Endoscopy 2013; 45(11): 883-889
DOI: 10.1055/s-0033-1344760
Original article
© Georg Thieme Verlag KG Stuttgart · New York

Impact of preoperative endoscopic ultrasound-guided fine needle aspiration on postoperative recurrence and survival in cholangiocarcinoma patients

Abdul Hamid El Chafic
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
John Dewitt
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Julia Kim LeBlanc
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Ihab I El Hajj
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Gregory Cote
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Michael G House
2   Department of Surgery, Indiana University, Indianapolis, United States
Stuart Sherman
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Lee McHenry
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Henry A Pitt
2   Department of Surgery, Indiana University, Indianapolis, United States
Cynthia Johnson
3   Department of Biostatistics, Indiana University, Indianapolis, United States
Mehdi Mohamadnejad
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
Mohammad Al-Haddad
1   Department of Gastroenterology and Hepatology, Indiana University, Indianapolis, United States
› Author Affiliations
Further Information

Publication History

submitted 30 June 2012

sccepted after revision 01 July 2013

Publication Date:
28 October 2013 (online)

Background and study aim: Endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) is frequently performed for suspected biliary tumors for diagnosis and staging but carries a theoretical risk of needle-track seeding. We aimed to evaluate the impact of preoperative EUS-FNA on long-term outcomes for patients with cholangiocarcinoma (CCA).

Patients and methods: In a retrospective single-center study of consecutive patients with CCA with preoperative EUS-FNA, main outcome measures were overall survival and progression-free survival.

Results: In 150 patients with confirmed CCA, 61 underwent preoperative FNA. Median overall survival was 18.5 months (95 % confidence limits [CL] 15.4, 25.7): 111 patients died and 39 survived. Of the 150 patients, 119 underwent curative-intent surgical resection, with median progression-free survival of 17.8 months (95 %CL 14.5, 22.8); 89/119 patients had tumor recurrence or died, and 30/119 remained alive and disease-free. On multivariable analysis, overall survival was associated with: undergoing curative-intent surgery (hazard ratio [HR] 5.79, P = 0.001), lack of lymph node involvement (HR 1.89, P = 0.011), younger age (HR 1.51 for every 10 years, P < 0.0015), and small tumor size (HR 1.11 for every 1 cm, P = 0.029). For patients undergoing curative-intent surgery, on multivariable analysis, improved progression-free survival was associated with: lack of lymph node involvement (HR 1.88, P = 0.010), smaller tumor size (HR 1.16 for every 1 cm smaller, P = 0.003), and younger age (HR 1.53 for every 10 years, P < 0.001). Number of needle passes showed no statistically significant impact on overall survival.

Conclusion: Preoperative EUS-FNA in patients with CCA does not appear to adversely affect overall or progression-free survival.

