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10.1245/ASO.2006.05.053
Annals of Surgical Oncology 13:872-880 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Improved Outcome of Resection of Hilar Cholangiocarcinoma (Klatskin Tumor)

Sander Dinant, MD1, Michael F. Gerhards, MD1, E. A. J. Rauws, MD2, Olivier R. C. Busch, MD1, Dirk J. Gouma, MD1 and Thomas M. van Gulik, MD1

1 Department of Surgery, Academic Medical Center, P.O. Box 227001100 DE Amsterdam The Netherlands
2 Department of Gastroenterology, Academic Medical Center, P.O. Box 22700, 1100 DE Amsterdam The Netherlands

Correspondence: Address correspondence and reprint requests to: Thomas M. van Gulik, MD; E-mail: t.m.vangulik{at}amc.uva.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Treatment of hilar cholangiocarcinoma (Klatskin tumors) has changed in many aspects. A more extensive surgical approach, as proposed by Japanese surgeons, has been applied in our center over the last 5 years; it combines hilar resection with partial hepatectomy for most tumors. The aim of this study was to assess the outcome of a 15-year evolution in the surgical treatment of Klatskin tumors.

Methods: A total of 99 consecutive patients underwent resection for hilar cholangiocarcinoma in three 5-year time periods: periods 1 (1988–1993; n = 45), 2 (1993–1998; n = 25), and 3 (1998–2003; n = 29). Outcome was evaluated by assessment of completeness of resection, postoperative morbidity and mortality, and survival.

Results: The proportion of margin negative resections increased significantly from 13% in period 1 to 59% in period 3 (P < .05). Two-year survival increased significantly from 33% ± 7% and 39% ± 10% in periods 1 and 2 to 60% ± 11% in period 3 (P < .05). Postoperative morbidity and mortality were considerable but did not increase with this changed surgical strategy (68% and 10%, respectively, in period 3). Lymph node metastasis was, next to period of resection, also associated with survival in univariate analysis.

Conclusions: Mainly in the last 5-year period (1998–2003), when the Japanese surgical approach was followed, more hilar resections were combined with partial liver resections that included segments 1 and 4, thus leading to more R0 resections. This, together with a decrease in lymph node metastases, resulted in improved survival without significantly affecting postoperative morbidity or mortality.

Key Words: Hilar cholangiocarcinoma • Hepatectomy • Liver • Surgery • Mortality • Survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Treatment of hilar cholangiocarcinoma or adenocarcinoma of the hepatic duct confluence, first described by Klatskin1 in 1965, remains a great surgical challenge. Whereas surgical resection offers the only chance for cure, resections with a free margin are difficult to achieve because of the relation of these tumors with different structures in the liver hilum and frequent infiltration into the intrahepatic biliary system. Invasive growth into important structures such as the portal venous system, hepatic artery, or both has often occurred at the onset of clinical symptoms.2–4

The treatment of hilar cholangiocarcinoma has changed over the last three decades. In the 1970s and 1980s, hepatic resections were infrequently performed, whereas during the last 15 years, a more aggressive approach including extensive liver resections prevailed.5–10 Several, mainly Japanese, authors have emphasized the importance of complete resection with tumor-free margins for improved survival.2,11–17 When American and Japanese experience with surgical management of hilar cholangiocarcinoma was compared, it was found that combined hilar resection and partial hepatectomy including caudate lobe resection, as performed by Japanese surgeons, contributed to a higher margin-negative resection rate.17 Resection of segments 4 and 1 (caudate lobe) was advocated, because frequent invasive growth into the anterior and posterior segments of the liver could be shown.18–20

Also in our institution, an increasing proportion of patients with hilar cholangiocarcinoma underwent hilar resection combined with partial liver resection as of the early 1990s. Before this time, most tumors were treated by local resection. The outcome of resections from 1983 to 1997 was described by Gerhards et al.11,21 In 1998, collaboration was initiated with the Division of Surgical Oncology of Nagoya University in Japan, with the aim of adopting the techniques developed by Japanese surgeons. From that time, hilar resections were performed en bloc with (extended) hemihepatectomy, routinely including complete resection of the caudate lobe and lymphadenectomy of the hepatoduodenal ligament. In case of portal vein involvement, resection was combined with excision of the portal bifurcation and reconstruction of the vein. The aim of this study was to assess the outcome of this change in surgical strategy, based on Japanese experience, in patients with hilar cholangiocarcinoma with regard to postoperative morbidity and mortality, microscopic tumor clearance, and patient survival.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From January 1988 to January 2003, 99 patients with hilar cholangiocarcinoma underwent resection. Criteria for resectability were (1) the absence of peritoneal or liver metastases, (2) massive ingrowth into the contralateral branch of the portal vein or into the main stem, (3) infiltration of the main hepatic artery or its branch(es) to the contralateral liver segments, (4) atrophy of the contralateral liver lobe, (5) lymph node involvement outside the hepatic hilar region, and (6) extensive proximal ingrowth into the biliary radicals of the contralateral liver lobe, thus precluding a free margin for biliary anastomosis.

