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Annals of Surgical Oncology 9:430-438 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Significance of Hepatic Pedicle Lymph Node Involvement in Patients With Colorectal Liver Metastases: A Prospective Study

Daniel Jaeck, MD, PhD, Hiroshi Nakano, MD, PhD, Philippe Bachellier, MD, Keiichiro Inoue, MD, Jean-Christophe Weber, MD, Elie Oussoultzoglou, MD, Philippe Wolf, MD, PhD and Marie-Pierre Chenard-Neu, MD, PhD

From Centre de Chirurgie Viscérale et de Transplantation (DJ, HN, PB, KI, J-CW, EO, PW) and Service d’Anatomie Pathologique (M-PC-N), Hôpital de Hautepierre, Strasbourg, France.

Correspondence: Address correspondence and reprint requests to: Daniel Jaeck, MD, PhD, Centre de Chirurgie Viscérale et de Transplantation, Hôpital de Hautepierre, Avenue Molière, 67098 Strasbourg Cedex, France; Fax: 33-3-88-12-72-86; E-mail: daniel.jaeck{at}chru-strasbourg.fr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: We investigated whether hepatic pedicle lymph node (HP-LN) involvement is a more significant prognostic factor and whether HP-LN dissection could be efficient in patients with positive HP-LN involvement.

Methods: From 1988 to 1998, HP-LN dissection was prospectively performed in 160 patients undergoing hepatectomy for colorectal liver metastases. Survival of patients with HP-LN involvement limited to the hepatoduodenal ligament and retropancreatic portion (area 1) was compared with that of patients with HP-LN involvement spreading over the common hepatic artery and celiac axis (area 2).

Results: HP-LN involvement was detected in 17 patients. The survival rate was significantly lower in patients with HP-LN involvement. HP-LN involvement was the most significant prognostic factor. Survival was significantly higher in patients with HP-LN involvement limited to area 1 than in those with HP-LN involvement spreading over area 2.

Conclusions: HP-LN involvement was the most significant prognostic indicator in patients with colorectal liver metastases. Positive LNs of area 1 should no longer be considered an absolute contraindication to liver resection, but in case of area 2 lymph node involvement, liver resection does not seem justified.

Key Words: Hepatic pedicle lymph node involvement • Colorectal liver metastasis • Hepatic resection • Prognostic factors


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Hepatic resection has been accepted as the best way to offer long-term survival in patients with colorectal liver metastases, and several reports showed satisfactory 5-year survival rates ranging from 20% to 54% after hepatectomy.1–14 In addition, a multimodality treatment using radiofrequency or cryotherapy ablation has been increasing the indication for conventionally unresectable liver metastases.15–17 Recent articles also showed that neoadjuvant chemotherapy followed by resection can be efficient for initially unresectable colorectal liver metastases.18,19

Among prognostic factors analyzed after hepatectomy, Fong et al.20 recently reported that positive tumor margin, extrahepatic disease, node-positive primary tumor, disease-free interval from primary tumor to liver metastases, number and diameter of metastases, and carcinoembryonic antigen level were significant prognostic factors in an analysis of 1001 consecutive patients with colorectal liver metastases. However, they did not show data concerning involvement of hepatic pedicle lymph nodes (HP-LNs). Iwatsuki et al.11 recently reported that the presence of HP-LN involvement was one of the significant prognostic factors in 305 patients. Several other articles have focused on HP-LN involvement.21–29 They concluded that the positive involvement of HP-LNs predicts extremely poor survival and is usually considered a contraindication for hepatectomy in patients with colorectal liver metastases.11,21–24,26,27,29 Therefore, whether or not HP-LN dissection benefits patients with positive involvement of HP-LNs has yet to be confirmed. A French multi-institutional prospective study, in which we took part, subclassified HP-LNs into six main groups and reported a 14% incidence of HP-LN involvement in patients with colorectal liver metastases.24 However, this study did not show which group of HP-LN involvement predicts patient survival. The aim of this study was to investigate whether HP-LN involvement is a significant prognostic factor and, more precisely, which type of HP-LN involvement may be of higher prognostic value. Therefore, we classified patients with positive HP-LN involvement into two groups according to the area involved, and their survival rates were compared.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
From April 1988 to December 1998, 221 consecutive patients with colorectal liver metastases underwent a first hepatectomy for the intent of curative treatment of colorectal liver metastases in our institution. HP-LN dissection was prospectively performed from October 1993 until December 1998. During this period, 174 patients underwent hepatectomy for colorectal liver metastases, and among them, 160 were included in this study, according to the following criteria: (1) first hepatectomy; (2) age <75 years; (3) absence of severe cardiovascular, pulmonary, or other associated diseases; (4) absence of other malignant disease; (5) absence of distant metastases secondary to colorectal cancer other than liver metastases (except a solitary peritoneal tumor that could be completely resected during hepatectomy); and (6) complete resection of liver metastases confirmed during surgery. All patients undergoing curative liver resection during the study period for colorectal liver metastases were evaluated and included in this study, provided they fulfilled the above-mentioned criteria. The primary colorectal carcinoma was curatively resected between 1988 and 1998 in these 160 patients. The mean interval between colorectal resection and hepatectomy was 2.2 years. The number and location of liver metastases were preoperatively defined by ultrasonography, computed tomography, magnetic resonance imaging, or a combination of these. Intraoperative ultrasonography was routinely performed in all 160 patients to find additional occult metastases and to determine the sufficient margin of excision. The site of the primary tumor was routinely explored before and during surgery.

