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Published in: Journal of Gastrointestinal Surgery 11/2013

01-11-2013 | Original Article

Patterns and Prognostic Significance of Lymph Node Dissection for Surgical Treatment of Perihilar and Intrahepatic Cholangiocarcinoma

Authors: Alfredo Guglielmi, Andrea Ruzzenente, Tommaso Campagnaro, Alessandro Valdegamberi, Fabio Bagante, Francesca Bertuzzo, Simone Conci, Calogero Iacono

Published in: Journal of Gastrointestinal Surgery | Issue 11/2013

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Abstract

Introduction

The prognostic significance of lymph node dissection (LND), the number and status of harvested lymph nodes (LNs), and the lymph node ratio (LNR) are still under debate in intrahepatic (ICC) and perihilar (PCC) cholangiocarcinoma. The aims of this study were to evaluate the prognostic value of the extent of LN dissection, the number of positive LNs, the distribution of positive LNs along different LN stations, and the LNR in a cohort of patients with ICC and PCC who underwent surgical resection and to compare the different prognostic values of lymph node involvement.

Material and Methods

A retrospective analysis was done evaluating extent of LND, number, status, and location of harvested LNs in a cohort of 145 patients with cholangiocarcinoma submitted to surgical resection with curative intent from 1990 to 2012.

Results

Seventy patients had ICC and 75 had PCC. The median survival times of patients with N0 and N+ tumors were 42 and 19 months in ICC patients (p = 0.05) and 42 and 22 months in PCC patients (p = 0.01). In patients without LN metastases, the median survival times of patients with up to three LNs retrieved and with more than three LNs retrieved were 38 and 69 months in ICC patients (p = 0.05) and 18 and 43 months in PCC patients (p = 0.04), respectively. In N+ patients, the location of positive LNs (hepatoduodenal ligament or other regional stations) did not influence overall survival in ICC or PCC patients (p = 0.6). The median survival times of patients with LNRs of 0 and >0.25 were 43 and 19 months in ICC patients (p = 0.01); the 0–0.25 group did not reach the value. In PCC patients, median survival of 0, 0–0.25, and >0.25 groups of patients were 42, 23, and 11 months (p = 0.01), respectively.

Conclusions

LN metastasis is a major prognostic factor after surgical resection of cholangiocarcinoma. The number of harvested LNs and the LNR showed a high prognostic value in ICC and PCC.
Literature
1.
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.CrossRef Khan SA, Toledano MB, Taylor-Robinson SD. Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford) 2008;10(2): 77–82.CrossRef
2.
go back to reference Nakeeb A, Pitt HA, Sohn TA, Coleman J, Abrams RA, Piantadosi S, Hruban RH, Lillemoe KD, Yeo CJ, Cameron JL. Cholangiocarcinoma. A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg 1996;224(4): 463–473; discussion 473–465.PubMedCrossRef Nakeeb A, Pitt HA, Sohn TA, Coleman J, Abrams RA, Piantadosi S, Hruban RH, Lillemoe KD, Yeo CJ, Cameron JL. Cholangiocarcinoma. A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg 1996;224(4): 463–473; discussion 473–465.PubMedCrossRef
3.
go back to reference DeOliveira ML, Cunningham SC, Cameron JL, Kamangar F, Winter JM, Lillemoe KD, Choti MA, Yeo CJ, Schulick RD. Cholangiocarcinoma: thirty-one-year experience with 564 patients at a single institution. Ann Surg 2007;245(5): 755–762.PubMedCrossRef DeOliveira ML, Cunningham SC, Cameron JL, Kamangar F, Winter JM, Lillemoe KD, Choti MA, Yeo CJ, Schulick RD. Cholangiocarcinoma: thirty-one-year experience with 564 patients at a single institution. Ann Surg 2007;245(5): 755–762.PubMedCrossRef
4.
