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Original Article |

A Second Liver Resection Due to Recurrent Colorectal Liver Metastases FREE

Antonio Sa Cunha, MD; Christophe Laurent, MD; Alexandre Rault, MD; Philippe Couderc, MD; Eric Rullier, MD; Jean Saric, MD
[+] Author Affiliations

Author Affiliations: Department of Digestive Surgery, University Hospital of Bordeaux, Bordeaux, France.


Arch Surg. 2007;142(12):1144-1149. doi:10.1001/archsurg.142.12.1144.
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Published online

Background  Repeat liver resection because of recurrent colorectal liver metastases can provide survival benefit with a low rate of complications.

Design  Retrospective study.

Participants  Forty patients who underwent a second hepatectomy because of liver metastases from colorectal cancer.

Main Outcome Measures  Short- and long-term results of a second hepatectomy and determination of prognostic factors.

Results  The postoperative mortality rate was 2.5%. The postoperative morbidity rate was not significantly different after a second hepatectomy compared with single hepatectomy (42.5% and 27.5%, respectively; P = .10). Transfusion requirement and hospital stay were comparable for both a single and a second hepatectomy. Three- and 5-year overall survival rates were 55% and 31%, respectively. Disease-free survival rates at 3 and 5 years were, respectively, 49% and 27%. The interval between first and second hepatectomies and the presence of extrahepatic disease were independently related to survival (multivariate analysis).

Conclusions  A second liver resection because of recurrent liver metastases from colorectal cancer is safe and provides a survival benefit similar to that with single hepatectomy. Our analysis suggests that the benefit of treatment is limited in patients who undergo a second hepatectomy within 1 year of the first operation and in those with extrahepatic disease.

Figures in this Article

Hepatic resection is well accepted as the only curative treatment for colorectal liver metastases, offering 5-year survival of 25% to 58%.16 However, two-thirds of patients experience recurrence. Of these, only one-third will have recurrent metastases limited to the liver.2,4 As improvements in surgical techniques and perioperative management have enabled the reduction in mortality and morbidity associated with liver surgery, the rate of a repeat hepatectomy has increased in the last years.722 The development of percutaneous radiofrequency ablation and the increased efficacy of systemic chemotherapy regimens should lead us to evaluate the results and the role of a repeat hepatectomy. We performed a retrospective analysis of a 15-year experience with hepatic resection of colorectal metastases to assess the feasibility, morbidity, and survival benefits in patients undergoing a second hepatectomy and to determine prognostic factors.

We report the single-center experience of a second liver resection because of recurrent liver metastases at Saint André Hospital, Bordeaux, France. Patients were identified by a computer-based indexing system, and hospital medical records were retrospectively reviewed. Data analyzed included demographic information, pathologic features of primary and metastatic disease, surgical and adjuvant treatment of primary and metastatic disease, and predictors of outcome and survival. All patients who underwent a second resection of hepatic metastases were enrolled in the study.

SELECTION OF PATIENTS

Our criteria for a second hepatectomy were similar to those for first hepatectomy. Repeat hepatectomy was considered, in the absence of any medical contraindication to liver surgery, when the recurrent metastasis was technically resectable, preserving at least 30% of the liver parenchyma. Patients with extrahepatic disease (local recurrence, lung metastases, or both) that was resectable (R0 resection) were included. The preoperative evaluation included carcinoembryonic antigen; abdominal ultrasonography; computed tomography of the abdomen, pelvis, and thorax; and colonoscopy.

OPERATIVE PROCEDURE

The operative technique of liver resection in our unit has been described previously.23 At laparotomy, patients underwent surgical exploration via intraoperative ultrasonography and manual palpation to confirm the extent of the hepatic and extrahepatic disease. According to the anatomical classification of the liver by Couinaud,24 hepatectomy was considered major if 3 segments or more were removed.

FOLLOW-UP

Systematic postoperative follow-up included clinical examination, serum carcinoembryonic antigen assay, and abdominal ultrasonography every 3 months and chest radiographic examination and computed tomography every 6 months. Colonoscopy was performed at 1 and 3 years to exclude local recurrence of the primary tumor.

