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Published in: Annals of Surgical Oncology 7/2019

01-07-2019 | Metastasis | Hepatobiliary Tumors

Should Utilization of Lymphadenectomy Vary According to Morphologic Subtype of Intrahepatic Cholangiocarcinoma?

Authors: Xu-Feng Zhang, MD, PhD, Yi Lv, MD, PhD, Matthew Weiss, MD, Irinel Popescu, MD, Hugo P. Marques, MD, Luca Aldrighetti, MD, Shishir K. Maithel, MD, Carlo Pulitano, MD, Todd W. Bauer, MD, Feng Shen, MD, George A. Poultsides, MD, Oliver Soubrane, MD, Guillaume Martel, MD, B. Groot Koerkamp, MD, Endo Itaru, MD, Timothy M. Pawlik, MD, MPH, PhD

Published in: Annals of Surgical Oncology | Issue 7/2019

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Abstract

Objective

We sought to evaluate the utilization of lymphadenectomy (LND) and the incidence of lymph node metastasis (LNM) among different morphologic types of intrahepatic cholangiocarcinoma (ICC).

Methods

Clinical data of patients undergoing curative-intent resection for ICC between 1990 and 2017 were collected and analyzed. The preoperative nodal status was evaluated by imaging studies, and the morphologic and lymph node (LN) status was collected on final pathology report.

Results

Overall, 1032 patients had a mass-forming (MF) or intraductal growth (IG) ICC subtype, whereas 150 patients had a periductal infiltrating (PI) or MF + PI subtype. Among the 924 patients with MF/IG ICC subtype who had nodal assessment on preoperative imaging, 747 (80.8%) were node-negative, whereas 177 (19.2%) patients were suspicious for metastatic nodal disease. On final pathological analysis, 71 of 282 (25.2%) patients who had preoperative node-negative disease ultimately had LNM. In contrast, 79 of 135 (58.5%) patients with preoperative suspicious/metastatic LNs had pathologically confirmed LNM (odds ratio [OR] 4.2, p < 0.001). Among the 129 patients with PI/MF + PI ICC subtype and preoperative nodal information, 72 (55.8%) were node-negative on preoperative imaging. In contrast, 57 (44.2%) patients had suspicious/metastatic LNs. On final pathologic examination, 45.3% (n = 24) of patients believed to be node-negative on preoperative imaging had LNM; 68.0% (n = 34) of patients who had suspicious/positive nodal disease on imaging ultimately had LNM (OR 2.6, p = 0.009).