According to a previous multicentric study,24 six subgroups of LNs were identified during HP-LN dissection (Fig. 1). In all 160 patients, we performed a lymphadenectomy of the hepatoduodenal ligament and retropancreatic portion, as well as around the common hepatic artery and celiac axis. A systematic wide LN clearance was performed, arbitrarily separating the LNs into six main groups (Fig. 1): (1) pedicular antero superior, (2) pedicular antero inferior, (3) pedicular postero superior, (4) pedicular postero inferior, (5) along and behind the transverse part of the hepatic artery, and (6) at the origin of the hepatic artery, around the celiac trunk. The procedure began with cholecystectomy, and a virtual line, passing transversely at the level where the cystic duct had been divided, allowed arbitrary separation between the superior and the inferior LN groups of the hepatoduodenal ligament. Retropancreatic LNs, behind the head of the pancreas, were allocated to the pedicular postero inferior group. To evaluate the prognostic significance of HP-LN involvement, we defined two areas (Fig. 2). The proximal area 1 included groups 1 to 4, and the distal area 2 included groups 5 and 6.



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  		FIG. 1. Hepatic pedicle lymph node (HP-LN) dissection according to the protocol of the prospective multicentric study.24 This figure shows the topography of the six main groups of lymph nodes removed (HA, hepatic artery; CA, celiac axis; BD, common bile duct).

 


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  		FIG. 2. Hepatic pedicle lymph nodes (HP-LN) were classified into two groups: area 1, lymph nodes of the hepatoduodenal ligament (HD) and retropancreatic portion (RP); and area 2, nodes around the common hepatic artery (HA) and celiac axis (CA).

 
Intraoperative and postoperative histopathologic examinations of the LNs were performed in all 160 patients undergoing HP-LN dissection. Only histopathological metastatic involvement of HP-LNs was defined as positive. Histopathological examination of the liver metastases was also performed to obtain the greatest diameter of liver tumor size, histological differentiation, type of tumor progression, and existence of pseudocapsule of tumor. It also assessed the safety margin.

Patient survival was investigated in September 1999. All mean values were expressed with SEM. Mann-Whitney U-tests and {chi}2 tests were used as appropriate. Cumulative survival was calculated with the Kaplan-Meier method, and differences were analyzed with the log-rank test. When univariately significant prognostic factors were found with the log-rank test, a multivariate analysis was performed according to Cox’s proportional hazard test. A difference was considered significant when P < .05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The mean age of the 160 patients at hepatectomy was 60.6 years (range, 29 to 75 years), and the male:female ratio was 94:66. Sixty-five patients had a solitary metastasis, and 95 patients had multiple liver metastases: two metastases (n = 31), three metastases (n = 25), four metastases (n = 13), and five or more metastases (n = 26). One hundred patients had unilobar metastases, and 60 had bilobar disease. A simultaneous resectable peritoneal solitary tumor was detected and resected with curative intent in 20 patients (Table 1). Fifty-four patients had synchronous lesions, and 106 had metachronous lesions. Simultaneous hepatectomy combined with colorectal resection was performed in 20 patients, and hepatectomy was postponed to a second stage in 34 patients with synchronous metastases.


