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Figure 1.
Survival based on presence or absence of positive histologic margins (P = .9).

Survival based on presence or absence of positive histologic margins (P = .9).

Figure 2.
Overall survival among 77 patients evaluated.

Overall survival among 77 patients evaluated.

Figure 3.
Survival curves categorized by type of surgical resection (P<.001).

Survival curves categorized by type of surgical resection (P<.001).

Table 1. 
Patient Characteristics and Laboratory Data on Admission*
Patient Characteristics and Laboratory Data on Admission*
Table 2. 
Tumor Location*
Tumor Location*
Table 3. 
Operative Mortality and Complications
Operative Mortality and Complications
Table 4. 
Analysis of Factors Predictive of Survival
Analysis of Factors Predictive of Survival
Table 5. 
Published Series on Resectional Treatment of Cholangiocarcinoma, 1980-2000*
Published Series on Resectional Treatment of Cholangiocarcinoma, 1980-2000*
1.
Greenlee  RTMurray  TBolden  SWingo  PA Cancer statistics, 2000. CA Cancer J Clin. 2000;507- 33Article
2.
Klatskin  G Adenocarcinoma of the hepatic duct at its bifurcation within the porta hepatis an unusual tumor with distinctive clinical and pathological features. Am J Med. 1965;38241- 256Article
3.
Brown  GMyers  N The hepatic ducts: a surgical approach for resection of tumours. Aust N Z J Surg. 1954;23308- 312Article
4.
Altmeier  WAGall  EAZinninger  MHHoxworth  PI Sclerosing carcinoma of the major intrahepatic bile ducts. Arch Surg. 1957;75450- 461Article
5.
Pitt  HADooley  WCYeo  CJCameron  JL Malignancies of the biliary tree. Curr Probl Surg. 1995;321- 90Article
6.
Tsuzuki  TUekusa  M Carcinoma of the proximal bile duct. Surg Gynecol Obstet. 1978;146933- 943
7.
Mizumoto  RKawarada  YSuzuki  H Surgical treatment of hilar carcinoma of the bile duct. Surg Gynecol Obstet. 1986;162153- 158
8.
Nimura  YHayakawa  NKamiya  JKondo  SShionoya  S Hepatic segmentectomy with caudate lobe resection for bile duct carcinoma of the hepatic hilus. World J Surg. 1990;14535- 544Article
9.
Blumgart  LHHadjis  NSBenjamin  ISBeazley  RM Surgical approaches to cholangiocarcinoma at the confluence of the hepatic ducts. Lancet. 1984;166- 70Article
10.
Gazzaniga  GMFaggioni  AFilauro  M Surgical treatment of proximal bile duct tumors. Int Surg. 1985;7045- 48
11.
Iwasaki  YOkamura  TOzaki  A  et al.  Surgical treatment of carcinoma of the confluence of major hepatic ducts. Surg Gynecol Obstet. 1986;162457- 464
12.
Pinson  CWRossi  RL Extended right hepatic lobectomy, left hepatic lobectomy and skeletonization resection for proximal bile duct cancer. World J Surg. 1988;1252- 59Article
13.
Launois  BLebeau  GKioff  GOddi  RCampion  JP Survival after surgical resection of carcinoma of the upper third of the biliary tract. Dig Surg. 1990;7106- 110Article
14.
Pichlmayr  RRinge  BLauchart  WBechstein  WOGubernatis  GWagner  E Radical resection and liver grafting as the two main components of surgical strategy in the treatment of proximal bile duct cancer. World J Surg. 1988;1268- 77Article
15.
Bismuth  HNakache  RDiamond  T Management strategies in resection for hilar cholangiocarcinoma. Ann Surg. 1992;21531- 38Article
16.