STATISTICAL ANALYSIS

A retrospective study of factors predictive of survival was performed including patient age and sex; site and stage of the colorectal tumor; disease-free interval between primitive tumor and the first hepatectomy; resection margin at the first hepatectomy; disease-free interval between first and second hepatectomies; presence of extrahepatic disease; number, size, and distribution of metastases; preoperative level of carcinoembryonic antigen; resection margin at the second hepatectomy; postoperative morbidity; and adjuvant chemotherapy. The overall survival was evaluated using the Kaplan-Meier method and included operative mortality. Univariate analysis was performed using the log-rank test. All variables associated with survival with P ≤ .20 at univariate analysis were considered for multivariate analysis using a Cox proportional hazards regression model. P < .05 was considered significant.

From January 1, 1985, to December 31, 2000, among 311 patients who underwent liver resection because of colorectal metastases, 140 (45%) developed liver metastases with or without extrahepatic recurrence. Fifty-six patients developed liver metastases with nonresectable extrahepatic recurrence, 38 patients had liver metastases not amenable to resection, and 6 patients had general contraindications to surgery. Thus, 40 patients (12.9%; 27 men and 13 women; mean age, 63 years [age range, 45-82 years]) were eligible for a second hepatectomy.

The primary carcinoma was located in the colon in 30 patients (75%) and in the rectum in 10 patients (25%). Cancer stage was T2 in 6 patients (15%), T3 in 34 patients (85%), N0 in 9 patients (22.5%), and N+ in 31 patients (77.5%). Liver metastases were synchronous in 18 patients (45%). The median interval between the colectomy and the first hepatectomy was 10 months (range, 0-34 months), and 70% of patients underwent hepatectomy within 1 year. At the time of the first hepatectomy, no patients had extrahepatic disease. The median interval between the first and the second hepatectomies was 15 months (range, 4-63 months) and was less than 1 year in 37.5% of patients. Adjuvant chemotherapy (intravenous fluorouracil with folinic acid, 5 days a month for 6 months) was given to 138 of 311 patients (44%) after resection of liver metastases. In the 40 patients who underwent a second hepatectomy, 27 (67.5%) received adjuvant chemotherapy after the first hepatectomy and 15 (37.5%) received adjuvant chemotherapy (intravenous fluorouracil with folinic acid, 5 days a month for 6 months) after the second hepatectomy (including 3 patients who also received chemotherapy before surgery).

Five patients (12.5%) had resectable extrahepatic disease: 3 locoregional recurrences that were resected during the same laparotomy and 2 pulmonary metastases that were resected after the second hepatectomy. All 5 patients underwent R0 resection of extrahepatic disease.

Characteristics of tumors in patients who underwent a single and those who underwent a second hepatectomy are given in Table 1. Solitary metastasis was present in 122 patients (40%) who underwent a single hepatectomy and in 21 patients (52.5%) at the second hepatectomy. The mean diameter of metastases was larger in the single hepatectomy group (44 ± 26 mm) than in the second hepatectomy group (36 ± 16 mm). One hundred ninety-four patients (62%) underwent major hepatectomy in the single hepatectomy group and 11 patients (27.5%) in the second hepatectomy group (P < .001). The percentage of R0 resections was not significantly different between the 2 groups: 98% in the single hepatectomy group and 87.5% in the second hepatectomy group.

Table Graphic Jump LocationTable 1. Tumor Data in Patients With Colorectal Liver Metastases Who Underwent a Single and a Second Hepatic Resection
OPERATIVE MORTALITY AND MORBIDITY

One patient (2.5%) died of peritonitis after the second hepatectomy. Transfusion of red blood cells was necessary in 49 patients (15%) in the single hepatectomy group and 6 patients (15%) in the second hepatectomy group ( = .91). Two patients underwent additional operations, 1 because of intestinal occlusion and 1 because of peritonitis that was the result of an intestinal perforation. The mean complication rate was higher but not significantly different after the second hepatectomy compared with the first hepatectomy (42.5% vs 30%) (Table 2). The mean (SD) hospital stay was not significantly different between the 2 groups (14 [10] vs 17 [8] days).

OVERALL AND DISEASE-FREE SURVIVAL

The 3- and 5-year overall survival rates after the second hepatectomy were 55% and 31%, respectively, with a median of 31.8 months. In comparison, overall survival in the 271 patients who underwent only 1 hepatectomy was 49% at 3 years and 34% at 5 years (Figure 1). After a median follow-up of 31 months (range, 9-87.6 months) after the second hepatectomy, 17 patients (42.5%) are alive, of whom 13 patients (32.5%) are disease free. Twenty-three patients (57.5%) died of disease recurrence. Ten patients are alive at 5 years, and 8 of these patients have had no disease recurrence. The 3- and 5-year disease-free survival rates were 49% and 27%, respectively. Twenty-seven patients developed recurrent disease: isolated liver metastases in 12 patients, hepatic and extrahepatic recurrence in 9 patients, isolated lung metastases in 3 patients, and other extrahepatic disease in 3 patients.

