World Journal of Surgery

, Volume 38, Issue 7, pp 1763–1768 | Cite as

Pathological Confirmation of Para-Aortic Lymph Node Status as a Potential Criterion for the Selection of Intrahepatic Cholangiocarcinoma Patients for Radical Resection with Regional Lymph Node Dissection

  • Tomohide Nakayama
  • Takahiro Tsuchikawa
  • Toshiaki Shichinohe
  • Toru Nakamura
  • Yuma Ebihara
  • Satoshi Hirano



Para-aortic lymph node (PAN) metastasis traditionally has been defined as distant metastasis. Many studies suggest that lymph node metastasis in intrahepatic cholangiocarcinoma (ICC) is one of the strongest prognostic factors for patient survival; however, the status of the PAN was not examined separately from regional lymph node metastasis in these reports. Here, we investigated whether regional lymph node metastasis without PAN metastasis in ICC can be classified as resectable disease and whether curative resection can have a prognostic impact.


Between 1998 and 2010, a total of 47 ICC patients underwent hepatic resection and systematic lymphadenectomy with curative intent. We routinely dissected the PANs and had frozen-section pathological examinations performed intraoperatively. If PAN metastases were identified, curative resection was abandoned. We retrospectively investigated the prognostic factors for patient survival after curative resection for ICC without PAN metastases, with particular attention paid to the prognostic impact of lymphadenectomy.


Univariate analysis identified concomitant portal vein resection, concomitant hepatic artery resection, intraoperative blood loss, intraoperative transfusion, and residual tumor as significant negative prognostic factors. However, lymph node status was not identified as a significant prognostic factor. The 14 patients with node-positive cancer had a survival rate of 20 % at 5 years. Based on multivariate analysis, intraoperative transfusion was an independent prognostic factor associated with a poor prognosis (risk ratio = 4.161; P = 0.0056).


Regional lymph node metastasis in ICC should be classified as resectable disease, because the survival rate after surgical intervention was acceptable when PAN metastasis was pathologically negative.