  • References

  • 1 de Groen PC, Gores GJ, LaRusso NF et al. Biliary tract cancers. N Engl J Med 1999; 341: 1368-1378
  • 2 Jepsen P, Vilstrup H, Tarone RE et al. Incidence rates of intra- and extrahepatic cholangiocarcinomas in Denmark from 1978 through 2002. J Natl Cancer Inst 2007; 99: 895-897
  • 3 Khan SA, Taylor-Robinson SD, Toledano MB et al. Changing international trends in mortality rates for liver, biliary and pancreatic tumours. J Hepatol 2002; 37: 806-813
  • 4 Patel T. Increasing incidence and mortality of primary intrahepatic cholangiocarcinoma in the United States. Hepatology 2001; 33: 1353-1357
  • 5 Rajagopalan V, Daines WP, Grossbard ML et al. Gallbladder and biliary tract carcinoma: A comprehensive update, Part 1. Oncology (Williston Park) 2004; 18: 889-896
  • 6 Shaib YH, Davila JA, McGlynn K et al. Rising incidence of intrahepatic cholangiocarcinoma in the United States: a true increase?. J Hepatol 2004; 40: 472-477
  • 7 Welzel TM, McGlynn KA, Hsing AW et al. Impact of classification of hilar cholangiocarcinomas (Klatskin tumors) on the incidence of intra- and extrahepatic cholangiocarcinoma in the United States. J Natl Cancer Inst 2006; 98: 873-875
  • 8 West J, Wood H, Logan RF et al. Trends in the incidence of primary liver and biliary tract cancers in England and Wales 1971–2001. Br J Cancer 2006; 94: 1751-1758
  • 9 Gusani NJ, Balaa FK, Steel JL et al. Treatment of unresectable cholangiocarcinoma with gemcitabine-based transcatheter arterial chemoembolization (TACE): a single-institution experience. J Gastrointest Surg 2008; 12: 129-137
  • 10 Hemming AW, Reed AI, Fujita S et al. Surgical management of hilar cholangiocarcinoma. Ann Surg 2005; 241: 693-699 ; discussion 699 – 702
  • 11 Jarnagin WR, Fong Y, DeMatteo RP et al. Staging, resectability, and outcome in 225 patients with hilar cholangiocarcinoma. Ann Surg 2001; 234: 507-517 ; discussion 517 – 509
  • 12 Mohamadnejad M, DeWitt JM, Sherman S et al. Role of EUS for preoperative evaluation of cholangiocarcinoma: a large single-center experience. Gastrointest Endosc 2011; 73: 71-78
  • 13 Abu-Hamda EM, Baron TH. Endoscopic management of cholangiocarcinoma. Semin Liver Dis 2004; 24: 165-175
  • 14 Fritscher-Ravens A, Broering DC, Knoefel WT et al. EUS-guided fine-needle aspiration of suspected hilar cholangiocarcinoma in potentially operable patients with negative brush cytology. Am J Gastroenterol 2004; 99: 45-51
  • 15 Sugiyama M, Hagi H, Atomi Y et al. Diagnosis of portal venous invasion by pancreatobiliary carcinoma: value of endoscopic ultrasonography. Abdom Imaging 1997; 22: 434-438
  • 16 Byrne MF, Gerke H, Mitchell RM et al. Yield of endoscopic ultrasound-guided fine-needle aspiration of bile duct lesions. Endoscopy 2004; 36: 715-719
  • 17 DeWitt J, Misra VL, Leblanc JK et al. EUS-guided FNA of proximal biliary strictures after negative ERCP brush cytology results. Gastrointest Endosc 2006; 64: 325-333
  • 18 Eloubeidi MA, Chen VK, Jhala NC et al. Endoscopic ultrasound-guided fine needle aspiration biopsy of suspected cholangiocarcinoma. Clin Gastroenterol Hepatol 2004; 2: 209-213
  • 19 Lee JH, Salem R, Aslanian H et al. Endoscopic ultrasound and fine-needle aspiration of unexplained bile duct strictures. Am J Gastroenterol 2004; 99: 1069-1073
  • 20 Rosch T, Hofrichter K, Frimberger E et al. ERCP or EUS for tissue diagnosis of biliary strictures? A prospective comparative study. Gastrointest Endosc 2004; 60: 390-396
  • 21 Al-Leswas D, O'Reilly DA, Poston GJ. Biopsy of solid liver tumors: adverse consequences. Hepatobiliary Pancreat Dis Int 2008; 7: 325-327
  • 22 Doi S, Yasuda I, Iwashita T et al. Needle tract implantation on the esophageal wall after EUS-guided FNA of metastatic mediastinal lymphadenopathy. Gastrointest Endosc 2008; 67: 988-990
  • 23 Jones OM, Rees M, John TG et al. Biopsy of resectable colorectal liver metastases causes tumour dissemination and adversely affects survival after liver resection. Br J Surg 2005; 92: 1165-1168
  • 24 Micames C, Jowell PS, White R et al. Lower frequency of peritoneal carcinomatosis in patients with pancreatic cancer diagnosed by EUS-guided FNA vs. percutaneous FNA. Gastrointest Endosc 2003; 58: 690-695
  • 25 Paquin SC, Gariepy G, Lepanto L et al. A first report of tumor seeding because of EUS-guided FNA of a pancreatic adenocarcinoma. Gastrointest Endosc 2005; 61: 610-611
  • 26 Shah JN, Fraker D, Guerry D et al. Melanoma seeding of an EUS-guided fine needle track. Gastrointest Endosc 2004; 59: 923-924
  • 27 Wiksell H, Schassburger KU, Janicijevic M et al. Prevention of tumour cell dissemination in diagnostic needle procedures. Br J Cancer 2010; 103: 1706-1709
  • 28 Aloia TA, Charnsangavej C, Faria S et al. High-resolution computed tomography accurately predicts resectability in hilar cholangiocarcinoma. Am J Surg 2007; 193: 702-706