Patients were divided according to three 5-year periods: period 1 (1988–1993; n = 45), period 2 (1993–1998; n = 25), and period 3 (1998–2003; n = 29). Resections were performed in 61 men and 38 women with a mean age of 60 ± 1.1 years (range, 21–79 years). There was no significant difference in sex or age among the three different study periods.

Preoperative Work-Up and Imaging Studies
Preoperative work-up consisted of routine physical examination and laboratory analysis of liver function parameters. In period 1, the preoperative diagnostic approach consisted of (endoscopic) ultrasonography and endoscopic retrograde cholangiopancreatography (ERCP) with subsequent biliary drainage.22 Angiography was performed in two thirds of all patients, and percutaneous transhepatic cholangiography (PTC) was performed in seven patients. In period 2, ERCP and ultrasonography with Doppler imaging were still used routinely, but endoscopic ultrasonography was not performed anymore. PTC was performed in only one patient, and angiography was used in only three cases (12%). Diagnostic laparoscopy was performed in the last 19 patients (76%) as an additional means of tumor staging.23,24 In period 3, ERCP, transabdominal ultrasonography with Doppler imaging, and diagnostic laparoscopy were routinely performed, whereas PTC was used in five patients. Angiography was not performed anymore. It was gradually replaced by thin-sliced helical computed tomographic scan. Computed tomographic scan was used throughout the three periods in 42%, 48%, and 76% of the patients, respectively. As of the end of 2000, magnetic resonance cholangiopancreatography was performed to assess tumor extent in seven patients (7%) in total.

Preoperative Biliary Drainage
Preoperative biliary drainage was performed in 85 patients (86%). ERCP was applied in 72 (85%) patients by using 1 to 3 stents, PTC was used in 4 patients (5%), and in 8 patients (9%), both techniques were used. In periods 1, 2, and 3, the percentage of patients who underwent preoperative biliary drainage was 82%, 96%, and 83%, respectively. The mean values of total bilirubin after biliary drainage in the three periods were 123 ± 24 µmol/L, 48 ± 11 µmol/L, and 18 ± 11 µmol/L, respectively (P < .01).

Tumor Classification and Histopathologic Examination
The Bismuth-Corlette classification was used to define proximal tumor extension.25 During resection, tumor extension was verified, if necessary by histopathologic examination of frozen sections. The resection and dissection margins of the resected specimens, as well as perineural tissue and lymph nodes, were studied for tumor ingrowth. Also, tumor type and differentiation were assessed.

Adjuvant Therapy
From 1990, preoperative radiotherapy (3 x 3.5 Gy) was given to patients who had undergone endoscopic or percutaneous biliary drainage to prevent seeding of tumor cells into the drainage tract.26 Patients underwent adjuvant postoperative radiotherapy (55 Gy) on a routine basis during all three periods.27

Statistical Analysis
The {chi}2 test (Pearson or the Fisher’s exact test) was used to assess the differences between periods. Numeric data were evaluated by using one-way analysis of variance and were expressed as mean ± SEM. The Kaplan-Meier method was used to construct survival curves, and the log-rank significance test was used for comparison of survival between groups. Multivariate analysis was performed by using logistic regression and the Cox proportional hazards model. SPSS 10.0.7 for Windows (SPSS Inc., Chicago, IL) was used as statistical software, and a P value <.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Surgical Procedures
In period 1, local resection was performed in 41 patients (91%; Table 1Go). Local resections included excision of the tumor with intention to obtain adequate macroscopic margins. This sometimes required partial resection of segments 1 and 4. Only 4 (24%) of 17 patients with type III or IV tumors underwent a hilar resection in combination with a partial liver resection (Table 1Go). Sixteen patients (36%) underwent R2 resection to achieve adequate biliary drainage for palliation. In period 2, 13 (81%) of 16 patients with type III tumors underwent hilar resection in combination with partial hepatectomy (6 with extended hemihepatectomy). Portal vein reconstruction was performed in one patient. Five patients (20%) underwent R2 resection for palliation. In period 3, 21 (95%) hemihepatectomies were performed (including 7 extended hemihepatectomies) in 22 patients with type III or IV tumors. From 1999, total resection of the caudate lobe was performed in 15 (71%) of 21 patients in addition to partial liver resection. In six patients (6%) portal vein reconstruction was performed, and in one patient (1%) local resection was combined with pancreatoduodenectomy.