go back to reference Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Valdegamberi A, Capelli P, Pedica F, Nicoli P, Conci S, Iacono C. Does intrahepatic cholangiocarcinoma have better prognosis compared to perihilar cholangiocarcinoma? J Surg Oncol 2010;101(2): 111–115.PubMed Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Valdegamberi A, Capelli P, Pedica F, Nicoli P, Conci S, Iacono C. Does intrahepatic cholangiocarcinoma have better prognosis compared to perihilar cholangiocarcinoma? J Surg Oncol 2010;101(2): 111–115.PubMed
5.
go back to reference Launois B, Terblanche J, Lakehal M, Catheline JM, Bardaxoglou E, Landen S, Campion JP, Sutherland F, Meunier B. Proximal bile duct cancer: high resectability rate and 5-year survival. Ann Surg 1999;230(2): 266–275.PubMedCrossRef Launois B, Terblanche J, Lakehal M, Catheline JM, Bardaxoglou E, Landen S, Campion JP, Sutherland F, Meunier B. Proximal bile duct cancer: high resectability rate and 5-year survival. Ann Surg 1999;230(2): 266–275.PubMedCrossRef
6.
go back to reference Kitagawa Y, Nagino M, Kamiya J, Uesaka K, Sano T, Yamamoto H, Hayakawa N, Nimura Y. Lymph node metastasis from hilar cholangiocarcinoma: audit of 110 patients who underwent regional and paraaortic node dissection. Ann Surg 2001;233(3): 385–392.PubMedCrossRef Kitagawa Y, Nagino M, Kamiya J, Uesaka K, Sano T, Yamamoto H, Hayakawa N, Nimura Y. Lymph node metastasis from hilar cholangiocarcinoma: audit of 110 patients who underwent regional and paraaortic node dissection. Ann Surg 2001;233(3): 385–392.PubMedCrossRef
7.
go back to reference Lang H, Sotiropoulos GC, Fruhauf NR, Domland M, Paul A, Kind EM, Malago M, Broelsch CE. Extended hepatectomy for intrahepatic cholangiocellular carcinoma (ICC): when is it worthwhile? Single center experience with 27 resections in 50 patients over a 5-year period. Ann Surg 2005;241(1): 134–143.PubMed Lang H, Sotiropoulos GC, Fruhauf NR, Domland M, Paul A, Kind EM, Malago M, Broelsch CE. Extended hepatectomy for intrahepatic cholangiocellular carcinoma (ICC): when is it worthwhile? Single center experience with 27 resections in 50 patients over a 5-year period. Ann Surg 2005;241(1): 134–143.PubMed
8.
go back to reference Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Valdegamberi A, Nicoli P, Cappellani A, Malfermoni G, Iacono C. Intrahepatic cholangiocarcinoma: prognostic factors after surgical resection. World J Surg 2009;33(6): 1247–1254.PubMedCrossRef Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Valdegamberi A, Nicoli P, Cappellani A, Malfermoni G, Iacono C. Intrahepatic cholangiocarcinoma: prognostic factors after surgical resection. World J Surg 2009;33(6): 1247–1254.PubMedCrossRef
9.
go back to reference Valverde A, Bonhomme N, Farges O, Sauvanet A, Flejou JF, Belghiti J. Resection of intrahepatic cholangiocarcinoma: a Western experience. J Hepatobiliary Pancreat Surg 1999;6(2): 122–127.PubMedCrossRef Valverde A, Bonhomme N, Farges O, Sauvanet A, Flejou JF, Belghiti J. Resection of intrahepatic cholangiocarcinoma: a Western experience. J Hepatobiliary Pancreat Surg 1999;6(2): 122–127.PubMedCrossRef
10.
go back to reference Morimoto Y, Tanaka Y, Ito T, Nakahara M, Nakaba H, Nishida T, Fujikawa M, Yamamoto S, Kitagawa T. Long-term survival and prognostic factors in the surgical treatment for intrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Surg 2003;10(6): 432–440.PubMedCrossRef Morimoto Y, Tanaka Y, Ito T, Nakahara M, Nakaba H, Nishida T, Fujikawa M, Yamamoto S, Kitagawa T. Long-term survival and prognostic factors in the surgical treatment for intrahepatic cholangiocarcinoma. J Hepatobiliary Pancreat Surg 2003;10(6): 432–440.PubMedCrossRef
11.