Chung  CBautista  NO'Connell  TX Prognosis and treatment of bile duct carcinomas. Am Surg. 1998;64921- 925
17.
Terblanche  JKahn  DBornman  PCWerener  D The role of U tube palliative treatment in high bile duct carcinoma. Surgery. 1988;103624- 632
18.
Lai  ECSTompkins  RKRoslyn  JJMann  LL Proximal bile duct cancer: quality of survival. Ann Surg. 1987;205111- 118Article
19.
Gibson  RNYeung  EHadjis  N  et al.  Percutaneous transhepatic endoprostheses for hilar cholangiocarcinoma. Am J Surg. 1989;157395- 399Article
20.
Longmire  WPMcArthur  MSBastounis  EAHiatt  J Carcinoma of the extrahepatic biliary tract. Ann Surg. 1973;178333- 345Article
21.
Kuwayti  KBaggenstoss  AHStauffer  MHPriestley  JT Carcinoma of the major intrahepatic and the extrahepatic bile ducts exclusive of the papilla of Vater. Surg Gynecol Obstet. 1957;104357- 366
22.
Kirshbaum  JDKozoll  DD Carcinoma of the gall bladder and extrahepatic bile ducts. Surg Gynecol Obstet. 1941;73740- 754
23.
Yamaguchi  KEnjoji  MNakayama  F Cancer of the extrahepatic bile duct: a clinicopathologic study of immunochemistry for CEA, CA 19-9, and p21. World J Surg. 1988;1211- 17Article
24.
Nagorney  DMDonohue  JHFarnell  MBSchleck  CDIlstrup  DM Outcomes after curative resections of cholangiocarcinoma. Arch Surg. 1993;128871- 879Article
25.
Burke  ECJarnagin  WRHochwald  SNPisters  PWTFong  YBlumgart  LH Hilar cholangiocarcinoma: patterns of spread, the importance of hepatic resection for curative operation, and a presurgical clinical staging system. Ann Surg. 1998;228385- 394Article
26.
Launois  BTerblanche  JLakehal  M  et al.  Proximal bile duct cancer: high resectability rate and 5-year survival. Ann Surg. 1999;230266- 275Article
27.
Schoenthaler  RPhillips  TLCastro  JEfird  JTBetter  AWay  LW Carcinoma of the extrahepatic bile ducts: the University of California at San Francisco experience. Ann Surg. 1994;219267- 274Article
28.
Washburn  WKLewis  DJenkins  KL Aggressive surgical resection for cholangiocarcinoma. Arch Surg. 1995;130270- 276Article
29.
Tompkins  RKThomas  DWile  ALongmire  WP Prognostic factors in bile duct carcinoma: analysis of 96 cases. Ann Surg. 1981;194447- 457Article
30.
Klempnauer  JRidder  GJvon Wasielewski  RWerner  MWeimann  APichlmayr  R Resectional surgery of hilar cholangiocarcinoma: a multivariate analysis of prognostic factors. J Clin Oncol. 1997;15947- 954
31.
Klempnauer  JRidder  GJWerner  MWeimann  APichlmayr  R What constitutes long-term survival after surgery for hilar cholangiocarcinoma? Cancer. 1997;7926- 34Article
32.
Pichlmayr  RWeimann  AKlempnauer  J  et al.  Surgical treatment in proximal bile duct cancer: a single center experience. Ann Surg. 1996;224628- 638Article
33.
Fortner  JGVitelli  CEMaclean  BJ Proximal extrahepatic bile duct tumors: analysis of a series of 52 consecutive patients treated over a period of 13 years. Arch Surg. 1989;1241275- 1279Article
34.
Smith  ACDowsett  JFHatfield  ARW  et al.  Prospective randomized trial of bypass surgery versus endoscopic stenting in patients with malignant obstructive jaundice. Gut. 1989;301513Article
35.
Lai  ESCChu  KMLo  CYFan  STLo  CMWong  J Coice of palliation for malignant hilar obstruction. Am J Surg. 1992;163208- 212Article
36.
