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Low Incidence of Lymph Node Metastasis After Resection of Hepatitis Virus-Related Intrahepatic Cholangiocarcinoma

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Abstract

Background and objectives

We determined the rates of initial lymph node metastasis following curative resection of mass-forming type-intrahepatic cholangiocarcinoma (ICC) in patients with and without hepatitis virus infection.

Methods

We enrolled 87 patients between January 2000 and December 2013 with ICC without preoperative lymph node metastasis and without lymph node dissection. Patients included 32 who were seropositive for hepatitis B or C virus (virus group) and 55 who had no evidence of hepatitis virus infection (nonvirus group). Postsurgical outcomes and initial recurrence of the groups were compared, and we identified the risk factors for lymph node metastasis as initial recurrence.

Results

Platelet counts and prothrombin activities were significantly lower in the virus group compared with those of the nonvirus group. The number of patients with chronic hepatitis or liver cirrhosis was significantly higher in the virus group compared with the nonvirus group as well as their respective rates of recurrence-free survival. One patient (3%) in the virus group and 14 patients (25%) in the nonvirus group had lymph node metastasis as initial recurrence (p = 0.007). Multivariate analysis revealed that the absence of hepatitis virus infection as an independent risk factor (p = 0.047).

Conclusion

Hepatitis virus-associated mass-forming-type ICC confers a low risk of lymph node metastasis as initial postoperative recurrence.

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References

  1. Kudo M, Izumi N, Ichida T et al (2016) Report of the 19th follow-up survey of primary liver cancer in japan. Hepatol Res 46:372–390

    Article  PubMed  Google Scholar 

  2. Lubezky N, Facciuto M, Harimoto N et al (2015) Surgical treatment of intrahepatic cholangiocarcinoma in the USA. J Hepatobiliary Pancreat Sci 22:124–130

    Article  PubMed  Google Scholar 

  3. Patel T (2001) Increasing incidence and mortality of primary intrahepatic cholangiocarcinoma in the United States. Hepatology 33:1353–1357

    Article  CAS  PubMed  Google Scholar 

  4. Khan SA, Taylor-Robinson SD, Toledano MB et al (2002) Changing international trends in mortality rates for liver, biliary and pancreatic tumours. J Hepatol 37:806–813

    Article  PubMed  Google Scholar 

  5. Utada M, Ohno Y, Tamaki T et al (2014) Long-term trends in incidence and mortality of intrahepatic and extrahepatic bile duct cancer in Japan. J Epidemiol 24(193–19):9

    Google Scholar 

  6. Ikeda A, Miyashiro I, Nakayama T et al (2013) Descriptive epidemiology of bile duct carcinoma in Osaka. Jpn J Clin Oncol 43(1150–115):5

    Google Scholar 

  7. Parkin DM, Ohshima H, Srivatanakul P et al (1993) Cholangiocarcinoma: epidemiology, mechanisms of carcinogenesis and prevention. Cancer Epidemiol Biomark Prev 2:537–544

    CAS  Google Scholar 

  8. Shaib Y, El-Serag HB (2004) The epidemiology of cholangiocarcinoma. Semin Liver Dis 24:115–125

    Article  PubMed  Google Scholar 

  9. Khan SA, Toledano MB, Taylor-Robinson SD (2008) Epidemiology, risk factors, and pathogenesis of cholangiocarcinoma. HPB (Oxford) 10:77–82

    Article  CAS  Google Scholar 

  10. Kubo S, Kinoshita H, Hirohashi K et al (1995) Hepatolithiasis associated with cholangiocarcinoma. World J Surg 19:637–641. doi:10.1007/BF00294744

    Article  CAS  PubMed  Google Scholar 

  11. Watanapa P, Watanapa WB (2002) Liver fluke-associated cholangiocarcinoma. Br J Surg 89:962–970

    Article  CAS  PubMed  Google Scholar 

  12. Kobayashi M, Ikeda K, Saitoh S et al (2000) Incidence of primary cholangiocellular carcinoma of the liver in Japanese patients with hepatitis C virus-related cirrhosis. Cancer 88:2471–2477

    Article  CAS  PubMed  Google Scholar 

  13. Yamamoto S, Kubo S, Hai S et al (2004) Hepatitis C virus infection as a likely etiology of intrahepatic cholangiocarcinoma. Cancer Sci 95:592–595

    Article  CAS  PubMed  Google Scholar 

  14. Tyson GL, El-Serag HB (2011) Risk factors for cholangiocarcinoma. Hepatology 54:173–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kubo S, Nakanuma Y, Takemura S et al (2014) Case series of 17 patients with cholangiocarcinoma among young adult workers of a printing company in Japan. J Hepatobiliary Pancreat Sci 21:479–488

    Article  PubMed  Google Scholar 

  16. Kubo S, Kinoshita M, Takemura S et al (2014) Characteristics of printing company workers newly diagnosed with occupational cholangiocarcinoma. J Hepatobiliary Pancreat Sci 21:809–817