  1. 1.
    Liver Cancer Study Group of Japan (1990) Primary liver cancer in Japan. Clinicopathologic features and results of surgical treatment. Ann Surg 211:277–287Google Scholar
  2. 2.
    Chen MF (1999) Peripheral cholangiocarcinoma (cholangiocellular carcinoma): clinical features, diagnosis and treatment. J Gastroenterol Hepatol 14:1144–1149PubMedCrossRefGoogle Scholar
  3. 3.
    Ikai I, Itai Y, Okita K et al (2004) Report of the 15th follow-up survey of primary liver cancer. Hepatol Res 28:21–29PubMedCrossRefGoogle Scholar
  4. 4.
    Khan SA, Thomas HC, Davidson BR et al (2005) Cholangiocarcinoma. Lancet 366:1303–1314PubMedCrossRefGoogle Scholar
  5. 5.
    Okabayashi T, Yamamoto J, Kosuge T et al (2001) A new staging system for mass-forming intrahepatic cholangiocarcinoma: analysis of preoperative and postoperative variables. Cancer 92:2374–2383PubMedCrossRefGoogle Scholar
  6. 6.
    Nanashima A, Sumida Y, Abo T et al (2007) Patient outcome and prognostic factors in intrahepatic cholangiocarcinoma after hepatectomy. Hepatogastroenterology 54:2337–2342PubMedGoogle Scholar
  7. 7.
    Uenishi T, Kubo S, Yamazaki O et al (2008) Indications for surgical treatment of intrahepatic cholangiocarcinoma with lymph node metastases. J Hepatobiliary Pancreat Surg 15:417–422PubMedCrossRefGoogle Scholar
  8. 8.
    Tamandl D, Herberger B, Gruenberger B et al (2008) Influence of hepatic resection margin on recurrence and survival in intrahepatic cholangiocarcinoma. Ann Surg Oncol 5:2787–2794CrossRefGoogle Scholar
  9. 9.
    Lang H, Sotiropoulos GC, Sgourakis G et al (2009) Operations for intrahepatic cholangiocarcinoma: single-institution experience of 158 patients. J Am Coll Surg 208:218–228PubMedCrossRefGoogle Scholar
  10. 10.
    Zhang L, Cai JQ, Zhao JJ et al (2010) Impact of hepatitis B virus infection on outcome following resection for intrahepatic cholangiocarcinoma. J Surg Oncol 101:233–238PubMedCrossRefGoogle Scholar
  11. 11.
    Miwa S, Miyagawa S, Kobayashi A et al (2006) Predictive factors for intrahepatic cholangiocarcinoma recurrence in the liver following surgery. J Gastroenterol 41:893–900PubMedCrossRefGoogle Scholar
  12. 12.
    Shen WF, Zhong W, Xu F et al (2009) Clinicopathological and prognostic analysis of 429 patients with intrahepatic cholangiocarcinoma. World J Gastroenterol 15:5976–5982PubMedCentralPubMedCrossRefGoogle Scholar
  13. 13.
    Guglielmi A, Ruzzenente A, Campagnaro T et al (2009) Intrahepatic cholangiocarcinoma: prognostic factors after surgical resection. World J Surg 33:1247–1254. doi:10.1007/s00268-009-9970-0 PubMedCrossRefGoogle Scholar
  14. 14.
    Choi SB, Kim KS, Choi JY et al (2009) 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 16:3048–3056PubMedCrossRefGoogle Scholar
  15. 15.
    Shirabe K, Mano Y, Taketomi A et al (2010) Clinicopathological prognostic factors after hepatectomy for patients with mass-forming type intrahepatic cholangiocarcinoma: relevance of the lymphatic invasion index. Ann Surg Oncol 17:1816–1822PubMedCrossRefGoogle Scholar
  16. 16.
    Uchiyama K, Yamamoto M, Yamaue H et al (2011) Impact of nodal involvement on surgical outcomes of intrahepatic cholangiocarcinoma: a multicenter analysis by the Study Group for Hepatic Surgery of the Japanese Society of Hepato-Biliary-Pancreatic Surgery. J Hepatobiliary Pancreat Sci 18:443–452PubMedCrossRefGoogle Scholar
  17. 17.
    Pedrazzoli S, DiCarlo V, Dionigi R et al (1998) Standard versus extended lymphadenectomy associated with pancreatoduodenectomy in the surgical treatment of adenocarcinoma of the head of the pancreas: a multicenter, prospective, randomized study. Lymphadenectomy Study Group. Ann Surg 228:508–517PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Kondo S, Nimura Y, Hayakawa N et al (2000) Regional and para-aortic lymphadenectomy in radical surgery for advanced gallbladder carcinoma. Br J Surg 87:418–422PubMedCrossRefGoogle Scholar
  19. 19.
    Farnell MB, Aranha GV, Nimura Y et al (2008) The role of extended lymphadenectomy for adenocarcinoma of the head of the pancreas: strength of the evidence. J Gastrointest Surg 12:651–656PubMedCrossRefGoogle Scholar
  20. 20.
