Oncologist. 2012;17(12):1504–7.PubMedPubMedCentral
22.
go back to reference Horgan AM, Amir E, Walter T, Knox JJ. Adjuvant therapy in the treatment of biliary tract cancer: a systematic review and meta-analysis. J Clin Oncol. 2012;30(16):1934–40.PubMed Horgan AM, Amir E, Walter T, Knox JJ. Adjuvant therapy in the treatment of biliary tract cancer: a systematic review and meta-analysis. J Clin Oncol. 2012;30(16):1934–40.PubMed
23.
go back to reference Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362(14):1273–81.PubMed Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362(14):1273–81.PubMed
24.
go back to reference Dripps RD. New classification of physical status. Anesthesiology. 1963;24:111. Dripps RD. New classification of physical status. Anesthesiology. 1963;24:111.
25.
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.PubMedPubMedCentral Weber SM, Ribero D, O=Reilly EM, Kokudo N, Miyazaki M, Pawlik TM. Intrahepatic Cholangiocarcinoma: expert consensus statement. HPB 2015;17(8):669–80.PubMedPubMedCentral
27.
go back to reference Camacho JC, Kokabi N, Xing M, Prajapati HJ, El-Rayes B, Kim HS. Modified response evaluation criteria in solid tumors and European Association for The Study of the Liver criteria using delayed-phase imaging at an early time point predict survival in patients with unresectable intrahepatic cholangiocarcinoma following yttrium-90 radioembolization. J Vasc Interv Radiol. 2014;25(2):256–65.PubMed Camacho JC, Kokabi N, Xing M, Prajapati HJ, El-Rayes B, Kim HS. Modified response evaluation criteria in solid tumors and European Association for The Study of the Liver criteria using delayed-phase imaging at an early time point predict survival in patients with unresectable intrahepatic cholangiocarcinoma following yttrium-90 radioembolization. J Vasc Interv Radiol. 2014;25(2):256–65.PubMed
28.
go back to reference Hoffmann RT, Paprottka PM, Schon A, Bamberg F, Haug A, Durr EM, et al. Transarterial hepatic yttrium-90 radioembolization in patients with unresectable intrahepatic cholangiocarcinoma: factors associated with prolonged survival. Cardiovasc Intervent Radiol. 2012;35(1):105–16.PubMed Hoffmann RT, Paprottka PM, Schon A, Bamberg F, Haug A, Durr EM, et al. Transarterial hepatic yttrium-90 radioembolization in patients with unresectable intrahepatic cholangiocarcinoma: factors associated with prolonged survival. Cardiovasc Intervent Radiol. 2012;35(1):105–16.PubMed
29.
go back to reference Ibrahim SM, Mulcahy MF, Lewandowski RJ, Sato KT, Ryu RK, Masterson EJ, et al. Treatment of unresectable cholangiocarcinoma using yttrium-90 microspheres: results from a pilot study. Cancer. 2008;113(8):2119–28.PubMed Ibrahim SM, Mulcahy MF, Lewandowski RJ, Sato KT, Ryu RK, Masterson EJ, et al. Treatment of unresectable cholangiocarcinoma using yttrium-90 microspheres: results from a pilot study. Cancer. 2008;113(8):2119–28.PubMed
30.
go back to reference Mouli S, Memon K, Baker T, Benson AB, 3rd, Mulcahy MF, Gupta R, et al. Yttrium-90 radioembolization for intrahepatic cholangiocarcinoma: safety, response, and survival analysis. J Vasc Interv Radiol. 2013;24(8):1227–34.PubMedPubMedCentral Mouli S, Memon K, Baker T, Benson AB, 3rd, Mulcahy MF, Gupta R, et al. Yttrium-90 radioembolization for intrahepatic cholangiocarcinoma: safety, response, and survival analysis. J Vasc Interv Radiol. 2013;24(8):1227–34.PubMedPubMedCentral
31.
go back to reference Rafi S, Piduru SM, El-Rayes B, Kauh JS, Kooby DA, Sarmiento JM, et al. Yttrium-90 radioembolization for unresectable standard-chemorefractory intrahepatic cholangiocarcinoma: survival, efficacy, and safety study. Cardiovasc Intervent Radiol. 2013;36(2):440–8.PubMed Rafi S, Piduru SM, El-Rayes B, Kauh JS, Kooby DA, Sarmiento JM, et al. Yttrium-90 radioembolization for unresectable standard-chemorefractory intrahepatic cholangiocarcinoma: survival, efficacy, and safety study. Cardiovasc Intervent Radiol. 2013;36(2):440–8.PubMed
32.