Conclusion

Given the low accuracy of preoperative imaging evaluation of nodal status, routine LND should be performed at the time of resection for both MF/IG and PI/MF + PI ICC subtypes.
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Literature
1.
go back to reference de Jong MC, Nathan H, Sotiropoulos GC, et al. Intrahepatic cholangiocarcinoma: an international multi-institutional analysis of prognostic factors and lymph node assessment. J Clin Oncol. 2011;29:3140-5.CrossRefPubMed de Jong MC, Nathan H, Sotiropoulos GC, et al. Intrahepatic cholangiocarcinoma: an international multi-institutional analysis of prognostic factors and lymph node assessment. J Clin Oncol. 2011;29:3140-5.CrossRefPubMed
2.
go back to reference Yamasaki S. Intrahepatic cholangiocarcinoma: macroscopic type and stage classification. J Hepatobiliary Pancreat Surg. 2003;10:288–91.CrossRefPubMed Yamasaki S. Intrahepatic cholangiocarcinoma: macroscopic type and stage classification. J Hepatobiliary Pancreat Surg. 2003;10:288–91.CrossRefPubMed
3.
go back to reference Bagante F, Spolverato G, Weiss M, et al. Impact of morphological status on long-term outcome among patients undergoing liver surgery for intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2017;24:2491–501.CrossRefPubMed Bagante F, Spolverato G, Weiss M, et al. Impact of morphological status on long-term outcome among patients undergoing liver surgery for intrahepatic cholangiocarcinoma. Ann Surg Oncol. 2017;24:2491–501.CrossRefPubMed
4.
go back to reference Shimada K, Sano T, Sakamoto Y, Esaki M, Kosuge T, Ojima H. Surgical outcomes of the mass-forming plus periductal infiltrating types of intrahepatic cholangiocarcinoma: a comparative study with the typical mass-forming type of intrahepatic cholangiocarcinoma. World J Surg. 2007;31:2016–22.CrossRefPubMed Shimada K, Sano T, Sakamoto Y, Esaki M, Kosuge T, Ojima H. Surgical outcomes of the mass-forming plus periductal infiltrating types of intrahepatic cholangiocarcinoma: a comparative study with the typical mass-forming type of intrahepatic cholangiocarcinoma. World J Surg. 2007;31:2016–22.CrossRefPubMed
5.
go back to reference Ohtsuka M, Ito H, Kimura F, et al. Results of surgical treatment for intrahepatic cholangiocarcinoma and clinicopathological factors influencing survival. Br J Surg. 2002;89:1525–31.CrossRefPubMed Ohtsuka M, Ito H, Kimura F, et al. Results of surgical treatment for intrahepatic cholangiocarcinoma and clinicopathological factors influencing survival. Br J Surg. 2002;89:1525–31.CrossRefPubMed
6.
go back to reference Yamamoto M, Takasaki K, Yoshikawa T, Ueno K, Nakano M. Does gross appearance indicate prognosis in intrahepatic cholangiocarcinoma? J Surg Oncol. 1998;69:162–7.CrossRefPubMed Yamamoto M, Takasaki K, Yoshikawa T, Ueno K, Nakano M. Does gross appearance indicate prognosis in intrahepatic cholangiocarcinoma? J Surg Oncol. 1998;69:162–7.CrossRefPubMed
7.
go back to reference Aishima S, Oda Y. Pathogenesis and classification of intrahepatic cholangiocarcinoma: different characters of perihilar large duct type versus peripheral small duct type. J Hepatobiliary Pancreat Sci. 2015;22:94–100.CrossRefPubMed Aishima S, Oda Y. Pathogenesis and classification of intrahepatic cholangiocarcinoma: different characters of perihilar large duct type versus peripheral small duct type. J Hepatobiliary Pancreat Sci. 2015;22:94–100.CrossRefPubMed
8.
go back to reference Liau JY, Tsai JH, Yuan RH, Chang CN, Lee HJ, Jeng YM. Morphological subclassification of intrahepatic cholangiocarcinoma: etiological, clinicopathological, and molecular features. Mod Pathol. 2014;27:1163–73.CrossRefPubMed Liau JY, Tsai JH, Yuan RH, Chang CN, Lee HJ, Jeng YM. Morphological subclassification of intrahepatic cholangiocarcinoma: etiological, clinicopathological, and molecular features. Mod Pathol. 2014;27:1163–73.CrossRefPubMed