go back to reference Nakagawa T, Kamiyama T, Kurauchi N, Matsushita M, Nakanishi K, Kamachi H, Kudo T, Todo S. Number of lymph node metastases is a significant prognostic factor in intrahepatic cholangiocarcinoma. World J Surg 2005;29(6): 728–733.PubMedCrossRef Nakagawa T, Kamiyama T, Kurauchi N, Matsushita M, Nakanishi K, Kamachi H, Kudo T, Todo S. Number of lymph node metastases is a significant prognostic factor in intrahepatic cholangiocarcinoma. World J Surg 2005;29(6): 728–733.PubMedCrossRef
12.
go back to reference Kondo S, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T, Katoh H. Forty consecutive resections of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins: results of a prospective study. Ann Surg 2004;240(1): 95–101.PubMedCrossRef Kondo S, Hirano S, Ambo Y, Tanaka E, Okushiba S, Morikawa T, Katoh H. Forty consecutive resections of hilar cholangiocarcinoma with no postoperative mortality and no positive ductal margins: results of a prospective study. Ann Surg 2004;240(1): 95–101.PubMedCrossRef
13.
go back to reference Dinant S, Gerhards MF, Rauws EA, Busch OR, Gouma DJ, van Gulik TM. Improved outcome of resection of hilar cholangiocarcinoma (Klatskin tumor). Ann Surg Oncol 2006;13(6): 872–880.PubMedCrossRef Dinant S, Gerhards MF, Rauws EA, Busch OR, Gouma DJ, van Gulik TM. Improved outcome of resection of hilar cholangiocarcinoma (Klatskin tumor). Ann Surg Oncol 2006;13(6): 872–880.PubMedCrossRef
14.
go back to reference Miwa S, Miyagawa S, Kobayashi A, Akahane Y, Nakata T, Mihara M, Kusama K, Soeda J, Ogawa S. Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol 2006;41(9): 893–900.PubMedCrossRef Miwa S, Miyagawa S, Kobayashi A, Akahane Y, Nakata T, Mihara M, Kusama K, Soeda J, Ogawa S. Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol 2006;41(9): 893–900.PubMedCrossRef
15.
go back to reference Nagakawa T, Kayahara M, Ikeda S, Futakawa S, Kakita A, Kawarada H, Matsuno M, Takada T, Takasaki K, Tanimura H, Tashiro S, Yamaoka Y. Biliary tract cancer treatment: results from the Biliary Tract Cancer Statistics Registry in Japan. J Hepatobiliary Pancreat Surg 2002;9(5): 569–575.PubMedCrossRef Nagakawa T, Kayahara M, Ikeda S, Futakawa S, Kakita A, Kawarada H, Matsuno M, Takada T, Takasaki K, Tanimura H, Tashiro S, Yamaoka Y. Biliary tract cancer treatment: results from the Biliary Tract Cancer Statistics Registry in Japan. J Hepatobiliary Pancreat Surg 2002;9(5): 569–575.PubMedCrossRef
16.
go back to reference Hanazaki K, Kajikawa S, Shimozawa N, Shimada K, Hiraguri M, Koide N, Adachi W, Amano J. Prognostic factors of intrahepatic cholangiocarcinoma after hepatic resection: univariate and multivariate analysis. Hepatogastroenterology 2002;49(44): 311–316.PubMed Hanazaki K, Kajikawa S, Shimozawa N, Shimada K, Hiraguri M, Koide N, Adachi W, Amano J. Prognostic factors of intrahepatic cholangiocarcinoma after hepatic resection: univariate and multivariate analysis. Hepatogastroenterology 2002;49(44): 311–316.PubMed
17.
go back to reference Shimada M, Yamashita Y, Aishima S, Shirabe K, Takenaka K, Sugimachi K. Value of lymph node dissection during resection of intrahepatic cholangiocarcinoma. Br J Surg 2001;88(11): 1463–1466.PubMedCrossRef Shimada M, Yamashita Y, Aishima S, Shirabe K, Takenaka K, Sugimachi K. Value of lymph node dissection during resection of intrahepatic cholangiocarcinoma. Br J Surg 2001;88(11): 1463–1466.PubMedCrossRef
18.