    Article  PubMed  Google Scholar 

  17. Kinoshita M, Kubo S, Nakanuma Y et al (2016) Pathological spectrum of bile duct lesions from chronic bile duct injury to invasive cholangiocarcinoma corresponding to bile duct imaging findings of occupational cholangiocarcinoma. J Hepatobiliary Pancreat Sci 23:92–101

    Article  PubMed  Google Scholar 

  18. Welzel TM, Graubard BI, El-Serag HB et al (2007) Risk factors for intrahepatic and extrahepatic cholangiocarcinoma in the United States: a population-based case–control study. Clin Gastroenterol Hepatol 5:1221–1228

    Article  PubMed  PubMed Central  Google Scholar 

  19. Shaib YH, El-Serag HB, Davila JA et al (2005) Risk factors of intrahepatic cholangiocarcinoma in the United States: a case-control study. Gastroenterology 128:620–626

    Article  PubMed  Google Scholar 

  20. Hai S, Kubo S, Yamamoto S et al (2005) Clinicopathologic characteristics of hepatitis C virus-associated intrahepatic cholangiocarcinoma. Dig Surg 22:432–439

    Article  PubMed  Google Scholar 

  21. Wakabayashi H, Hashimoto N, Okano K et al (2008) Clinicopathological comparison between intrahepatic cholangiocarcinoma arising in livers positive and negative for hepatitis B or C virus. Liver Int 28:717–718

    Article  PubMed  Google Scholar 

  22. Ariizumi S, Kotera Y, Takahashi Y et al (2011) Mass-forming intrahepatic cholangiocarcinoma with marked enhancement on arterial-phase computed tomography reflects favorable surgical outcomes. J Surg Oncol 104:130–139

    Article  PubMed  Google Scholar 

  23. Zhou HB, Wang H, Li YQ et al (2011) Hepatitis B virus infection: a favorable prognostic factor for intrahepatic cholangiocarcinoma after resection. World J Gastroenterol 17:1292–1303

    Article  PubMed  PubMed Central  Google Scholar 

  24. 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 101:233–238

    Article  PubMed  Google Scholar 

  25. Uenishi T, Nagano H, Marubashi S et al (2014) The long-term outcomes after curative resection for mass-forming intrahepatic cholangiocarcinoma associated with hepatitis C viral infection: a multicenter analysis by Osaka Hepatic Surgery Study Group. J Surg Oncol 110:176–181

    Article  PubMed  Google Scholar 

  26. Kubo S, Uenishi T, Yamamoto S et al (2004) Clinicopathologic characteristics of small intrahepatic cholangiocarcinomas of mass-forming type. Hepatol Res 29:223–227

    Article  PubMed  Google Scholar 

  27. Li YY, Li H, Lv P et al (2011) Prognostic value of cirrhosis for intrahepatic cholangiocarcinoma after surgical treatment. J Gastrointest Surg 15:608–613

    Article  PubMed  Google Scholar 

  28. Komuta M, Govaere O, Vandecaveye V et al (2012) Histological diversity in cholangiocellular carcinoma reflects the different cholangiocyte phenotypes. Hepatology 55:1876–1888

    Article  CAS  PubMed  Google Scholar 

  29. Fujimoto A, Furuta M, Shiraishi Y et al (2015) Whole-genome mutational landscape of liver cancers displaying biliary phenotype reveals hepatitis impact and molecular diversity. Nat Commun 6:6120

    Article  CAS  PubMed  Google Scholar 

  30. Aishima S, Oda Y (2015) Pathogenesis and classification of intrahepatic cholangiocarcinoma: different characters of perihilar large duct type versus peripheral small duct type. J Hepatobiliary Pancreat Sci 22:94–100

    Article  PubMed  Google Scholar 

  31. Uenishi T, Hirohashi K, Kubo S et al (2001) Clinicopathological factors predicting outcome after resection of mass-forming intrahepatic cholangiocarcinoma. Br J Surg 88:969–974

    Article  CAS  PubMed  Google Scholar 

  32. Uenishi T, Ariizumi S, Aoki T et al (2014) Proposal of a new staging system for mass-forming 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 21:499–508

    Article  PubMed  Google Scholar 

  33. 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 18:443–452

    Article  PubMed  Google Scholar 

  34. Uenishi T, Yamamoto T, Takemura S et al (2014) Surgical treatment for intrahepatic cholangiocarcinoma. Clin J Gastroenterol 7:87–93

    Article  PubMed  Google Scholar 

  35. Yamamoto M, Ariizumi S (2011) Surgical outcomes of intrahepatic cholangiocarcinoma. Surg Today 41:896–902

    Article  PubMed  Google Scholar 

  36. Sakamoto Y, Kokudo N, Matsuyama Y et al (2016) Proposal of a new staging system for intrahepatic cholangiocarcinoma: analysis of surgical patients from a nationwide survey of the Liver Cancer Study Group of Japan. Cancer 122:61–70