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  		TABLE 1. Bismuth-Corlette classification and resection types according to resection period
 
Morbidity and Mortality
Overall postoperative morbidity occurred in 66% of the patients (postoperative complications could not be retrieved in two patients; Table 2Go). No significant differences were found in postoperative complications among the three time periods. The most frequent complications were bile leakage (25%) and liver or intra-abdominal abscesses (24%; Table 3Go). Complications categorized as miscellaneous consisted of pleural effusion, pulmonary emboli, cardiac failure, myocardial infarction, wound infection, urinary tract infection, renal failure, intestinal obstruction, pancreatic fluid leakage, cerebral infarction, and delirium. A total of 22 patients (22%) had to undergo reoperation because of bile leakage and/or intra-abdominal abscesses or bleeding.


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  		TABLE 2. Hospital morbidity and mortality according to resection period
 

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  		TABLE 3. Postoperative complications according to resection period
 
The hospital mortality rate was 20%, 12%, and 10% for the periods 1, 2, and 3, respectively (overall 15.2% [15 of 99]; Table 2Go). No significant differences were found in mortality among the time periods. All patients died of multiorgan failure. In 9 of 15 patients, multiorgan failure was preceded by massive intra-abdominal or upper gastrointestinal bleeding, combined with liver failure (n = 5) or sepsis (n = 4). Multiorgan failure was preceded by liver failure/necrosis together with sepsis in 5 of 15 patients. In one patient, the cause of death was not specified.

Factors associated with increased morbidity in univariate analysis were Klatskin type IIIa, (extended) right hemihepatectomy, and portal vein resection (Table 4Go). No factors were found to correlate with increased mortality. No independent factors associated with morbidity or mortality were found in multivariate analysis (data not shown).


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  		TABLE 4. Risk factors correlated with postoperative morbidity and mortality
 
Tumor Classification and Histopathologic Examination
In periods 1 to 3, the definitive intraoperative staging differed from preoperative staging of tumor extension in 20 (44%), 5 (20%), and 4 (14%) patients, respectively (P < .02). Intraoperative tumor classifications according to resection period are listed in Table 1Go. A significantly larger percentage of well-differentiated tumors was found in period 3 as compared with period 1 (36% vs. 5%; Table 5Go). The incidence of lymph node involvement decreased significantly from 49% in period 1 to 14% and 4% in periods 2 and 3, respectively. The proportion of R0 resections increased significantly from 13% and 32% in periods 1 and 2, respectively, to 59% in period 3. Factors associated with an increased rate of R0 resections in univariate analysis were resection period, resection type, and total resection of the caudate lobe (Table 6Go). In multivariate analysis, the only independent factor associated with R0 resection was the treatment period (Table 7Go).


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  		TABLE 5. Histological characteristics according to resection period
 

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  		TABLE 6. Univariate analysis of variables associated with R0 resections
 

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  		TABLE 7. Multivariate analysis of factors associated with R0 resection
 
Survival
The overall survival rate was 70% after 1 year, 37% after 3 years, 27% after 5 years, and 12% after 10 years. The 5-year survival of R0 or R1 resections was 33% (median survival, 27.0 ± 7.8 months) and was 0% for R2 resections (median survival, 16.7 ± 2.0 months). The 2-year survival of R0 and R1 resections increased significantly from 33.3% ± 7.0% and 39.1% ± 10.2% in periods 1 and 2, respectively, to 60.0% ± 11.4% in period 3 (Figure 1Go). A trend was found toward an increased median survival time of R0 resections (38.8 ± 11.6 months) as compared with R1 resections (22.6 ± 10.0 months). In univariate analysis, R2 resections were associated with a worse survival compared with R0 or R1 resections (Table 8Go). In univariate analysis of R0 and R1 resections, resection period and lymph node involvement were found to be significantly related to survival time. Survival of patients with R0 resections did not differ significantly from survival of patients with R1 resections. No independent factor was found to be related to survival time in multivariate analysis (data not shown). A total of 21 patients were still alive at the end of the study period, of which 4 underwent operation in the period 1993 to 1998 and 17 in the period 1998 to 2003.


Figure 1
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  		FIG. 1. Kaplan-Meier survival curves of R0 and R1 resections according to the resection period. A significantly increased 2-year survival was found in the period 1998 to 2003 as compared with the other time periods (P < .05).

 

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  		TABLE 8. Univariate analysis of variables associated with survival
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Survival after surgical treatment of hilar cholangiocarcinoma has improved during the last 10 to 15 years.11,22 This, without doubt, owes to the fact that more resections have been combined with partial hepatectomy, thus leading to more R0 resections.2,13–18 Also in this study, the 2-year survival significantly increased during the 15-year period, whereas the number of R0 resections increased from 13% in the first period to 59% in the last period (P < .05). A combination of factors, such as improved imaging techniques and patient selection, but, foremost, the adoption of a more aggressive Japanese-based surgical technique, have all contributed to the increase in the proportion of margin-negative resections in the third period. Of R0 resections performed in 1998 to 2003, 77% represented hilar resections in combination with partial liver resections. In contrast to several reports in literature, no significant difference was found in survival time between patients with R0 and R1 resections in this study. The reason for this is that of all patients with R0 resections, 47.8% were alive at the completion of this study, compared with 16.7% in the R1 resection group. Most R0 resections occurred in the last time period (17 of 31 patients). Of these 17 patients, 12 (70.6%) were alive at the completion of the study. Therefore, it is likely that the mean survival of patients with R0 resection is underestimated and will probably increase more rapidly than the mean survival of patients with R1 resections.