go back to reference Lai EC, Lau WY. Aggressive surgical resection for hilar cholangiocarcinoma. ANZ J Surg 2005;75(11): 981–985.PubMedCrossRef Lai EC, Lau WY. Aggressive surgical resection for hilar cholangiocarcinoma. ANZ J Surg 2005;75(11): 981–985.PubMedCrossRef
19.
go back to reference Nishio H, Nagino M, Nimura Y. Surgical management of hilar cholangiocarcinoma: the Nagoya experience. HPB (Oxford) 2005;7(4): 259–262.CrossRef Nishio H, Nagino M, Nimura Y. Surgical management of hilar cholangiocarcinoma: the Nagoya experience. HPB (Oxford) 2005;7(4): 259–262.CrossRef
20.
go back to reference Inoue K, Makuuchi M, Takayama T, Torzilli G, Yamamoto J, Shimada K, Kosuge T, Yamasaki S, Konishi M, Kinoshita T, Miyagawa S, Kawasaki S. Long-term survival and prognostic factors in the surgical treatment of mass-forming type cholangiocarcinoma. Surgery 2000;127(5): 498–505.PubMedCrossRef Inoue K, Makuuchi M, Takayama T, Torzilli G, Yamamoto J, Shimada K, Kosuge T, Yamasaki S, Konishi M, Kinoshita T, Miyagawa S, Kawasaki S. Long-term survival and prognostic factors in the surgical treatment of mass-forming type cholangiocarcinoma. Surgery 2000;127(5): 498–505.PubMedCrossRef
21.
go back to reference Shirabe K, Shimada M, Harimoto N, Sugimachi K, Yamashita Y, Tsujita E, Aishima S. Intrahepatic cholangiocarcinoma: its mode of spreading and therapeutic modalities. Surgery 2002;131(1 Suppl): S159-164.PubMedCrossRef Shirabe K, Shimada M, Harimoto N, Sugimachi K, Yamashita Y, Tsujita E, Aishima S. Intrahepatic cholangiocarcinoma: its mode of spreading and therapeutic modalities. Surgery 2002;131(1 Suppl): S159-164.PubMedCrossRef
22.
go back to reference Tamandl D, Kaczirek K, Gruenberger B, Koelblinger C, Maresch J, Jakesz R, Gruenberger T. Lymph node ratio after curative surgery for intrahepatic cholangiocarcinoma. Br J Surg 2009;96(8): 919–925.PubMedCrossRef Tamandl D, Kaczirek K, Gruenberger B, Koelblinger C, Maresch J, Jakesz R, Gruenberger T. Lymph node ratio after curative surgery for intrahepatic cholangiocarcinoma. Br J Surg 2009;96(8): 919–925.PubMedCrossRef
23.
go back to reference Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Conci S, Valdegamberi A, Sandri M, Iacono C. Prognostic significance of lymph node ratio after resection of peri-hilar cholangiocarcinoma. HPB (Oxford) 2011;13(4): 240–245.CrossRef Guglielmi A, Ruzzenente A, Campagnaro T, Pachera S, Conci S, Valdegamberi A, Sandri M, Iacono C. Prognostic significance of lymph node ratio after resection of peri-hilar cholangiocarcinoma. HPB (Oxford) 2011;13(4): 240–245.CrossRef
24.
go back to reference Choi SB, Kim KS, Choi JY, Park SW, Choi JS, Lee WJ, Chung JB. The prognosis and survival outcome of intrahepatic cholangiocarcinoma following surgical resection: association of lymph node metastasis and lymph node dissection with survival. Ann Surg Oncol 2009;16(11): 3048–3056.PubMedCrossRef Choi SB, Kim KS, Choi JY, Park SW, Choi JS, Lee WJ, Chung JB. The prognosis and survival outcome of intrahepatic cholangiocarcinoma following surgical resection: association of lymph node metastasis and lymph node dissection with survival. Ann Surg Oncol 2009;16(11): 3048–3056.PubMedCrossRef
25.