Place holder to copy figure label and caption
Figure 1.

Kaplan-Meier curves comparing survival after liver resection in patients who underwent a single liver resection and those who underwent a second hepatectomy.

Graphic Jump Location
PROGNOSTIC FACTORS AFTER REPEAT HEPATECTOMY

The results of univariate analysis of overall survival after the second hepatectomy are given in Table 3. Survival was significantly better in patients without extrahepatic disease, with an interval of more than 1 year between the first and second hepatectomies, and with R0 resection. Multivariate analysis revealed that only an interval of less than 1 year between the first and second hepatectomies (mean hazard ratio, 7.3 [95% confidence interval, 1.01-26.6]; P = .003, Cox proportional hazards regression model) and presence of extrahepatic disease (mean hazard ratio, 3.3 [95% confidence interval, 1.07-6]; P = .04, Cox proportional hazards regression model) were independent prognostic factors of poor survival (Figure 2 and Figure 3).

Table Graphic Jump LocationTable 3. Univariate Analysis of Prognostic Factors for Survival After a Second Liver Resection of Colorectal Liver Metastases
Place holder to copy figure label and caption
Figure 2.

Kaplan-Meier curves comparing survival after liver resection in patients with and without extrahepatic disease.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Kaplan-Meier curves comparing survival after liver resection according to interval between the first and second hepatectomies.

Graphic Jump Location

To our knowledge, our study is one of the largest single-center studies of repeat liver resection because of recurrent liver metastases (Table 4). Results of the present study show that a second hepatectomy can be performed safely and provides a 5-year survival rate of 31%. Factors associated with poor prognosis are an interval of less than 1 year between the first and second hepatectomies and the presence of extrahepatic disease.

Table Graphic Jump LocationTable 4. Summary of Large Series of Repeat Hepatectomy in Patients With Recurrent Liver Metastases

Owing to recent advances in hepatic surgery and survival benefits observed after liver resection because of colorectal metastases, the repeat hepatectomy rate has dramatically increased. In our study, 13% of patients who underwent liver resection because of colorectal metastases underwent a second operation, according to the results from specialized institutes.8,9,13,21

Repeat liver resection is associated with increased technical difficulties related to adhesions on the raw surface of the previous hepatectomy and consistency of the liver induced by regeneration. Therefore, some authors report increased morbidity and increased risk of bleeding.25,26 Despite a high incidence of major repeat hepatectomies in our study, morbidity was similar to that reported in the literature710,12,13,16,18,19,21,22 and not significantly different than after the first hepatectomy.710,12,13,16,18,19,21,22 In addition, the transfusion rate and hospital stay were not significantly different than those observed after the first hepatectomy. We conclude that a second hepatectomy, even major resection, can be performed safely.

Our policy is to always discuss the possibility of a second hepatectomy in patients with recurrence of liver cancer, using the same selection criteria as for a first hepatectomy. Repeat hepatectomy is associated with a 5-year survival rate (31%) similar to that observed after the first hepatectomy. In addition, 8 of our patients (20%) are alive without recurrence at 5 years.

The resectability rate of recurrent liver metastases is similar to that reported for the first liver metastases. This rate could be increased by associated radiofrequency ablation.27 Radiofrequency ablation was not used in the present study.

In our study, 2 variables were independently associated with overall survival after the second hepatectomy because of recurrent liver metastases: an interval of less than 1 year between the first and second hepatectomies and the presence of extrahepatic disease. As in the 3 other studies that identified independent prognostic factors by multivariate analysis,8,13,21 no tumor factor related to the primary tumor and the first hepatectomy was found in our study to be an independent prognostic factor related to the second hepatectomy.

Adjuvant chemotherapy after hepatic resection of colorectal metastasis has been advocated because of the substantial risk of tumor recurrence. In our study, survival in patients who underwent a second hepatectomy was not influenced by using adjuvant chemotherapy; nevertheless, fluorouracil with folinic acid was administered. The use of new drugs (irinotecan, oxiliplatin, and targeted therapies) and the response to preoperative chemotherapy, as shown by Adam et al,28 should improve results and aid in selection of patients who can benefit from a second hepatectomy.