Nordback  IHPitt  HAColeman  JA  et al.  Unresectable hilar cholangiocarcinoma: percutaneous versus operative palliation. Surgery. 1994;115597- 603
37.
Bornman  PCHarries-Jones  EPTobias  Rvan Stiegman  GTerblanche  J Prospective controlled trial of transhepatic biliary endoprosthesis versus bypass surgery for incurable carcinoma of the head of the pancreas. Lancet. 1986;169- 71Article
38.
Shepherd  HARoyle  GRoss  APRDiba  AArthur  MColin-Jones  D Endoscopic biliary endoprosthesis in palliation of malignant obstruction of the distal common bile duct: a randomized trial. Br J Surg. 1988;751166- 1168Article
39.
Andersen  JRSorensen  SMKruse  ARokkjaer  MMatzen  P Randomized trial of endoscopic endoprosthesis versus operative bypass in malignant obstructive jaundice. Gut. 1989;301132- 1135Article
40.
Guthrie  CMHaddock  GDe Beaux  ACGarden  OJCarter  DC Changing trends in the management of extrahepatic cholangiocarcinoma. Br J Surg. 1993;801434- 1439Article
41.
Tsuzuki  TYoshiro  OIida  SNakanishi  ITakenaka  YYoshii  H Carcinoma of the bifurcation of the hepatic ducts. Arch Surg. 1983;1181147- 1151Article
42.
Alexander  FRossi  RLO'Bryan  MKhettry  UBraasch  JWWatkins  E Biliary carcinoma: a review of 109 cases. Am J Surg. 1984;147503- 509Article
43.
Tsuzuki  TUeda  MKuramochi  SIida  STakahashi  SIri  H Carcinoma of the main hepatic duct junction: indications, operative morbidity and mortality, and long-term survival. Surgery. 1990;108495- 501
44.
Ouchi  KMatsuno  SSato  T Long-term survival in carcinoma of the biliary tract: analysis of prognostic factors in 146 resections. Arch Surg. 1989;124248- 252Article
45.
Tompkins  RKSaunders  KRoslyn  JJLongmire  WP Changing patterns in diagnosis and management of bile duct cancer. Ann Surg. 1990;211614- 621
46.
Boerma  EJ Research into the results of resection of hilar bile duct cancer. Surgery. 1990;108572- 580
47.
Hadjis  NSBlenkharn  JIAlexander  NBenjamin  ISBlumgart  LH Outcome of radical surgery in hilar cholangiocarcinoma. Surgery. 1990;107597- 604
48.
Reding  RBuard  JLLebeau  GLaunois  B Surgical management of 552 carcinomas of the extrahepatic bile ducts (gallbladder and periampullary tumors excluded): results of the French surgical association survey. Ann Surg. 1991;213236- 241Article
49.
Childs  THart  M Aggressive surgical therapy for Klatskin tumors. Am J Surg. 1993;165554- 555Article
50.
Baer  HUStain  SCDennison  AREggers  BBlumgart  LH Improvements in survival by aggressive resections of hilar cholangiocarcinoma. Ann Surg. 1993;21720- 27Article
51.
Ogura  YMizumoto  RTabata  MMatsuda  SKusuda  T Surgical treatment of carcinoma of the hepatic duct confluence: analysis of 55 resected carcinomas. World J Surg. 1993;1785- 93Article
52.
Tashiro  STsuji  TKanemitsu  KKamimoto  YHiraoka  TMiyauchi  Y Prolongation of survival of carcinoma at the hepatic duct confluence. Surgery. 1993;113270- 278
53.
Koyama  KTanaka  JSato  YSeki  HKato  YUmezawa  A Experience in twenty patients with carcinoma of hilar bile duct treated by resection targeting chemotherapy and intracavitary irradiation. Surg Gynecol Obstet. 1993;176239- 245
54.
Myburgh  JA Resection and bypass for malignant obstruction of the bile duct. World J Surg. 1995;19108- 112Article
Original Article
February 2001