go back to reference Jarnagin WR, Fong Y, DeMatteo RP, Gonen M, Burke EC, Bodniewicz BJ, Youssef BM, Klimstra D, Blumgart LH. Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg 2001;234(4): 507–517; discussion 517–509.PubMedCrossRef Jarnagin WR, Fong Y, DeMatteo RP, Gonen M, Burke EC, Bodniewicz BJ, Youssef BM, Klimstra D, Blumgart LH. Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg 2001;234(4): 507–517; discussion 517–509.PubMedCrossRef
26.
go back to reference Iacono C, Ruzzenente A, Campagnaro T, Bortolasi L, Valdegamberi A, Guglielmi A. Role of preoperative biliary drainage in jaundiced patients who are candidates for pancreatoduodenectomy or hepatic resection: highlights and drawbacks. Ann Surg 2013;257(2): 191–204.PubMedCrossRef Iacono C, Ruzzenente A, Campagnaro T, Bortolasi L, Valdegamberi A, Guglielmi A. Role of preoperative biliary drainage in jaundiced patients who are candidates for pancreatoduodenectomy or hepatic resection: highlights and drawbacks. Ann Surg 2013;257(2): 191–204.PubMedCrossRef
27.
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): 351–355.PubMedCrossRef Strasberg SM. Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 2005;12(5): 351–355.PubMedCrossRef
28.
go back to reference Surgery JSoB. Classification of Biliary Tract Carcinoma. Japanese Society of Biliary Surgery (Second edn). Kanehara & Co. Ltd.: Tokyo, 2004. Surgery JSoB. Classification of Biliary Tract Carcinoma. Japanese Society of Biliary Surgery (Second edn). Kanehara & Co. Ltd.: Tokyo, 2004.
29.
go back to reference Nishio H, Nagino M, Oda K, Ebata T, Arai T, Nimura Y. TNM classification for perihilar cholangiocarcinoma: comparison between 5th and 6th editions of the AJCC/UICC staging system. Langenbecks Arch Surg 2005;390(4): 319–327.PubMedCrossRef Nishio H, Nagino M, Oda K, Ebata T, Arai T, Nimura Y. TNM classification for perihilar cholangiocarcinoma: comparison between 5th and 6th editions of the AJCC/UICC staging system. Langenbecks Arch Surg 2005;390(4): 319–327.PubMedCrossRef
30.
go back to reference Igami T, Nishio H, Ebata T, Yokoyama Y, Sugawara G, Nimura Y, Nagino M. Surgical treatment of hilar cholangiocarcinoma in the “new era”: the Nagoya University experience. J Hepatobiliary Pancreat Sci 2010;17(4): 449–454.PubMedCrossRef Igami T, Nishio H, Ebata T, Yokoyama Y, Sugawara G, Nimura Y, Nagino M. Surgical treatment of hilar cholangiocarcinoma in the “new era”: the Nagoya University experience. J Hepatobiliary Pancreat Sci 2010;17(4): 449–454.PubMedCrossRef
31.
go back to reference Sano T, Shimada K, Sakamoto Y, Ojima H, Esaki M, Kosuge T. Prognosis of perihilar cholangiocarcinoma: hilar bile duct cancer versus intrahepatic cholangiocarcinoma involving the hepatic hilus. Ann Surg Oncol 2008;15(2): 590–599.PubMedCrossRef Sano T, Shimada K, Sakamoto Y, Ojima H, Esaki M, Kosuge T. Prognosis of perihilar cholangiocarcinoma: hilar bile duct cancer versus intrahepatic cholangiocarcinoma involving the hepatic hilus. Ann Surg Oncol 2008;15(2): 590–599.PubMedCrossRef
32.
go back to reference Ebata T, Kamiya J, Nishio H, Nagasaka T, Nimura Y, Nagino M. The concept of perihilar cholangiocarcinoma is valid. Br J Surg 2009;96(8): 926–934.PubMedCrossRef Ebata T, Kamiya J, Nishio H, Nagasaka T, Nimura Y, Nagino M. The concept of perihilar cholangiocarcinoma is valid. Br J Surg 2009;96(8): 926–934.PubMedCrossRef
33.
go back to reference Edge S.B. AJCoc. AJCC Cancer Staging Manual. (7th ed. edn). Springer: New York, 2010. Edge S.B. AJCoc. AJCC Cancer Staging Manual. (7th ed. edn). Springer: New York, 2010.