9.
10.
go back to reference Wei M, Lu L, Lin P, Chen Z, Quan Z, Tang Z. Multiple cellular origins and molecular evolution of intrahepatic cholangiocarcinoma. Cancer Lett. 2016;379:253–61.CrossRefPubMed Wei M, Lu L, Lin P, Chen Z, Quan Z, Tang Z. Multiple cellular origins and molecular evolution of intrahepatic cholangiocarcinoma. Cancer Lett. 2016;379:253–61.CrossRefPubMed
11.
go back to reference Aishima S, Kuroda Y, Nishihara Y, et al. Proposal of progression model for intrahepatic cholangiocarcinoma: clinicopathologic differences between hilar type and peripheral type. Am J Surg Pathol. 2007;31:1059–67.CrossRefPubMed Aishima S, Kuroda Y, Nishihara Y, et al. Proposal of progression model for intrahepatic cholangiocarcinoma: clinicopathologic differences between hilar type and peripheral type. Am J Surg Pathol. 2007;31:1059–67.CrossRefPubMed
12.
go back to reference Shimada H, Endo I, Togo S, Nakano A, Izumi T, Nakagawara G. The role of lymph node dissection in the treatment of gallbladder carcinoma. Cancer. 1997;79:892–9.CrossRefPubMed Shimada H, Endo I, Togo S, Nakano A, Izumi T, Nakagawara G. The role of lymph node dissection in the treatment of gallbladder carcinoma. Cancer. 1997;79:892–9.CrossRefPubMed
13.
go back to reference Kitagawa Y, Nagino M, Kamiya J, et al. Lymph node metastasis from hilar cholangiocarcinoma: audit of 110 patients who underwent regional and paraaortic node dissection. Ann Surg. 2001;233:385–92.CrossRefPubMedPubMedCentral Kitagawa Y, Nagino M, Kamiya J, et al. Lymph node metastasis from hilar cholangiocarcinoma: audit of 110 patients who underwent regional and paraaortic node dissection. Ann Surg. 2001;233:385–92.CrossRefPubMedPubMedCentral
14.
go back to reference Morine Y, Shimada M. The value of systematic lymph node dissection for intrahepatic cholangiocarcinoma from the viewpoint of liver lymphatics. J Gastroenterol. 2015;50:913–27.CrossRefPubMed Morine Y, Shimada M. The value of systematic lymph node dissection for intrahepatic cholangiocarcinoma from the viewpoint of liver lymphatics. J Gastroenterol. 2015;50:913–27.CrossRefPubMed
15.
go back to reference Zhang XF, Chakedis J, Bagante F, et al. Trends in use of lymphadenectomy in surgery with curative intent for intrahepatic cholangiocarcinoma. Br J Surg. 2018;105:857–66.CrossRefPubMed Zhang XF, Chakedis J, Bagante F, et al. Trends in use of lymphadenectomy in surgery with curative intent for intrahepatic cholangiocarcinoma. Br J Surg. 2018;105:857–66.CrossRefPubMed
16.
go back to reference Zhang XF, Chen Q, Kimbrough CW, et al. Lymphadenectomy for intrahepatic cholangiocarcinoma: has nodal evaluation been increasingly adopted by surgeons over time? A national database analysis. J Gastrointest Surg. 2018;22:668–75.CrossRefPubMed Zhang XF, Chen Q, Kimbrough CW, et al. Lymphadenectomy for intrahepatic cholangiocarcinoma: has nodal evaluation been increasingly adopted by surgeons over time? A national database analysis. J Gastrointest Surg. 2018;22:668–75.CrossRefPubMed
17.
go back to reference Miwa S, Miyagawa S, Kobayashi A, et al. Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol. 2006;41:893–900.CrossRefPubMed Miwa S, Miyagawa S, Kobayashi A, et al. Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol. 2006;41:893–900.CrossRefPubMed
18.
go back to reference Marubashi S, Gotoh K, Takahashi H, et al. Prediction of the postoperative prognosis of intrahepatic cholangiocarcinoma (ICC): importance of preoperatively- determined anatomic invasion level and number of tumors. Dig Dis Sci. 2014;59:201–13.CrossRefPubMed Marubashi S, Gotoh K, Takahashi H, et al. Prediction of the postoperative prognosis of intrahepatic cholangiocarcinoma (ICC): importance of preoperatively- determined anatomic invasion level and number of tumors. Dig Dis Sci. 2014;59:201–13.CrossRefPubMed