Surgical Treatment and Outcomes in Carcinoma of the Extrahepatic Bile DuctsThe University of Rochester Experience

Author Affiliations

From the Department of Surgery, University of Southern California, Los Angeles (Dr Blom); and the Department of Surgery, University of Rochester, Rochester, NY (Dr Schwartz).

Arch Surg. 2001;136(2):209-214. doi:10.1001/archsurg.136.2.209
Abstract

Hypothesis  To our knowledge, few individual surgeons and only a handful of institutions have gained a meaningful experience with the treatment of adenocarcinoma of the extrahepatic bile ducts or cholangiocarcinoma. The purpose of this study was to critically evaluate the experience of a single center in the treatment of these tumors.

Design  Retrospective cohort study with a median follow-up of 48 months.

Setting  Department of surgery at a university referral center.

Patients  Seventy-seven patients with biopsy-confirmed adenocarcinoma of the extrahepatic bile ducts evaluated and treated between January 1980 and February 1998.

Main Outcome Measures  Prognostic variables, resectability rates, morbidity, and survival.

Results  Thirty-eight male and 39 female patients were studied (median age, 71 years). Twenty-three patients (30%) underwent curative resections, 32 patients (41%) underwent palliative surgery, and 22 patients (29%) received nonoperative therapies. The 30-day perioperative morbidity rate was 18%, and mortality was 6%. Overall median survival was 11 months; 4 months for patients receiving nonoperative therapy; 8 months for patients recieving palliative surgery; and 72 months for curative resection. Five-year survival rates were 23%, 0%, 10%, and 55%, respectively. Curative resection was the only prognostic variable to have a statistically significant effect on survival.

Conclusions  Curative resection could be achieved in approximately one third of patients who had cholangiocarcinoma, and should be the goal of treatment. Survival is significantly improved in those patients who are considered to have resectable tumors and who undergo removal of all gross disease. Palliative surgical treatments also revealed a survival advantage over nonoperative therapies.

ADENOCARCINOMA OF the extrahepatic bile ducts, or cholangiocarcinoma, is a rare malignant neoplasm. In the United States, it is estimated that extrahepatic biliary cancers will represent less than 1% of all new cancers and less than 3% of gastrointestinal cancers in the year 2000. During the same period, approximately 50% of these patients will die of their disease.1 Because of this, few individual surgeons and only a handful of institutions have gained significant experience with these tumors.

Often referred to as Klatskin tumors, after the internist Gerald Klatskin who described 13 cases of sclerosing adenocarcinoma localized to the hepatic duct bifurcation in 1965,2 the first resection of a primary cancer of the hepatic duct bifurcation was reported by Brown and Myers3 in 1954, and in 1957, Altmeier et al4 described proximal bile duct neoplasia as a cause of jaundice.

The precise cause of these tumors remains unknown. Cholangiocarcinoma is uncommon in patients younger than 40 years, with most tumors occurring in patients aged between 50 and 70 years. When discovered, they tend to be small, exhibit a slow rate of growth, and rarely metastasize.5 Reported resectability rates, however, vary widely in the literature (10%-90% resectability).615 Local invasion and proximity of vital structures within the porta hepatis contribute to the difficulty in achieving complete tumor clearance, and local recurrence is common. For these reasons, cholangiocarcinoma continues to represent a therapeutic dilemma and technical challenge to the surgeon, leading many to adopt a nihilistic approach to the treatment of these tumors.1619

The purpose of this study was to critically evaluate the experience of a single tertiary referral center in the treatment of adenocarcinoma of the extrahepatic bile ducts and to determine the prognostic factors, the rate of tumor resectability, morbidity rates, and survival for these patients.

PATIENTS AND METHODS

Medical records of all patients evaluated and treated for adenocarcinoma of the extrahepatic bile ducts at the University of Rochester School of Medicine and Dentistry (Strong Memorial Hospital, Department of Surgery, Rochester, NY) between January 1980 and February 1998 were retrospectively reviewed. Patients without pathologic confirmation of the diagnosis of adenocarcinoma of the extrahepatic bile ducts, or with a diagnosis of carcinoma of the Vater ampulla, carcinoma of the gallbladder, or primary adenocarcinoma of the intrahepatic bile ducts were excluded from this study.

Admission notes, consultations, laboratory reports, radiologic imaging reports, operative reports, and pathology reports, as well as discharge summaries and follow-up records were reviewed. Variables measured at admission included patient demographics, the symptoms of pain and pruritus, jaundice, weight loss, presence of cholangitis, total serum bilirubin (mg/dL), and alkaline phosphatase (U/L). Preoperative diagnostic modalities, tumor location, and type of operation were recorded. Tumor location was categorized into upper, middle, and lower tumors based on the system of Longmire et al.20 The main outcome measures were tumor resectability, the development of complications, and survival. Perioperative morbidity and mortality were defined as any complication or death occurring within 30 days of operation.

Patients were grouped into 1 of 3 categories: tumor unresectable for cure, nonoperative intervention (group 1); tumor unresectable for cure, palliative surgical procedure performed (group 2); and tumor potentially resectable for cure (group 3). A potentially curative procedure was defined by the ability to remove all tumor with negative surgical margins at the initial operation. Palliative procedures consisted of any operation that left residual tumor in situ.