    Shimada H, Endo I, Togo S et al (1997) The role of lymph node dissection in the treatment of gallbladder carcinoma. Cancer 79:892–899PubMedCrossRefGoogle Scholar
  21. 21.
    Kitagawa Y, Nagino M, Kamiya J et al (2001) Lymph node metastasis from hilar cholangiocarcinoma: audit of 110 patients who underwent regional and paraaortic node dissection. Ann Surg 233:385–392PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Sobin LH, Gospodarowicz MK, Wittekind C (2010) International Union Against Cancer (UICC) TNM classification of malignant tumours, 7th edn. Wiley-Liss, New York, pp 114–117Google Scholar
  23. 23.
    Liver Cancer Study Group of Japan (2008) Macroscopic gross type. The general rules for the clinical and pathological study of primary liver cancer, 5th edn. Kanehara, Tokyo, pp 17–18Google Scholar
  24. 24.
    Yamashita Y, Taketomi A, Morita K et al (2008) The impact of surgical treatment and poor prognostic factors for patients with intrahepatic cholangiocarcinoma: retrospective analysis of 60 patients. Anticancer Res 28:2353–2359PubMedGoogle Scholar
  25. 25.
    Paik KY, Jung JC, Heo JS et al (2008) What prognostic factors are important for resected intrahepatic cholangiocarcinoma? J Gastroenterol Hepatol 23:766–770PubMedCrossRefGoogle Scholar
  26. 26.
    Ohtsuka M, Ito H, Kimura F et al (2002) Results of surgical treatment for intrahepatic cholangiocarcinoma and clinicopathological factors influencing survival. Br J Surg 89:1525–1531PubMedCrossRefGoogle Scholar
  27. 27.
    Shirai K, Ebata T, Oda K et al (2008) Perineural invasion is a prognostic factor in intrahepatic cholangiocarcinoma. World J Surg 32:2395–2402. doi:10.1007/s00268-008-9726-2 PubMedCrossRefGoogle Scholar
  28. 28.
    Noji T, Kondo S, Hirano S et al (2005) CT evaluation of paraaortic lymph node metastasis in patients with biliary cancer. J Gastroenterol 40:739–743PubMedCrossRefGoogle Scholar
  29. 29.
    Imai H, Doi R, Kanazawa H et al (2010) Preoperative assessment of para-aortic lymph node metastasis in patients with pancreatic cancer. Int J Clin Oncol 15:294–300PubMedCrossRefGoogle Scholar
  30. 30.
    Sugezawa A, Kaibara N, Sumi K et al (1989) Blood transfusion and the prognosis of patients with gastric cancer. J Surg Oncol 42:113–116PubMedCrossRefGoogle Scholar
  31. 31.
    Ojima T, Iwahashi M, Nakamori M et al (2009) Association of allogeneic blood transfusions and long-term survival of patients with gastric cancer after curative gastrectomy. J Gastrointest Surg 13:1821–1830PubMedCrossRefGoogle Scholar
  32. 32.
    Asahara T, Katayama K, Itamoto T et al (1999) Perioperative blood transfusion as a prognostic indicator in patients with hepatocellular carcinoma. World J Surg 23:676–680. doi:10.1007/PL00012367 PubMedCrossRefGoogle Scholar
  33. 33.
    Makino Y, Yamanoi A, Kimoto T et al (2000) The influence of perioperative blood transfusion on intrahepatic recurrence after curative resection of hepatocellular carcinoma. Am J Gastroenterol 95:1294–1300PubMedCrossRefGoogle Scholar
  34. 34.
    Chung M, Steinmetz OK, Gordon PH (1993) Perioperative blood transfusion and outcome after resection for colorectal carcinoma. Br J Surg 80:427–432PubMedCrossRefGoogle Scholar
  35. 35.
    Yeh JJ, Gonen M, Tomlinson JS et al (2007) Effect of blood transfusion on outcome after pancreaticoduodenectomy for exocrine tumour of the pancreas. Br J Surg 94:466–472PubMedCrossRefGoogle Scholar
  36. 36.
    Salvadori S, Martinelli G, Zier K (2000) Resection of solid tumors reverses T cell defects and restores protective immunity. J Immunol 164:2214–2220PubMedCrossRefGoogle Scholar
  37. 37.
    Clark E, Connor S, Taylor MA et al (2007) Perioperative transfusion for pancreaticoduodenectomy and its impact on prognosis in resected pancreatic ductal adenocarcinoma. HPB (Oxford) 9:472–477CrossRefGoogle Scholar

Copyright information

© Société Internationale de Chirurgie 2013

Authors and Affiliations

  • Tomohide Nakayama
    • 1
  • Takahiro Tsuchikawa
    • 1
  • Toshiaki Shichinohe
    • 1
  • Toru Nakamura
    • 1
  • Yuma Ebihara
    • 1
  • Satoshi Hirano
    • 1
  1. 1.Department of Gastroenterological Surgery IIHokkaido University Graduate School of MedicineSapporoJapan

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