  • 29 Tsao JI, Nimura Y, Kamiya J et al. Management of hilar cholangiocarcinoma: comparison of an American and a Japanese experience. Ann Surg 2000; 232: 166-174
  • 30 Rosen CB, Heimbach JK, Gores GJ. Surgery for cholangiocarcinoma: the role of liver transplantation. HPB (Oxford) 2008; 10: 186-189
  • 31 Greene FL Page DL, Fleming ID et al. American Joint Committee on Cancer: AJCC cancer staging manual. 6th edition. New York: Springer-Verlag; 2002
  • 32 Smith EH. The hazards of fine-needle aspiration biopsy. Ultrasound Med Biol 1984; 10: 629-634
  • 33 Boutin C, Rey F, Viallat JR. Prevention of malignant seeding after invasive diagnostic procedures in patients with pleural mesothelioma. A randomized trial of local radiotherapy. Chest 1995; 108: 754-758
  • 34 Herts BR, Baker ME. The current role of percutaneous biopsy in the evaluation of renal masses. Semin Urol Oncol 1995; 13: 254-261
  • 35 Vaghefi H, Magi-Galluzzi C, Klein EA. Local recurrence of prostate cancer in rectal submucosa after transrectal needle biopsy and radical prostatectomy. Urology 2005; 66: 881
  • 36 Livraghi T, Damascelli B, Lombardi C et al. Risk in fine-needle abdominal biopsy. J Clin Ultrasound 1983; 11: 77-81
  • 37 Roussel F, Dalion J, Benozio M. The risk of tumoral seeding in needle biopsies. Acta Cytol 1989; 33: 936-939
  • 38 Smith EH. Complications of percutaneous abdominal fine-needle biopsy. Review. Radiology 1991; 178: 253-258
  • 39 Beane JD, House MG, Cote GA et al. Outcomes after preoperative endoscopic ultrasonography and biopsy in patients undergoing distal pancreatectomy. Surgery 2011; 150: 844-853
  • 40 Ikezawa K, Uehara H, Sakai A et al. Risk of peritoneal carcinomatosis by endoscopic ultrasound-guided fine needle aspiration for pancreatic cancer. J Gastroenterol 2013; 48: 966-972 . Epub 2012 Oct 13
  • 41 Hong SM, Presley AE, Stelow EB et al. Reconsideration of the histologic definitions used in the pathologic staging of extrahepatic bile duct carcinoma. Am J Surg Pathol 2006; 30: 744-749
  • 42 Chung YE, Kim MJ, Park YN et al. Staging of extrahepatic cholangiocarcinoma. Eur Radiol 2008; 18: 2182-2195
  • 43 Hong SM, Pawlik TM, Cho H et al. Depth of tumor invasion better predicts prognosis than the current American Joint Committee on Cancer T classification for distal bile duct carcinoma. Surgery 2009; 146: 250-257
  • 44 de Jong MC, Hong SM, Augustine MM et al. Hilar cholangiocarcinoma: tumor depth as a predictor of outcome. Arch Surg 2011; 146: 697-703
  • 45 Argani P, Shaukat A, Kaushal M et al. Differing rates of loss of DPC4 expression and of p53 overexpression among carcinomas of the proximal and distal bile ducts. Cancer 2001; 91: 1332-1341
  • 46 Yang B, House MG, Guo M et al. Promoter methylation profiles of tumor suppressor genes in intrahepatic and extrahepatic cholangiocarcinoma. Mod Pathol 2005; 18: 412-420
  • 47 Edge SB, Byrd DR, Compton CC. et al., eds. AJCC cancer staging manual. 7th edition. New York: Springer; 2010
  • 48 Su CH, Tsay SH, Wu CC et al. Factors influencing postoperative morbidity, mortality, and survival after resection for hilar cholangiocarcinoma. Ann Surg 1996; 223: 384-394
  • 49 Pichlmayr R, Weimann A, Klempnauer J et al. Surgical treatment in proximal bile duct cancer. A single-center experience. Ann Surg 1996; 224: 628-638
  • 50 Wakai T, Shirai Y, Moroda T et al. Impact of ductal resection margin status on long-term survival in patients undergoing resection for extrahepatic cholangiocarcinoma. Cancer 2005; 103: 1210-1216
  • 51 Lillemoe KD, Cameron JL. Surgery for hilar cholangiocarcinoma: the Johns Hopkins approach. J Hepatobiliary Pancreat Surg 2000; 7: 115-121
  • 52 Nakeeb A, Tran KQ, Black MJ et al. Improved survival in resected biliary malignancies. Surgery 2002; 132: 555-563 ; discussion 563-554
  • 53 Nakeeb A, Pitt HA, Sohn TA et al. Cholangiocarcinoma. A spectrum of intrahepatic, perihilar, and distal tumors. Ann Surg 1996; 224: 463-473 ; discussion 473 – 465
  • 54 Heron DE, Stein DE, Eschelman DJ et al. Cholangiocarcinoma: the impact of tumor location and treatment strategy on outcome. Am J Clin Oncol 2003; 26: 422-428
  • 55 Allen PJ, Reiner AS, Gonen M et al. Extrahepatic cholangiocarcinoma: a comparison of patients with resected proximal and distal lesions. HPB (Oxford) 2008; 10: 341-346
  • 56 Singal AG, Rakoski MO, Salgia R et al. The clinical presentation and prognostic factors for intrahepatic and extrahepatic cholangiocarcinoma in a tertiary care centre. Aliment Pharmacol Ther 2010; 31: 625-633
  • 57 Hernandez J, Cowgill SM, Al-Saadi S et al. An aggressive approach to extrahepatic cholangiocarcinomas is warranted: margin status does not impact survival after resection. Ann Surg Oncol 2008; 15: 807-814