19.
go back to reference Shimada K, Sano T, Nara S, et al. Therapeutic value of lymph node dissection during hepatectomy in patients with intrahepatic cholangiocellular carcinoma with negative lymph node involvement. Surgery. 2009;145:411–6.CrossRefPubMed Shimada K, Sano T, Nara S, et al. Therapeutic value of lymph node dissection during hepatectomy in patients with intrahepatic cholangiocellular carcinoma with negative lymph node involvement. Surgery. 2009;145:411–6.CrossRefPubMed
20.
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;88:1463–6.CrossRefPubMed 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;88:1463–6.CrossRefPubMed
21.
go back to reference Kim DH, Choi DW, Choi SH, Heo JS, Kow AW. Is there a role for systematic hepatic pedicle lymphadenectomy in intrahepatic cholangiocarcinoma? A review of 17 years of experience in a tertiary institution. Surgery. 2015;157:666–75.CrossRefPubMed Kim DH, Choi DW, Choi SH, Heo JS, Kow AW. Is there a role for systematic hepatic pedicle lymphadenectomy in intrahepatic cholangiocarcinoma? A review of 17 years of experience in a tertiary institution. Surgery. 2015;157:666–75.CrossRefPubMed
22.
go back to reference Li DY, Zhang HB, Yang N, Quan Y, Yang GS. Routine lymph node dissection may be not suitable for all intrahepatic cholangiocarcinoma patients: results of a monocentric series. World J Gastroenterol. 2013;19:9084–91.CrossRefPubMedPubMedCentral Li DY, Zhang HB, Yang N, Quan Y, Yang GS. Routine lymph node dissection may be not suitable for all intrahepatic cholangiocarcinoma patients: results of a monocentric series. World J Gastroenterol. 2013;19:9084–91.CrossRefPubMedPubMedCentral
23.
go back to reference Reames BN, Ejaz A, Koerkamp BG, et al. Impact of major vascular resection on outcomes and survival in patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis. J Surg Oncol. 2017;116:133–9.CrossRefPubMed Reames BN, Ejaz A, Koerkamp BG, et al. Impact of major vascular resection on outcomes and survival in patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis. J Surg Oncol. 2017;116:133–9.CrossRefPubMed
24.
go back to reference Jutric Z, Johnston WC, Hoen HM, et al. Impact of lymph node status in patients with intrahepatic cholangiocarcinoma treated by major hepatectomy: a review of the National Cancer Database. HPB (Oxford). 2016;18:79–87.CrossRef Jutric Z, Johnston WC, Hoen HM, et al. Impact of lymph node status in patients with intrahepatic cholangiocarcinoma treated by major hepatectomy: a review of the National Cancer Database. HPB (Oxford). 2016;18:79–87.CrossRef
25.
go back to reference Bagante F, Gani F, Spolverato G, et al. Intrahepatic cholangiocarcinoma: prognosis of patients who did not undergo lymphadenectomy. J Am Coll Surg. 2015;221:1031-40.e1-4.CrossRefPubMed Bagante F, Gani F, Spolverato G, et al. Intrahepatic cholangiocarcinoma: prognosis of patients who did not undergo lymphadenectomy. J Am Coll Surg. 2015;221:1031-40.e1-4.CrossRefPubMed
26.
go back to reference Amini N, Ejaz A, Spolverato G, Maithel SK, Kim Y, Pawlik TM. Management of lymph nodes during resection of hepatocellular carcinoma and intrahepatic cholangiocarcinoma: a systematic review. J Gastrointest Surg. 2014;18:2136–48.CrossRefPubMed Amini N, Ejaz A, Spolverato G, Maithel SK, Kim Y, Pawlik TM. Management of lymph nodes during resection of hepatocellular carcinoma and intrahepatic cholangiocarcinoma: a systematic review. J Gastrointest Surg. 2014;18:2136–48.CrossRefPubMed
27.
go back to reference Bagante F, Spolverato G, Weiss M, et al. Assessment of the lymph node status in patients undergoing liver resection for intrahepatic cholangiocarcinoma: the new eighth edition AJCC staging system. J Gastrointest Surg. 2018;22(1):52–59.CrossRefPubMed Bagante F, Spolverato G, Weiss M, et al. Assessment of the lymph node status in patients undergoing liver resection for intrahepatic cholangiocarcinoma: the new eighth edition AJCC staging system. J Gastrointest Surg. 2018;22(1):52–59.CrossRefPubMed