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  		TABLE 1. Characteristics of the 20 patients presenting with extrahepatic solitary peritoneal deposits
 
Major hepatectomies—including extended right or left hepatectomy (n = 10), right hepatectomy (n = 18), and left hepatectomy (n = 27)—were performed in 55 patients. The other 105 patients underwent minor hepatectomy, including bisegmentectomy according to Couinaud’s classification (n = 60), segmentectomy (n = 32), and nonanatomical resection (n = 13).

Seventeen patients (10.6%) had positive HP-LN involvement among the 160 patients. There was no operative death, including during the month after the surgical procedure, in this group of 160 patients. The morbidity rate was 33% among the 160 patients who underwent lymphadenectomy and was 38% among the 61 patients who did not. No specific complications were observed after lymphadenectomy. The mean hospital stay was 17 days in the former group and 16 days in the latter group. Thirty of 160 patients underwent repeat hepatectomies during the study period. One hundred thirteen patients were alive, and 47 died of progression of recurrent diseases. Overall 1-, 3-, and 5-year survival rates after hepatectomy in the 160 patients were 85%, 56%, and 42%, respectively. The median survival was 3.4 years.

Univariate Analysis of Clinicopathological Factors in the 160 Patients
Univariate analysis of survival showed that synchronous metastases, bilobar lesions, four or more metastatic nodules, positive HP-LN involvement, and resectable solitary peritoneal tumor significantly predicted shorter survival in the 160 patients who underwent HP-LN dissection (Table 2).


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  		TABLE 2. Univariate analyses of survival in 160 patients undergoing dissection of hepatic pedicle lymph nodes (HP-LNs)
 
Univariate Analysis of Positive HP-LN Involvement
Among the 17 patients with positive involvement of HP-LN, 13 died within 1 year after hepatectomy. Four patients (23.5%) were still alive, and two of them were alive more than 3 years after hepatectomy. Retroperitoneal, mesenteric, and para-aortic LN metastases were not found in the 17 patients during hepatectomy. The survival rate was significantly lower in patients with HP-LN involvement than in those without involvement (3-year survival rate, 19% vs. 62%; P < .0001; Fig. 3). In the comparison of clinicopathologic characteristics between patients with and without HP-LN involvement, more than three metastases; metastases located at segment 4, segment 5, or both; existence of a resectable peritoneal tumor; and poorly differentiated adenocarcinoma of liver metastases were found to be significantly associated with positive HP-LN involvement (Table 3).



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  		FIG. 3. Survival after hepatectomy in patients with positive involvement of hepatic pedicle lymph nodes (HP-LNs) (n = 17, dashed line; 3-year survival, 19%) and that in patients without HP-LN involvement (n = 143, solid line; 3-year survival, 62%). P < .0001.

 

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  		TABLE 3. Factors with significant differences between patients with or without involvement of hepatic pedicle lymph nodes (HP-LNs)
 
Localization of metastatic LNs and liver tumors and the number of metastatic LNs of the 17 patients with HP-LN involvement are listed in Table 4. Forty LN metastases among 127 dissected LNs were found in the 17 patients. HP-LN involvement limited to area 1 was found in eight patients, and HP-LN involvement spreading over area 2 was found in nine patients (Table 4).


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  		TABLE 4. Comparison between patients with involvement of hepatic pedicle lymph nodes (HP-LNs) limited to area 1 LNs and those spreading to area 2 LNs
 
No patient with area 2 involvement survived longer than 1 year after hepatectomy, whereas two patients with area 1 involvement were still alive 3 years after hepatectomy. The survival rate was significantly higher in patients in whom HP-LN involvement was limited to area 1 than in patients with area 2 metastases (3-year survival, 38% vs. 0%; P < .001; Fig. 4).



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  		FIG. 4. Survival after hepatectomy in patients with involvement of hepatic pedicle lymph nodes limited to area 1 (n = 8, solid line; 3-year survival, 38%) and that in patients with involvement of area 2 (n = 9, dashed line; 1-year survival, 0%). P < .001.

 
Multivariate Analysis of Prognostic Factors in the 160 Patients
The Cox’s proportional hazard test showed that HP-LN involvement, existence of resectable solitary peritoneal tumor, four or more metastatic nodules, and synchronous metastases significantly predicted poorer survival (Table 5). The relative risk of HP-LN involvement was the highest among the all significant prognostic factors.