34.
go back to reference Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240(2): 205–213.PubMedCrossRef Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240(2): 205–213.PubMedCrossRef
35.
go back to reference Nuzzo G, Giuliante F, Ardito F, Giovannini I, Aldrighetti L, Belli G, Bresadola F, Calise F, Dalla Valle R, D’Amico DF, Gennari L, Giulini SM, Guglielmi A, Jovine E, Pellicci R, Pernthaler H, Pinna AD, Puleo S, Torzilli G, Capussotti L, Cillo U, Ercolani G, Ferrucci M, Mastrangelo L, Portolani N, Pulitano C, Ribero D, Ruzzenente A, Scuderi V, Federico B. Improvement in perioperative and long-term outcome after surgical treatment of hilar cholangiocarcinoma: results of an Italian multicenter analysis of 440 patients. Arch Surg 2012;147(1): 26–34.PubMedCrossRef Nuzzo G, Giuliante F, Ardito F, Giovannini I, Aldrighetti L, Belli G, Bresadola F, Calise F, Dalla Valle R, D’Amico DF, Gennari L, Giulini SM, Guglielmi A, Jovine E, Pellicci R, Pernthaler H, Pinna AD, Puleo S, Torzilli G, Capussotti L, Cillo U, Ercolani G, Ferrucci M, Mastrangelo L, Portolani N, Pulitano C, Ribero D, Ruzzenente A, Scuderi V, Federico B. Improvement in perioperative and long-term outcome after surgical treatment of hilar cholangiocarcinoma: results of an Italian multicenter analysis of 440 patients. Arch Surg 2012;147(1): 26–34.PubMedCrossRef
36.
go back to reference Uenishi T, Yamazaki O, Horii K, Yamamoto T, Kubo S. A long-term survivor of intrahepatic cholangiocarcinoma with paraaortic lymph node metastasis. J Gastroenterol 2006;41(4): 391–392.PubMedCrossRef Uenishi T, Yamazaki O, Horii K, Yamamoto T, Kubo S. A long-term survivor of intrahepatic cholangiocarcinoma with paraaortic lymph node metastasis. J Gastroenterol 2006;41(4): 391–392.PubMedCrossRef
37.
go back to reference Asakura H, Ohtsuka M, Ito H, Kimura F, Ambiru S, Shimizu H, Togawa A, Yoshidome H, Kato A, Miyazaki M. Long-term survival after extended surgical resection of intrahepatic cholangiocarcinoma with extensive lymph node metastasis. Hepatogastroenterology 2005;52(63): 722–724.PubMed Asakura H, Ohtsuka M, Ito H, Kimura F, Ambiru S, Shimizu H, Togawa A, Yoshidome H, Kato A, Miyazaki M. Long-term survival after extended surgical resection of intrahepatic cholangiocarcinoma with extensive lymph node metastasis. Hepatogastroenterology 2005;52(63): 722–724.PubMed
38.
go back to reference Nakagohri T, Asano T, Kinoshita H, Kenmochi T, Urashima T, Miura F, Ochiai T. Aggressive surgical resection for hilar-invasive and peripheral intrahepatic cholangiocarcinoma. World J Surg 2003;27(3): 289–293.PubMedCrossRef Nakagohri T, Asano T, Kinoshita H, Kenmochi T, Urashima T, Miura F, Ochiai T. Aggressive surgical resection for hilar-invasive and peripheral intrahepatic cholangiocarcinoma. World J Surg 2003;27(3): 289–293.PubMedCrossRef
39.
go back to reference Sano T, Shimada K, Sakamoto Y, Yamamoto J, Yamasaki S, Kosuge T. One hundred two consecutive hepatobiliary resections for perihilar cholangiocarcinoma with zero mortality. Ann Surg 2006;244(2): 240–247.PubMedCrossRef Sano T, Shimada K, Sakamoto Y, Yamamoto J, Yamasaki S, Kosuge T. One hundred two consecutive hepatobiliary resections for perihilar cholangiocarcinoma with zero mortality. Ann Surg 2006;244(2): 240–247.PubMedCrossRef
40.