Patient survival was calculated using the Kaplan-Meier method and included all hospital deaths. Survival differences were assessed using the log-rank test. Univariate analysis was accomplished using the χ2 test for nominal data and 1-way analysis of variance for comparisons of mean values. A P value less than or equal to .05 was considered to be significant. Statistical analysis was performed using SPSS version 7.5 (Statistical Package for Social Science; SPSS Inc, Chicago, Ill).

RESULTS

Seventy-seven patients with adenocarcinoma of the extrahepatic bile ducts were studied. There were 39 women and 38 men with a median age of 71 years (range, 38-89 years). Median time to follow-up was 48 months (range, 1-96 months). Patient characteristics and admission findings are listed in Table 1. No significant differences were found between study groups. Five patients (7%) underwent operative procedures without a radiologic workup that consisted of computed tomography scanning of the abdomen and/or biliary imaging using endoscopic retrograde cholangiopancreatography and percutaneous transhepatic cholangiography. Painless jaundice was the admitting complaint in 44% of patients.

The distribution of tumor locations for each of the patient groups is presented in Table 2. Forty-five percent of patients had tumors of the upper third of the extrahepatic biliary system, 38% had tumors of the middle third, 7% had tumors of the lower third, and 10% had diffuse disease. No significant differences were found in tumor location between study groups.

Tumor resectability was determined by the operating surgeon, and based on preoperative imaging studies or findings at celiotomy. Twenty-two patients (29%) were determined preoperatively to have unresectable tumors and underwent nonoperative therapies such as percutaneous transhepatic or endoscopic biliary drainage. Fifty-five patients (71%) underwent an exploratory celiotomy. Of these 55 patients, 32 (58%) had a palliative resection and/or a biliary bypass procedure after it was determined intraoperatively that a complete curative resection could not be safely performed. The remaining 23 patients (42%) underwent a potentially curative resection. In 16 patients, this consisted of the complete resection of the tumor and a Roux-en-Y biliary-enteric reconstruction; 4 patients underwent pancreaticoduodenectomy (Whipple procedure); 2 patients required hepatic resection; and 1 patient had an orthotopic liver transplant. These 23 patients represent 30% of all patients evaluated in this study. Data on the histological margin status were available for 19 (83%) of these 23 patients. Fifteen patients (79%) underwent complete tumor resections with negative histological margins, whereas in 4 patients, there was microscopic residual disease. Interestingly, no statistically significant difference was found in the survival curves of these 2 groups (Figure 1). In 2 cases, a hepatic resection was necessary to ensure negative margins, and 1 patient with concomitant biliary cirrhosis underwent hepatic transplantation.

Perioperative morbidity occurred in 10 patients (18%). Of note, 14% (3 patients) in group 1 developed cholangitis, biliary obstruction, and intractable ascites, respectively, while hospitalized. The 30-day operative mortality was 6%, with 4 of 5 deaths occurring in patients undergoing noncurative procedures (Table 3). Overall median survival time and 5-year survival rate were 11 months and 23%, respectively (Figure 2). Group 1 patients had a median survival of 4 months, with 0% 5-year survivors. Patients in group 2 had a median survival of 8 months, and 10% survived 5 years. Patients in group 3, had a median survival of 72 months and a 5-year survival of 55%. Two patients died of recurrent disease after 5 years at 72 months and 78 months, respectively. Fourteen patients (22%) remain alive with a mean follow-up of 48 months.

Type of resection was the only independent variable found to demonstrate a significant effect on survival (Figure 3). Patient age, sex, tumor location, presence of jaundice, weight loss, abdominal pain, pruritus, cholangitis, and admission of total bilirubin or alkaline phosphatase had no statistically significant impact on median or 5-year survival (Table 4).

COMMENT

Adenocarcinoma of the extrahepatic bile ducts, or cholangiocarcinoma, is a rare tumor. In autopsy studies, the incidence ranges between 0.01% and 0.5%.2123 It is estimated that 6900 new cases of cancer of the extrahepatic bile ducts and gallbladder will be diagnosed in the United States in 2000.1 Although the exact cause remains unknown, several factors have been associated with the development of this malignant neoplasm: ulcerative colitis or primary sclerosing cholangitis, choledochal cysts, hepatolithiasis, parasitic infection, and chemical carcinogens.5 Because of its rarity, indolent growth pattern, local invasiveness, and close proximity to vital structures challenging surgical resection, definitive guidelines regarding optimal surgical treatment and cure rates have been difficult to establish. There are quite disparate opinions in the literature regarding the resectability and curability of these tumors.1619,2426 However, recently there seems to be increasing support for an aggressive surgical approach to the treatment of cholangiocarcinoma.