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  		TABLE 5. Factors predictive of survival (multivariate analysis)
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
This study showed that the presence of HP-LN involvement is the most significant prognostic indicator after hepatectomy in patients with colorectal liver metastases. More than three metastases; metastases of segment 4, segment 5, or both; a resectable solitary peritoneal tumor; and poorly differentiated adenocarcinoma of liver metastases were significantly more frequently associated with positive HP-LN involvement. Because the survival rate in patients with positive HP-LN involvement limited to area 1 was of 38% at 3 years, HP-LN involvement in area 1 should not be considered an absolute contraindication for resection of colorectal liver metastases.

HP-LN involvement has not been considered as lymphatic metastasis of colorectal primary but recognized as remetastasis of liver secondaries.30 Indeed, the patients with positive HP-LN involvement do not have metastases of mesenteric or retroperitoneal LNs, as shown in this study. The significant correlation between the tumoral location at segment 4 or 5 and HP-LN involvement may also suggest this assumption.

Several lymphatic pathways from the liver have been proposed: (1) lymphatic drainage through the hepatic hilum and retropancreatic portion, and that along the hepatic artery and celiac axis; (2) along the falciform ligament, diaphragm, and mediastinum; (3) through the esophageal hiatus, caval foramen, and mediastinum; (4) through the lesser omentum and upper gastric portion; and (5) along the phrenic artery and celiac axis.30 Among the several lymphatic pathways from the liver, this study suggests that lymphatic drainage through the hepatic hilum and retropancreatic portion and along the hepatic artery is more relevant to the prognosis of patients with colorectal liver metastases. Indeed, there was no 1-year survivor in patients with area 2 involvement. This finding has to be confirmed by further studies; however, it suggests that in case of high risk of HP-LN involvement, sampling of LNs in area 2 seems justified. If positive nodes are found, it seems that liver resection cannot offer longer survival.

The prevalence of HP-LN involvement in patients with colorectal liver metastases has been reported to range from 3% to 33% (Table 6). 11,21–29 Beckurts et al.26 reported a much higher incidence (28%) than this study (10.6%) in a large series in which positive involvement of HP-LNs was shown in 35 of 126 patients. However, the mean value of the incidence of HP-LN involvement in the 10 main reported series in the literature and listed in Table 6 is 9.6% (206 of 2155), which is similar to our own result (11%).


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  		TABLE 6. Prevalence of involvement of hepatic pedicle lymph nodes (HP-LNs) and correlation with survival
 
A French multicentric prospective study, including our group, reported which factors were associated with HP-LN involvement.24 The study showed that carcinoembryonic antigen level, number of metastases, extent of liver involvement, and major hepatectomy were significantly more frequently associated with HP-LN involvement. Kokudo et al.29 reported that liver metastases in the right lobe were associated with nodal involvement of the hepatoduodenal ligament, whereas metastases in the left lobe caused nodal involvement around the common hepatic artery. Our results more clearly indicate that more than three metastases, metastases of segment 4 or 5, the existence of a solitary peritoneal deposit, and poorly differentiated adenocarcinoma of liver metastases were the significant risk factors for positive HP-LN involvement.

The French multicentric prospective study, including our group, also reported the prevalence of HP-LN metastases in different divisions of HP-LNs, e.g., the incidence of pedicular LNs and that of nodes around the common hepatic artery.24 However, no study has investigated the relationship between survival and different divisions of HP-LN involvement. This study suggests that area 1 involvement should not be considered as a contraindication for liver resection. Whether lymphadenectomy should be routinely performed during colorectal liver metastases resection is an important issue; the answer could only be found by a prospective randomized trial comparing both strategies (with or without lymphadenectomy). Our study also showed an extremely poor prognosis in patients with area 2 involvement.

The prognostic significance of HP-LN involvement has been examined by several authors (Table 6)11,21–29 and was also the subject of a systematic review.31 In the largest retrospective multicentric study available,27 the 5-year survival rate was 12% in patients with metastatic involvement of HP-LNs. Nakamura et al.28,32 also reported some 5-year survivors in patients with positive HP-LN involvement. However, almost all authors reported that the 5-year survival rate was 0% in these patients.11,21–23,25,26,29 In addition, 3-year survival was reported to range from 0% to 12% (Table 6).11,23,26,27,29 These extremely poor survival rates may lead to the conclusion that resection of liver metastases is contraindicated in patients with positive HP-LN involvement.11,21–24,26,29,32,33 However, this study showed that HP-LN involvement limited to area 1 may still be an indication for hepatectomy. Indeed, the 3-year survival of these patients was 38%. However, our results also suggest that resection of liver metastases is questionable when area 2 involvement is confirmed during surgery. Indeed, there was no survivor after 1 year among patients with area 2 involvement.