go back to reference Saxena A, Bester L, Chua TC, Chu FC, Morris DL. Yttrium-90 radiotherapy for unresectable intrahepatic cholangiocarcinoma: a preliminary assessment of this novel treatment option. Ann Surg Oncol. 2010;17(2):484–91.PubMed Saxena A, Bester L, Chua TC, Chu FC, Morris DL. Yttrium-90 radiotherapy for unresectable intrahepatic cholangiocarcinoma: a preliminary assessment of this novel treatment option. Ann Surg Oncol. 2010;17(2):484–91.PubMed
33.
go back to reference Tabrizian P, Jibara G, Hechtman JF, Franssen B, Labow DM, Schwartz ME, et al. Outcomes following resection of intrahepatic cholangiocarcinoma. HPB. 2015;17(4):344–51.PubMed Tabrizian P, Jibara G, Hechtman JF, Franssen B, Labow DM, Schwartz ME, et al. Outcomes following resection of intrahepatic cholangiocarcinoma. HPB. 2015;17(4):344–51.PubMed
34.
go back to reference Baheti AD, Tirumani SH, Shinagare AB, Rosenthal MH, Hornick JL, Ramaiya NH, 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. Abdominal Imaging. 2014;39(6):1193–201.PubMed Baheti AD, Tirumani SH, Shinagare AB, Rosenthal MH, Hornick JL, Ramaiya NH, 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. Abdominal Imaging. 2014;39(6):1193–201.PubMed
35.
go back to reference El Rassi ZE, Partensky C, Scoazec JY, Henry L, Lombard-Bohas C, Maddern G. Peripheral cholangiocarcinoma: presentation, diagnosis, pathology and management. Eur J Surg Oncol. 1999;25(4):375–80.PubMed El Rassi ZE, Partensky C, Scoazec JY, Henry L, Lombard-Bohas C, Maddern G. Peripheral cholangiocarcinoma: presentation, diagnosis, pathology and management. Eur J Surg Oncol. 1999;25(4):375–80.PubMed
36.
go back to reference Fasel JHD, Schenk A. Concepts for Liver Segment Classification: Neither Old Ones nor New Ones, but a Comprehensive One. Journal of clinical imaging science. 2013;3:48-.PubMedPubMedCentral Fasel JHD, Schenk A. Concepts for Liver Segment Classification: Neither Old Ones nor New Ones, but a Comprehensive One. Journal of clinical imaging science. 2013;3:48-.PubMedPubMedCentral
37.
go back to reference Conci S, Ruzzenente A, Viganò L, Ercolani G, Fontana A, Bagante F, et al. Patterns of Distribution of Hepatic Nodules (Single, Satellites or Multifocal) in Intrahepatic Cholangiocarcinoma: Prognostic Impact After Surgery. Annals of Surgical Oncology. 2018;25(12):3719–27.PubMed Conci S, Ruzzenente A, Viganò L, Ercolani G, Fontana A, Bagante F, et al. Patterns of Distribution of Hepatic Nodules (Single, Satellites or Multifocal) in Intrahepatic Cholangiocarcinoma: Prognostic Impact After Surgery. Annals of Surgical Oncology. 2018;25(12):3719–27.PubMed
38.
go back to reference Addeo P, Jedidi I, Locicero A, Faitot F, Oncioiu C, Onea A, et al. Prognostic Impact of Tumor Multinodularity in Intrahepatic Cholangiocarcinoma. Journal of Gastrointestinal Surgery. 2018. Addeo P, Jedidi I, Locicero A, Faitot F, Oncioiu C, Onea A, et al. Prognostic Impact of Tumor Multinodularity in Intrahepatic Cholangiocarcinoma. Journal of Gastrointestinal Surgery. 2018.