    Article  PubMed  Google Scholar 

  37. Ribero D, Pinna AD, Guglielmi A et al (2012) Surgical approach for long-term survival of patients with intrahepatic cholangiocarcinoma: a multi-institutional analysis of 434 patients. Arch Surg 147:1107–1113

    Article  PubMed  Google Scholar 

  38. Marubashi S, Gotoh K, Takahashi H et al (2014) Prediction of the postoperative prognosis of intrahepatic cholangiocarcinoma (ICC): importance of preoperatively-determined anatomic invasion level and number of tumors. Dig Dis Sci 59:201–213

    Article  PubMed  Google Scholar 

  39. Luo X, Yuan L, Wang Y et al (2014) Survival outcomes and prognostic factors of surgical therapy for all potentially resectable intrahepatic cholangiocarcinoma: a large single-center cohort study. J Gastrointest Surg 18:562–572

    Article  PubMed  Google Scholar 

  40. Ellis MC, Cassera MA, Vetto JT et al (2011) Surgical treatment of intrahepatic cholangiocarcinoma: outcomes and predictive factors. HPB (Oxford) 13:59–63

    Article  Google Scholar 

  41. 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

    Article  PubMed  Google Scholar 

  42. Bektas H, Yeyrek C, Kleine M et al (2015) Surgical treatment for intrahepatic cholangiocarcinoma in Europe: a single center experience. J Hepatobiliary Pancreat Sci 22:131–137

    Article  PubMed  Google Scholar 

  43. Murakami Y, Uemura K, Sudo T et al (2012) Adjuvant chemotherapy with gemcitabine and S-1 after surgical resection for advanced biliary carcinoma: outcomes and prognostic factors. J Hepatobiliary Pancreat Sci 19:306–313

    Article  PubMed  Google Scholar 

  44. Shimada K, Sano T, Nara S et al (2009) Therapeutic value of lymph node dissection during hepatectomy in patients with intrahepatic cholangiocellular carcinoma with negative lymph node involvement. Surgery 145:411–416

    Article  PubMed  Google Scholar 

  45. Shimada M, Yamashita Y, Aishima S et al (2001) Value of lymph node dissection during resection of intrahepatic cholangiocarcinoma. Br J Surg 88:1463–1466

    Article  CAS  PubMed  Google Scholar 

  46. Bosman FT, Carneiro F, Hruban RH et al (2010) WHO classification of tumours of the digestive system World Health Organization of Tumours, 4th edn. World Health Organization, Lyon, pp 217–224

  47. Aishima S, Kuroda Y, Nishihara Y et al (2007) Proposal of progression model for intrahepatic cholangiocarcinoma: clinicopathologic differences between hilar type and peripheral type. Am J Surg Pathol 31:1059–1067

    Article  PubMed  Google Scholar 

  48. Pang YY (2002) The brisbane 2000 terminology of liver anatomy and resections. HPB 2000; 2: 333-39. HPB (Oxford) 4:99 (author reply 99–100)

    Article  Google Scholar 

  49. Lee CH, Chang CJ, Lin YJ et al (2009) Viral hepatitis-associated intrahepatic cholangiocarcinoma shares common disease processes with hepatocellular carcinoma. Br J Cancer 100:1765–1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Zhou Y, Zhao Y, Li B et al (2012) Hepatitis viruses infection and risk of intrahepatic cholangiocarcinoma: evidence from a meta-analysis. BMC Cancer 12:289

    Article  PubMed  PubMed Central  Google Scholar 

  51. Zhou YM, Cao L, Li B et al (2012) Expression of HBx protein in hepatitis B virus-infected intrahepatic cholangiocarcinoma. Hepatobiliary Pancreat Dis Int 11:532–535

    Article  PubMed  Google Scholar 

  52. Luh F, Kuei A, Fann P et al (2009) Intrahepatic cholangiocarcinoma and hepatitis: case study and literature review. Anticancer Res 29:3239–3243

    PubMed  Google Scholar 

  53. Liu W, Chen JR, Hsu CH et al (2012) A zebrafish model of intrahepatic cholangiocarcinoma by dual expression of hepatitis B virus X and hepatitis C virus core protein in liver. Hepatology 56:2268–2276

    Article  CAS  PubMed  Google Scholar 

  54. Ariizumi S, Yamamoto M (2015) Intrahepatic cholangiocarcinoma and cholangiolocellular carcinoma in cirrhosis and chronic viral hepatitis. Surg Today 45:682–687

    Article  PubMed  Google Scholar 

  55. Adachi T, Eguchi S (2014) Lymph node dissection for intrahepatic cholangiocarcinoma: a critical review of the literature to date. J Hepatobiliary Pancreat Sci 21:162–168

    Article  PubMed  Google Scholar 

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Correspondence to Hiroya Iida.

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Iida, H., Kaibori, M., Tanaka, S. et al. Low Incidence of Lymph Node Metastasis After Resection of Hepatitis Virus-Related Intrahepatic Cholangiocarcinoma. World J Surg 41, 1082–1088 (2017). https://doi.org/10.1007/s00268-016-3843-0

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