The current study was conducted to examine the prognostic factors and outcomes in the treatment of cholangiocarcinoma at our institution. In the patient population evaluated, the clinical presentation and the pathologic features of these tumors were similar to those of previous reports.16,2628 The distribution of tumor locations is also similar to those reported in several recent series.16,24,27,29 Although tumors located in the lower third enjoyed longer median survival and 5-year survival, this did not reach statistical significance. The literature is divided regarding the importance of tumor location as a prognostic variable. Several investigators have reported that tumors located in the lower third of the biliary tree have a more favorable prognosis, while others have found no differences in survival.16,24,27,28 This finding, however, may be attributable to the increased ability to remove all macroscopic disease with a pancreaticoduodenectomy compared with tumors found more distally.

Jaundice was the most common indicator, followed by weight loss and abdominal pain. The presence, absence, or degree to which these signs and symptoms were present demonstrated no significant impact on prognosis. This finding is similar to that of other large series on resections for cholangiocarcinoma, which found that only those variables that correlate to the inability to remove all macroscopic disease (ie, residual tumor or positive lymph nodes) adversely affected survival.30,31 In fact, the only variable that affected survival in the current study was the ability to completely remove all macroscopic tumor at celiotomy. This finding corresponds with and corroborates several recent studies that have shown complete resection to prolong survival.2426,32

The observation that margin status did not significantly impact survival can likely be explained by the small numbers of patients involved and the indolent growth pattern of these tumors.33 Pichlmayr et al32 in a large series from Germany also found that incomplete resection imparted a survival advantage, albeit less than a complete resection, and could lead to survival times greater than 5 years. This study, however, was able to accumulate 249 patients through a nationwide referral pattern. In the current series, only 4 patients who underwent a potentially curative resection had microscopically positive margins, and although survival was not found to be statistically different, all of these patients eventually succumbed to their disease. We would therefore agree with other authors that an aggressive policy of resection whenever possible in the treatment of these tumors is warranted, and that a complete resection is the best chance for cure and should be the goal of resectional therapy.25

In most of our patients, this was possible without the use of hepatic resection or transplantation; however, we have begun to more liberally use these procedures to assure negative histologic margins in those patients considered suitable candidates.

This aggressive approach is also warranted on the grounds that in the event that a complete resection cannot be performed, removal of all macroscopic disease alone imparts a significant survival advantage and would seem to be the best form of palliation. This study revealed a large survival advantage for patients undergoing a potentially curative tumor resection and a statistically significant survival advantage in patients with macroscopic disease left in situ or bypassed compared with nonoperative therapies. A review of the literature evaluating surgical vs nonsurgical palliation does not reveal a consistent survival advantage for one form of palliation over another.3439 However, several series have found a similar increase in survival and perhaps more importantly, an improved quality of life after surgical palliation, free from percutaneous drainage tubes, with lower rates of cholangitis and hospitalizations compared with endoscopic or percutaneous palliation. Table 540 lists a survey of the published series since 1980 demonstrating rates of tumor resection and patient mortality and survival.

In conclusion, the findings of this review support an aggressive approach to patients presenting with adenocarcinoma of the extrahepatic bile ducts. In those patients considered suitable candidates, all efforts should be made to completely resect the tumor with negative histologic margins. If this is not possible, complete resection of all macroscopic disease seems to improve survival and provide optimal palliation of jaundice and its sequelae. Even patients in whom residual tumor must be left behind or on whom a surgical bypass must be performed experience a statistically significant increase in survival over nonoperative therapies. This surgical approach can be conducted with low perioperative morbidity rates and mortalities.

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Article Information

We thank Ngoc Thai, MD, for his assistance in the preparation of the manuscript.

Reprints: Seymour I. Schwartz, MD, FACS, Department of Surgery, School of Medicine and Dentistry, University of Rochester, 601 Elmwood Ave, Rochester, NY 14642.