Whether or not to routinely perform HP-LN dissection remains controversial, and whether HP-LN dissection can improve survival is also debatable. Yasui and Kato25 reported that obstructive jaundice after hepatectomy induced with recurrent involvement of HP-LNs was reduced in patients undergoing HP-LN dissection compared with those not undergoing HP-LN dissection. Beckurts et al.26 showed that survival during the 15 months after hepatectomy in patients with HP-LN involvement was equivalent to that in patients without HP-LN involvement. In addition, the survival of patients with area 1 involvement after HP-LN dissection was 38% at 3 years. These results suggest that HP-LN dissection may benefit patients with positive HP-LN involvement; however, only a randomized trial could answer this question.

However, some adverse effects of HP-LN dissection may be observed, such as severe adhesions at the time of possible repeat hepatectomy. Recurrent hepatic tumors will develop in more than half of patients with colorectal liver metastases,33,34 and the surgical outcome of repeat hepatic resection has been shown to be satisfactory.35,36 The 5-year survival rate after repeat hepatectomy is similar to that reported after the first resection. In addition, lymphatic leak after HP-LN may extend the hospital stay. However, our results suggest the need for histological control of HP-LNs, at least in the following circumstances: (1) presence of three or more metastatic liver tumors, (2) poorly differentiated adenocarcinoma of the liver, (3) presence of a resectable solitary peritoneal deposit, and (4) localization of liver metastases in segment 4 or 5.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
In conclusion, the involvement of HP-LNs seems to be one of the most significant prognostic indicators in patients with colorectal liver metastases. Sampling and intraoperative histological control of HP-LNs during surgery for colorectal liver metastases seems justified, at least in patients who are at high risk of HP-LN involvement, i.e., those who present with more than three metastases, metastases of segment 4 or 5, a resectable solitary peritoneal deposit, or a poorly differentiated carcinoma of liver metastases. The presence of positive LNs limited to area 1 does not seem to contraindicate resection of liver metastases. However, in case of involvement of area 2, liver resection does not seem justified. Whether or not lymphadenectomy of the hepatic pedicle should be routinely performed is an important question, which can be answered only by a prospective randomized trial.

Received for publication July 9, 2001. Accepted for publication February 12, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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M. Minagawa, J. Yamamoto, T. Kosuge, Y. Matsuyama, S.-i. Miyagawa, and M. Makuuchi
Simplified Staging System for Predicting the Prognosis of Patients With Resectable Liver Metastasis: Development and Validation
Arch Surg, March 1, 2007; 142(3): 269 - 276.
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 Ann. Surg. Oncol.Home page
E. K. Abdalla, R. Adam, A. J. Bilchik, D. Jaeck, J.-N. Vauthey, and D. Mahvi
Improving Resectability of Hepatic Colorectal Metastases: Expert Consensus Statement
Ann. Surg. Oncol., October 1, 2006; 13(10): 1271 - 1280.
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 Ann. Surg. Oncol.Home page
R. B. Adams, D. G. Haller, and M. S. Roh
Improving Resectability of Hepatic Colorectal Metastases: Expert Consensus Statement By Abdalla et al.
Ann. Surg. Oncol., October 1, 2006; 13(10): 1281 - 1283.
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 JCOHome page
V. P. Khatri, N. J. Petrelli, and J. Belghiti
Extending the Frontiers of Surgical Therapy for Hepatic Colorectal Metastases: Is There a Limit?
J. Clin. Oncol., November 20, 2005; 23(33): 8490 - 8499.
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D. Jaeck
The Significance of Hepatic Pedicle Lymph Nodes Metastases in Surgical Management of Colorectal Liver Metastases and of Other Liver Malignancies
Ann. Surg. Oncol., November 1, 2003; 10(9): 1007 - 1011.
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M. S. Roh
Should a Potentially Noncurative Resection that Prolongs Survival be Offered to Patients With Colorectal Liver Metastases?
Ann. Surg. Oncol., June 1, 2002; 9(5): 423 - 424.
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