go back to reference Hemming AW, Reed AI, Fujita S, Foley DP, Howard RJ. Surgical management of hilar cholangiocarcinoma. Ann Surg 2005;241(5): 693–699; discussion 699–702.PubMedCrossRef Hemming AW, Reed AI, Fujita S, Foley DP, Howard RJ. Surgical management of hilar cholangiocarcinoma. Ann Surg 2005;241(5): 693–699; discussion 699–702.PubMedCrossRef
41.
go back to reference Ribero D, Pinna AD, Guglielmi A, Ponti A, Nuzzo G, Giulini SM, Aldrighetti L, Calise F, Gerunda GE, Tomatis M, Amisano M, Berloco P, Torzilli G, Capussotti L. (2012) Surgical Approach for Long-term Survival of Patients With Intrahepatic Cholangiocarcinoma: A Multi-Institutional Analysis of 434 Patients. Arch Surg 147:1107–13PubMedCrossRef Ribero D, Pinna AD, Guglielmi A, Ponti A, Nuzzo G, Giulini SM, Aldrighetti L, Calise F, Gerunda GE, Tomatis M, Amisano M, Berloco P, Torzilli G, Capussotti L. (2012) Surgical Approach for Long-term Survival of Patients With Intrahepatic Cholangiocarcinoma: A Multi-Institutional Analysis of 434 Patients. Arch Surg 147:1107–13PubMedCrossRef
42.
go back to reference Ito K, Ito H, Allen PJ, Gonen M, Klimstra D, D’Angelica MI, Fong Y, DeMatteo RP, Brennan MF, Blumgart LH, Jarnagin WR. Adequate lymph node assessment for extrahepatic bile duct adenocarcinoma. Ann Surg 2010;251(4): 675–681.PubMedCrossRef Ito K, Ito H, Allen PJ, Gonen M, Klimstra D, D’Angelica MI, Fong Y, DeMatteo RP, Brennan MF, Blumgart LH, Jarnagin WR. Adequate lymph node assessment for extrahepatic bile duct adenocarcinoma. Ann Surg 2010;251(4): 675–681.PubMedCrossRef
43.
go back to reference Oshiro Y, Sasaki R, Kobayashi A, Murata S, Fukunaga K, Kondo T, Oda T, Ohkohchi N. Prognostic relevance of the lymph node ratio in surgical patients with extrahepatic cholangiocarcinoma. Eur J Surg Oncol 2011;37(1): 60–64.PubMedCrossRef Oshiro Y, Sasaki R, Kobayashi A, Murata S, Fukunaga K, Kondo T, Oda T, Ohkohchi N. Prognostic relevance of the lymph node ratio in surgical patients with extrahepatic cholangiocarcinoma. Eur J Surg Oncol 2011;37(1): 60–64.PubMedCrossRef
44.
go back to reference Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, Roviello F, de Manzoni G, Minicozzi A, Natalini G, De Santis F, Baiocchi L, Coniglio A, Nitti D. The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 2007;245(4): 543–552.PubMedCrossRef Marchet A, Mocellin S, Ambrosi A, Morgagni P, Garcea D, Marrelli D, Roviello F, de Manzoni G, Minicozzi A, Natalini G, De Santis F, Baiocchi L, Coniglio A, Nitti D. The ratio between metastatic and examined lymph nodes (N ratio) is an independent prognostic factor in gastric cancer regardless of the type of lymphadenectomy: results from an Italian multicentric study in 1853 patients. Ann Surg 2007;245(4): 543–552.PubMedCrossRef
45.
go back to reference Peschaud F, Benoist S, Julie C, Beauchet A, Penna C, Rougier P, Nordlinger B. The ratio of metastatic to examined lymph nodes is a powerful independent prognostic factor in rectal cancer. Ann Surg 2008;248(6): 1067–1073.PubMedCrossRef Peschaud F, Benoist S, Julie C, Beauchet A, Penna C, Rougier P, Nordlinger B. The ratio of metastatic to examined lymph nodes is a powerful independent prognostic factor in rectal cancer. Ann Surg 2008;248(6): 1067–1073.PubMedCrossRef
46.