References
1.
Greenlee  RTMurray  TBolden  SWingo  PA Cancer statistics, 2000. CA Cancer J Clin. 2000;507- 33Article
2.
Klatskin  G Adenocarcinoma of the hepatic duct at its bifurcation within the porta hepatis an unusual tumor with distinctive clinical and pathological features. Am J Med. 1965;38241- 256Article
3.
Brown  GMyers  N The hepatic ducts: a surgical approach for resection of tumours. Aust N Z J Surg. 1954;23308- 312Article
4.
Altmeier  WAGall  EAZinninger  MHHoxworth  PI Sclerosing carcinoma of the major intrahepatic bile ducts. Arch Surg. 1957;75450- 461Article
5.
Pitt  HADooley  WCYeo  CJCameron  JL Malignancies of the biliary tree. Curr Probl Surg. 1995;321- 90Article
6.
Tsuzuki  TUekusa  M Carcinoma of the proximal bile duct. Surg Gynecol Obstet. 1978;146933- 943
7.
Mizumoto  RKawarada  YSuzuki  H Surgical treatment of hilar carcinoma of the bile duct. Surg Gynecol Obstet. 1986;162153- 158
8.
Nimura  YHayakawa  NKamiya  JKondo  SShionoya  S Hepatic segmentectomy with caudate lobe resection for bile duct carcinoma of the hepatic hilus. World J Surg. 1990;14535- 544Article
9.
Blumgart  LHHadjis  NSBenjamin  ISBeazley  RM Surgical approaches to cholangiocarcinoma at the confluence of the hepatic ducts. Lancet. 1984;166- 70Article
10.
Gazzaniga  GMFaggioni  AFilauro  M Surgical treatment of proximal bile duct tumors. Int Surg. 1985;7045- 48
11.
Iwasaki  YOkamura  TOzaki  A  et al.  Surgical treatment of carcinoma of the confluence of major hepatic ducts. Surg Gynecol Obstet. 1986;162457- 464
12.
Pinson  CWRossi  RL Extended right hepatic lobectomy, left hepatic lobectomy and skeletonization resection for proximal bile duct cancer. World J Surg. 1988;1252- 59Article
13.
Launois  BLebeau  GKioff  GOddi  RCampion  JP Survival after surgical resection of carcinoma of the upper third of the biliary tract. Dig Surg. 1990;7106- 110Article
14.
Pichlmayr  RRinge  BLauchart  WBechstein  WOGubernatis  GWagner  E Radical resection and liver grafting as the two main components of surgical strategy in the treatment of proximal bile duct cancer. World J Surg. 1988;1268- 77Article
15.
Bismuth  HNakache  RDiamond  T Management strategies in resection for hilar cholangiocarcinoma. Ann Surg. 1992;21531- 38Article
16.
Chung  CBautista  NO'Connell  TX Prognosis and treatment of bile duct carcinomas. Am Surg. 1998;64921- 925
17.
Terblanche  JKahn  DBornman  PCWerener  D The role of U tube palliative treatment in high bile duct carcinoma. Surgery. 1988;103624- 632
18.
Lai  ECSTompkins  RKRoslyn  JJMann  LL Proximal bile duct cancer: quality of survival. Ann Surg. 1987;205111- 118Article
19.
Gibson  RNYeung  EHadjis  N  et al.  Percutaneous transhepatic endoprostheses for hilar cholangiocarcinoma. Am J Surg. 1989;157395- 399Article
20.
Longmire  WPMcArthur  MSBastounis  EAHiatt  J Carcinoma of the extrahepatic biliary tract. Ann Surg. 1973;178333- 345Article
21.
Kuwayti  KBaggenstoss  AHStauffer  MHPriestley  JT Carcinoma of the major intrahepatic and the extrahepatic bile ducts exclusive of the papilla of Vater. Surg Gynecol Obstet. 1957;104357- 366
22.
Kirshbaum  JDKozoll  DD Carcinoma of the gall bladder and extrahepatic bile ducts. Surg Gynecol Obstet. 1941;73740- 754
23.
Yamaguchi  KEnjoji  MNakayama  F Cancer of the extrahepatic bile duct: a clinicopathologic study of immunochemistry for CEA, CA 19-9, and p21. World J Surg. 1988;1211- 17Article
24.
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