In our study, only 5 patients (12.5%) underwent R1 liver resection; this rate is lower than those usually reported (17%-25%). This small number of R1 liver resections explains why we failed to show that residual tumor is an independent prognostic factor, as reported by others.8,13

In the present study, 3-year survival was dramatically decreased in the presence of extrahepatic disease and, therefore, is an independent prognostic factor, as after the first liver resection.29 The few patients with extrahepatic disease (2 patients with local recurrence and 3 patients with lung metastases) does not allow us to stratify free and overall survival by site of extrahepatic disease. Resection of liver and extrahepatic disease can lead to a 5-year survival of 20%.29 Therefore, we cannot conclude that the presence of extrahepatic disease must be considered a contraindication to a second hepatectomy. As also shown by Adam et al,8 the present study demonstrates that 5-year survival is significantly better if there is an interval of more than 1 year between the 2 hepatectomies compared with an interval of less than 1 year. These results may suggest that chemotherapy be given before surgery to enable observation of the evolution of the recurrent disease and to aid in the selection of patients who can benefit from a second hepatectomy.

In conclusion, a second hepatectomy is feasible, safe, and effective in selected patients with hepatic cancer recurrence after a first hepatectomy. In patients without extrahepatic disease and with an interval of more than 1 year between hepatectomies, 5-year survival is similar to that obtained after the first hepatectomy. Repeat hepatectomy can offer prolonged survival and is the only treatment with potential for cure.

Correspondence: Antonio Sa Cunha, MD, Department of Digestive Surgery, University Hospital of Bordeaux, Ave de Magellan, Pessac 33604, Bordeaux, France.

Accepted for Publication: May 26, 2006.

Author Contributions:Study concept and design: Sa Cunha, Laurent, Rullier, and Saric. Acquisition of data: Sa Cunha and Couderc. Analysis and interpretation of data: Sa Cunha and Saric. Drafting of the manuscript: Sa Cunha and Couderc. Critical revision of the manuscript for important intellectual content: Sa Cunha, Laurent, Rullier, and Saric. Statistical analysis: Sa Cunha. Study supervision: Sa Cunha and Saric.

Financial Disclosure: None reported.