go back to reference Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, Wolfgang C, Hruban RH, Schulick RD, Yeo CJ, Choti MA. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery 2007;141(5): 610–618.PubMedCrossRef Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, Wolfgang C, Hruban RH, Schulick RD, Yeo CJ, Choti MA. Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery 2007;141(5): 610–618.PubMedCrossRef
47.
go back to reference Schwarz RE, Smith DD. Lymph node dissection impact on staging and survival of extrahepatic cholangiocarcinomas, based on U.S. population data. J Gastrointest Surg 2007;11(2): 158–165.PubMedCrossRef Schwarz RE, Smith DD. Lymph node dissection impact on staging and survival of extrahepatic cholangiocarcinomas, based on U.S. population data. J Gastrointest Surg 2007;11(2): 158–165.PubMedCrossRef
48.
go back to reference Ikai I, Arii S, Ichida T, Okita K, Omata M, Kojiro M, Takayasu K, Nakanuma Y, Makuuchi M, Matsuyama Y, Yamaoka Y. Report of the 16th follow-up survey of primary liver cancer. Hepatol Res 2005;32(3): 163–172.PubMedCrossRef Ikai I, Arii S, Ichida T, Okita K, Omata M, Kojiro M, Takayasu K, Nakanuma Y, Makuuchi M, Matsuyama Y, Yamaoka Y. Report of the 16th follow-up survey of primary liver cancer. Hepatol Res 2005;32(3): 163–172.PubMedCrossRef
49.
go back to reference Yamamoto M, Takasaki K, Yoshikawa T. Lymph node metastasis in intrahepatic cholangiocarcinoma. Jpn J Clin Oncol 1999;29(3): 147–150.PubMedCrossRef Yamamoto M, Takasaki K, Yoshikawa T. Lymph node metastasis in intrahepatic cholangiocarcinoma. Jpn J Clin Oncol 1999;29(3): 147–150.PubMedCrossRef
50.
go back to reference Nozaki Y, Yamamoto M, Ikai I, Yamamoto Y, Ozaki N, Fujii H, Nagahori K, Matsumoto Y, Yamaoka Y. Reconsideration of the lymph node metastasis pattern (N factor) from intrahepatic cholangiocarcinoma using the International Union Against Cancer TNM staging system for primary liver carcinoma. Cancer 1998;83(9): 1923–1929.PubMedCrossRef Nozaki Y, Yamamoto M, Ikai I, Yamamoto Y, Ozaki N, Fujii H, Nagahori K, Matsumoto Y, Yamaoka Y. Reconsideration of the lymph node metastasis pattern (N factor) from intrahepatic cholangiocarcinoma using the International Union Against Cancer TNM staging system for primary liver carcinoma. Cancer 1998;83(9): 1923–1929.PubMedCrossRef
51.
go back to reference Todoroki T, Kawamoto T, Koike N, Takahashi H, Yoshida S, Kashiwagi H, Takada Y, Otsuka M, Fukao K. Radical resection of hilar bile duct carcinoma and predictors of survival. Br J Surg 2000;87(3): 306–313.PubMedCrossRef Todoroki T, Kawamoto T, Koike N, Takahashi H, Yoshida S, Kashiwagi H, Takada Y, Otsuka M, Fukao K. Radical resection of hilar bile duct carcinoma and predictors of survival. Br J Surg 2000;87(3): 306–313.PubMedCrossRef
Metadata
Title
Patterns and Prognostic Significance of Lymph Node Dissection for Surgical Treatment of Perihilar and Intrahepatic Cholangiocarcinoma
Authors
Alfredo Guglielmi
Andrea Ruzzenente
Tommaso Campagnaro
Alessandro Valdegamberi
Fabio Bagante
Francesca Bertuzzo
Simone Conci
Calogero Iacono
Publication date
01-11-2013
Publisher
Springer US
Published in
Journal of Gastrointestinal Surgery / Issue 11/2013
Print ISSN: 1091-255X
Electronic ISSN: 1873-4626
DOI
https://doi.org/10.1007/s11605-013-2331-1

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