The 5-year survival rate of 33% with a median survival of 27.0 months for patients treated with curative intent (R0 + R1) is comparable to the results of other recent studies from Western (European and American) and Japanese centers.15,16,28–30 The median survival of patients with R0 resection was 38.8 months in this study. This survival will probably increase in time, because 11 of 31 patients with R0 resection were alive at the completion of this study. In the literature, the median survival of R0-resected patients is reported up to 50 months.15 The median survival and 5-year survival rates could not be calculated in the period 1998 to 2003 because more than half of patients were still alive at the completion of this study. Therefore, no definitive conclusions can be drawn from the survival data of this period. However, 2-year survival rates increased from 41% in the first period to 45% in the second period and 59% in the third period.

A significant correlation was found between the absence of lymph node metastases and an increased median survival. This is in accordance with what can be found in the literature.14,15 Therefore, mainly in the last two periods, lymph nodes in the hepatoduodenal ligament and the peripancreatic and retroperitoneal lymph nodes were carefully checked for tumor invasion by frozen-section examinations during surgery. When lymph node invasion was found outside the hilar region, resection was canceled. This probably led to a decreased proportion of patients with lymph node metastases in the resected specimen along the three time periods. Lymph node metastases were present in only 4% of patients in the last time period. Tumour differentiation and perineural invasion did not have a significant relationship to survival time in this study.

An overall postoperative morbidity rate of 66% found in this study is comparable to recent studies with postoperative morbidity rates of 37% to 85%.15,16,20 Comparing recent and older (>5 years old) literature, a slight increase in postoperative morbidity can be observed along with a more aggressive surgical approach.8,18–20 In this study, the percentage of hilar resections in combination with partial hepatectomy increased from 9% in 1988 to 1993 to 52% in 1993 to 1998 and 72% in 1998 to 2003 (P < .01), whereas postoperative morbidity and mortality did not increase significantly.

Sewnath et al.31 concluded in a recent meta-analysis that the question of whether preoperative biliary drainage in patients with biliary obstruction can decrease postoperative morbidity cannot be answered yet because of a lack of controlled studies. Although the discussion on the benefit of preoperative biliary drainage is still ongoing, we consider optimal pre-operative drainage a prerequisite in this category of patients who will undergo major liver resections and rely heavily on functional reserve of the remnant liver after surgery.

In recent literature, overall in-hospital mortality rates vary from 0% to 10%.15,16,21,32–34 In our series, mortality decreased from 20.0% in 1988 to 1993 to 10.3% in 1998 to 2003, probably because of better patient selection and increased surgical experience, despite the increased proportion of extended resections, which carry a higher risk. Most postoperative mortality was due to liver failure, which was caused by a combination of factors such as the extent of resection, infection, and bile leakage.

Adjuvant radiotherapy was applied routinely in our institution as of 1986. The rationale for adjuvant radiotherapy was addressed in a previous article from our department.27 In the latter, retrospective study, we found a survival benefit for patients undergoing adjuvant radiotherapy. There are, however, no properly conducted trials that provide evidence for a benefit of adjuvant radiotherapy. Because of the lack of evidence, adjuvant radiotherapy is presently not applied anymore in our institution in these patients.

In the future, a decrease of postoperative complications and in-hospital mortality will need special emphasis. One of the ways to accomplish this is by careful preoperative assessment of remnant liver function. With this information, patients who are at risk of developing postoperative liver failure can be identified, and, by using techniques such as portal vein embolization, future remnant liver function can be improved.35 In conclusion, the results of resection of hilar cholangiocarcinoma were evaluated in this study relative to a 15-year time period. Mainly in the last 5-year period (1998–2003), when the Japanese surgical approach was followed, more hilar resections were combined with partial liver resections that included segments 1 and 4, thus leading to more R0 resections. This, together with more adequate patient selection and a decrease in N1 patients, resulted in improved survival while not significantly affecting postoperative morbidity or mortality.


   ACKNOWLEDGMENTS
 
The authors thank Professor Y. Nimura (Division of Surgical Oncology, Nagoya University Hospital) for his collaboration during the last 5 years. They also thank Professor H. Obertop (Department of Surgery, Academic Medical Center) for his contributions to this study.

Received for publication June 22, 2005. Accepted for publication December 1, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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