Hughes  KSSimon  RSonghorabodi  S  et al.  Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery 1986;100 (2) 278- 284
PubMed
Nordlinger  BGuiguet  MVaillant  JC  et al. Association Francaise de Chirurgie, Surgical resection of colorectal carcinoma metastases to the liver: a prognostic scoring system to improve case selection, based on 1568 patients. Cancer 1996;77 (7) 1254- 1262
PubMed
Ohlsson  BStenram  UTranberg  KG Resection of colorectal liver metastases: 25-year experience. World J Surg 1998;22 (3) 268- 277
PubMed
Fong  YFortner  JSun  RLBrennan  MFBlumgart  LH Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 1999;230 (3) 309- 321
PubMed
Minagawa  MMakuuchi  MTorzilli  G  et al.  Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results. Ann Surg 2000;231 (4) 487- 499
PubMed
Abdalla  EKVauthey  JNEllis  LM  et al.  Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004;239 (6) 818- 827
PubMed
Bozzetti  FBignami  PMontalto  FDoci  RGennari  L Repeated hepatic resection for recurrent metastases from colorectal cancer. Br J Surg 1992;79 (2) 146- 148
PubMed
Adam  RBismuth  HCastaing  D  et al.  Repeat hepatectomy for colorectal liver metastases. Ann Surg 1997;225 (1) 51- 62
PubMed
Fernandez-Trigo  VShamsa  FAldrete  J  et al. Repeat Hepatic Resection Registry, Repeat liver resections from colorectal metastasis. Cancer Treat Res 1994;69185- 196
PubMed
Fong  YBlumgart  LHCohen  AFortner  JBrennan  MF Repeat hepatic resections for metastatic colorectal cancer. Ann Surg 1994;220 (5) 657- 662
PubMed
Jaeck  DBachellier  PGuiguet  M  et al.  Survival benefit of repeat liver resection for recurrent colorectal metastases: 143 cases. Wiad Lek 1997;50 ((suppl 1, pt 1)) 102- 104
PubMed
Muratore  APolastri  RBouzari  HVergara  VFerrero  ACapussotti  L Repeat hepatectomy for colorectal liver metastases: a worthwhile operation? J Surg Oncol 2001;76 (2) 127- 132
PubMed
Petrowsky  HGonen  MJarnagin  W  et al.  Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi-institutional analysis. Ann Surg 2002;235 (6) 863- 871
PubMed
Pinson  CWWright  JKChapman  WCGarrard  CLBlair  TKSawyers  JL Repeat hepatic surgery for colorectal cancer metastasis to the liver. Ann Surg 1996;223 (6) 765- 776
PubMed
Sugarbaker  PH Repeat hepatectomy for colorectal metastases. J Hepatobiliary Pancreat Surg 1999;6 (1) 30- 38
PubMed
Suzuki  SSakaguchi  TYokoi  Y  et al.  Impact of repeat hepatectomy on recurrent colorectal liver metastases. Surgery 2001;129 (4) 421- 428
PubMed
Takahashi  SInoue  KKonishi  MNakagouri  TKinoshita  T Prognostic factors for poor survival after repeat hepatectomy in patients with colorectal liver metastases. Surgery 2003;133 (6) 627- 634
PubMed
Tuttle  TMCurley  SARoh  MS Repeat hepatic resection as effective treatment of recurrent colorectal liver metastases. Ann Surg Oncol 1997;4 (2) 125- 130
PubMed
Vaillant  JCBalladur  PNordlinger  B  et al.  Repeat liver resection for recurrent colorectal metastases. Br J Surg 1993;80 (3) 340- 344
PubMed
Yamada  HKatoh  HKondo  SOkushiba  SMorikawa  T Repeat hepatectomy for recurrent hepatic metastases from colorectal cancer. Hepatogastroenterology 2001;48 (39) 828- 830
PubMed
Yamamoto  JKosuge  TShimada  KYamasaki  SMoriya  YSugihara  K Repeat liver resection for recurrent colorectal liver metastases. Am J Surg 1999;178 (4) 275- 281
PubMed
Nordlinger  BVaillant  JCGuiguet  M  et al. Association Francaise de Chirurgie, Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 cases. J Clin Oncol 1994;12 (7) 1491- 1496
PubMed
Laurent  CSa Cunha  ACouderc  PRullier  ESaric  J Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg 2003;90 (9) 1131- 1136
PubMed
Couinaud  C Leading principles for controlled hepatectomies [author's transl] [in French]. Chirurgie 1980;106 (2) 136- 142
PubMed
Aramaki  MKawano  KKai  T  et al.  Postoperative complications of repeat hepatectomy for liver metastasis from colorectal carcinoma. Hepatogastroenterology 2000;47 (32) 478- 480
PubMed
Elias  DLasser  PHoang  JM  et al.  Repeat hepatectomy for cancer. Br J Surg 1993;80 (12) 1557- 1562
PubMed
Elias  DDe Baere  TSmayra  TOuellet  JFRoche  ALasser  P Percutaneous radiofrequency thermoablation as an alternative to surgery for treatment of liver tumour recurrence after hepatectomy. Br J Surg 2002;89 (6) 752- 756
PubMed
Adam  RPascal  GCastaing  D  et al.  Tumor progression while on chemotherapy: a contraindication to liver resection for multiple colorectal metastases? Ann Surg 2004;240 (6) 1052- 1064
PubMed
Elias  DOuellet  JFBellon  NPignon  JPPocard  MLasser  P Extrahepatic disease does not contraindicate hepatectomy for colorectal liver metastases. Br J Surg 2003;90 (5) 567- 574
PubMed

Figures

Place holder to copy figure label and caption
Figure 1.

Kaplan-Meier curves comparing survival after liver resection in patients who underwent a single liver resection and those who underwent a second hepatectomy.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Kaplan-Meier curves comparing survival after liver resection in patients with and without extrahepatic disease.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 3.

Kaplan-Meier curves comparing survival after liver resection according to interval between the first and second hepatectomies.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Tumor Data in Patients With Colorectal Liver Metastases Who Underwent a Single and a Second Hepatic Resection
Table Graphic Jump LocationTable 3. Univariate Analysis of Prognostic Factors for Survival After a Second Liver Resection of Colorectal Liver Metastases
Table Graphic Jump LocationTable 4. Summary of Large Series of Repeat Hepatectomy in Patients With Recurrent Liver Metastases