28.
go back to reference Palmer WC, Patel T. Are common factors involved in the pathogenesis of primary liver cancers? A meta-analysis of risk factors for intrahepatic cholangiocarcinoma. J Hepatol. 2012;57:69–76.CrossRefPubMedPubMedCentral Palmer WC, Patel T. Are common factors involved in the pathogenesis of primary liver cancers? A meta-analysis of risk factors for intrahepatic cholangiocarcinoma. J Hepatol. 2012;57:69–76.CrossRefPubMedPubMedCentral
29.
30.
go back to reference Lafaro KJ, Pawlik TM. Fibrolamellar hepatocellular carcinoma: current clinical perspectives. J Hepatocell Carcinoma. 2015;2:151–7.PubMedPubMedCentral Lafaro KJ, Pawlik TM. Fibrolamellar hepatocellular carcinoma: current clinical perspectives. J Hepatocell Carcinoma. 2015;2:151–7.PubMedPubMedCentral
31.
go back to reference Mayo SC, Mavros MN, Nathan H, et al. Treatment and prognosis of patients with fibrolamellar hepatocellular carcinoma: a national perspective. J Am Coll Surg. 2014;218:196–205.CrossRefPubMed Mayo SC, Mavros MN, Nathan H, et al. Treatment and prognosis of patients with fibrolamellar hepatocellular carcinoma: a national perspective. J Am Coll Surg. 2014;218:196–205.CrossRefPubMed
32.
go back to reference Seo S, Hatano E, Higashi T, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography predicts lymph node metastasis, P-glycoprotein expression, and recurrence after resection in mass-forming intrahepatic cholangiocarcinoma. Surgery. 2008;143:769–77.CrossRefPubMed Seo S, Hatano E, Higashi T, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography predicts lymph node metastasis, P-glycoprotein expression, and recurrence after resection in mass-forming intrahepatic cholangiocarcinoma. Surgery. 2008;143:769–77.CrossRefPubMed
33.
go back to reference Weber SM, Ribero D, O’Reilly EM, Kokudo N, Miyazaki M, Pawlik TM. Intrahepatic cholangiocarcinoma: expert consensus statement. HPB (Oxford). 2015;17:669–80.CrossRef Weber SM, Ribero D, O’Reilly EM, Kokudo N, Miyazaki M, Pawlik TM. Intrahepatic cholangiocarcinoma: expert consensus statement. HPB (Oxford). 2015;17:669–80.CrossRef
34.
go back to reference Ribero D, Pinna AD, Guglielmi A, et al. Surgical approach for long-term survival of patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis of 434 patients. Arch Surg. 2012;147:1107–13.CrossRefPubMed Ribero D, Pinna AD, Guglielmi A, et al. Surgical approach for long-term survival of patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis of 434 patients. Arch Surg. 2012;147:1107–13.CrossRefPubMed
35.
go back to reference Reames BN, Bagante F, Ejaz A, et al. Impact of adjuvant chemotherapy on survival in patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis. HPB (Oxford). 2017;19(10):901–909.CrossRef Reames BN, Bagante F, Ejaz A, et al. Impact of adjuvant chemotherapy on survival in patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis. HPB (Oxford). 2017;19(10):901–909.CrossRef
Metadata
Title
Should Utilization of Lymphadenectomy Vary According to Morphologic Subtype of Intrahepatic Cholangiocarcinoma?
Authors
Xu-Feng Zhang, MD, PhD
Yi Lv, MD, PhD
Matthew Weiss, MD
Irinel Popescu, MD
Hugo P. Marques, MD
Luca Aldrighetti, MD
Shishir K. Maithel, MD
Carlo Pulitano, MD
Todd W. Bauer, MD
Feng Shen, MD
George A. Poultsides, MD
Oliver Soubrane, MD
Guillaume Martel, MD
B. Groot Koerkamp, MD
Endo Itaru, MD
Timothy M. Pawlik, MD, MPH, PhD
Publication date
01-07-2019
Publisher
Springer International Publishing
Published in
Annals of Surgical Oncology / Issue 7/2019
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-019-07336-5

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