39.
go back to reference Nakagohri T, Kinoshita T, Konishi M, Takahashi S, Gotohda N. Surgical Outcome and Prognostic Factors in Intrahepatic Cholangiocarcinoma. World Journal of Surgery. 2008;32(12):2675–80.PubMed Nakagohri T, Kinoshita T, Konishi M, Takahashi S, Gotohda N. Surgical Outcome and Prognostic Factors in Intrahepatic Cholangiocarcinoma. World Journal of Surgery. 2008;32(12):2675–80.PubMed
40.
go back to reference Yoh T, Hatano E, Yamanaka K, Nishio T, Seo S, Taura K, et al. Is Surgical Resection Justified for Advanced Intrahepatic Cholangiocarcinoma? Liver Cancer. 2016;5(4):280–9.PubMedPubMedCentral Yoh T, Hatano E, Yamanaka K, Nishio T, Seo S, Taura K, et al. Is Surgical Resection Justified for Advanced Intrahepatic Cholangiocarcinoma? Liver Cancer. 2016;5(4):280–9.PubMedPubMedCentral
41.
go back to reference Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM. Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: Systematic review and meta-analysis. JAMA Surgery. 2014;149(6):565–74.PubMed Mavros MN, Economopoulos KP, Alexiou VG, Pawlik TM. Treatment and prognosis for patients with intrahepatic cholangiocarcinoma: Systematic review and meta-analysis. JAMA Surgery. 2014;149(6):565–74.PubMed
42.
go back to reference Seidensticker R, Ricke J, Seidensticker M. Integration of chemoembolization and radioembolization into multimodal treatment of cholangiocarcinoma. Best Pract Res Clin Gastroenterol. 2015;29(2):319–32.PubMed Seidensticker R, Ricke J, Seidensticker M. Integration of chemoembolization and radioembolization into multimodal treatment of cholangiocarcinoma. Best Pract Res Clin Gastroenterol. 2015;29(2):319–32.PubMed
44.
go back to reference Llovet JM, Real MI, Montana X, Planas R, Coll S, Aponte J, et al. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet. 2002;359(9319):1734–9.PubMed Llovet JM, Real MI, Montana X, Planas R, Coll S, Aponte J, et al. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet. 2002;359(9319):1734–9.PubMed
45.
go back to reference Konstantinidis IT, Koerkamp BG, Do RKG, Gönen M, Fong Y, Allen PJ, et al. Unresectable Intrahepatic Cholangiocarcinoma: Systemic Plus Hepatic Arterial Infusion Chemotherapy is Associated with Longer Survival Compared to Systemic Chemotherapy Alone. Cancer. 2016;122(5):758–65.PubMed Konstantinidis IT, Koerkamp BG, Do RKG, Gönen M, Fong Y, Allen PJ, et al. Unresectable Intrahepatic Cholangiocarcinoma: Systemic Plus Hepatic Arterial Infusion Chemotherapy is Associated with Longer Survival Compared to Systemic Chemotherapy Alone. Cancer. 2016;122(5):758–65.PubMed
46.
go back to reference Kuhlmann JB, Euringer W, Spangenberg HC, Breidert M, Blum HE, Harder J, et al. Treatment of unresectable cholangiocarcinoma: conventional transarterial chemoembolization compared with drug eluting bead-transarterial chemoembolization and systemic chemotherapy. Eur J Gastroenterol Hepatol. 2012;24(4):437–43.PubMed Kuhlmann JB, Euringer W, Spangenberg HC, Breidert M, Blum HE, Harder J, et al. Treatment of unresectable cholangiocarcinoma: conventional transarterial chemoembolization compared with drug eluting bead-transarterial chemoembolization and systemic chemotherapy. Eur J Gastroenterol Hepatol. 2012;24(4):437–43.PubMed
47.
go back to reference Jin S, Fu Q, Wuyun G, Wuyun T. Management of post-hepatectomy complications. World Journal of Gastroenterology : WJG. 2013;19(44):7983–91.PubMed Jin S, Fu Q, Wuyun G, Wuyun T. Management of post-hepatectomy complications. World Journal of Gastroenterology : WJG. 2013;19(44):7983–91.PubMed
Metadata
Title
Survival after Resection of Multiple Tumor Foci of Intrahepatic Cholangiocarcinoma
Authors
Stefan Buettner
David W. G. ten Cate
Fabio Bagante
Sorin Alexandrescu
Hugo P. Marques
Jorge Lamelas
Luca Aldrighetti
T. Clark Gamblin
Shishir K. Maithel
Carlo Pulitano
Georgios Antonios Margonis
Matthew Weiss
Todd W. Bauer
Feng Shen
George A. Poultsides
J. Wallis Marsh
Jan N. M. IJzermans
Timothy M. Pawlik
Bas Groot Koerkamp
Publication date
01-11-2019
Publisher
Springer US
Published in
Journal of Gastrointestinal Surgery / Issue 11/2019
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-019-04184-2

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