References

Hughes  KSSimon  RSonghorabodi  S  et al.  Resection of the liver for colorectal carcinoma metastases: a multi-institutional study of patterns of recurrence. Surgery 1986;100 (2) 278- 284
PubMed
Nordlinger  BGuiguet  MVaillant  JC  et al. Association Francaise de Chirurgie, Surgical resection of colorectal carcinoma metastases to the liver: a prognostic scoring system to improve case selection, based on 1568 patients. Cancer 1996;77 (7) 1254- 1262
PubMed
Ohlsson  BStenram  UTranberg  KG Resection of colorectal liver metastases: 25-year experience. World J Surg 1998;22 (3) 268- 277
PubMed
Fong  YFortner  JSun  RLBrennan  MFBlumgart  LH Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 1999;230 (3) 309- 321
PubMed
Minagawa  MMakuuchi  MTorzilli  G  et al.  Extension of the frontiers of surgical indications in the treatment of liver metastases from colorectal cancer: long-term results. Ann Surg 2000;231 (4) 487- 499
PubMed
Abdalla  EKVauthey  JNEllis  LM  et al.  Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004;239 (6) 818- 827
PubMed
Bozzetti  FBignami  PMontalto  FDoci  RGennari  L Repeated hepatic resection for recurrent metastases from colorectal cancer. Br J Surg 1992;79 (2) 146- 148
PubMed
Adam  RBismuth  HCastaing  D  et al.  Repeat hepatectomy for colorectal liver metastases. Ann Surg 1997;225 (1) 51- 62
PubMed
Fernandez-Trigo  VShamsa  FAldrete  J  et al. Repeat Hepatic Resection Registry, Repeat liver resections from colorectal metastasis. Cancer Treat Res 1994;69185- 196
PubMed
Fong  YBlumgart  LHCohen  AFortner  JBrennan  MF Repeat hepatic resections for metastatic colorectal cancer. Ann Surg 1994;220 (5) 657- 662
PubMed
Jaeck  DBachellier  PGuiguet  M  et al.  Survival benefit of repeat liver resection for recurrent colorectal metastases: 143 cases. Wiad Lek 1997;50 ((suppl 1, pt 1)) 102- 104
PubMed
Muratore  APolastri  RBouzari  HVergara  VFerrero  ACapussotti  L Repeat hepatectomy for colorectal liver metastases: a worthwhile operation? J Surg Oncol 2001;76 (2) 127- 132
PubMed
Petrowsky  HGonen  MJarnagin  W  et al.  Second liver resections are safe and effective treatment for recurrent hepatic metastases from colorectal cancer: a bi-institutional analysis. Ann Surg 2002;235 (6) 863- 871
PubMed
Pinson  CWWright  JKChapman  WCGarrard  CLBlair  TKSawyers  JL Repeat hepatic surgery for colorectal cancer metastasis to the liver. Ann Surg 1996;223 (6) 765- 776
PubMed
Sugarbaker  PH Repeat hepatectomy for colorectal metastases. J Hepatobiliary Pancreat Surg 1999;6 (1) 30- 38
PubMed
Suzuki  SSakaguchi  TYokoi  Y  et al.  Impact of repeat hepatectomy on recurrent colorectal liver metastases. Surgery 2001;129 (4) 421- 428
PubMed
Takahashi  SInoue  KKonishi  MNakagouri  TKinoshita  T Prognostic factors for poor survival after repeat hepatectomy in patients with colorectal liver metastases. Surgery 2003;133 (6) 627- 634
PubMed
Tuttle  TMCurley  SARoh  MS Repeat hepatic resection as effective treatment of recurrent colorectal liver metastases. Ann Surg Oncol 1997;4 (2) 125- 130
PubMed
Vaillant  JCBalladur  PNordlinger  B  et al.  Repeat liver resection for recurrent colorectal metastases. Br J Surg 1993;80 (3) 340- 344
PubMed
Yamada  HKatoh  HKondo  SOkushiba  SMorikawa  T Repeat hepatectomy for recurrent hepatic metastases from colorectal cancer. Hepatogastroenterology 2001;48 (39) 828- 830
PubMed
Yamamoto  JKosuge  TShimada  KYamasaki  SMoriya  YSugihara  K Repeat liver resection for recurrent colorectal liver metastases. Am J Surg 1999;178 (4) 275- 281
PubMed
Nordlinger  BVaillant  JCGuiguet  M  et al. Association Francaise de Chirurgie, Survival benefit of repeat liver resections for recurrent colorectal metastases: 143 cases. J Clin Oncol 1994;12 (7) 1491- 1496
PubMed
Laurent  CSa Cunha  ACouderc  PRullier  ESaric  J Influence of postoperative morbidity on long-term survival following liver resection for colorectal metastases. Br J Surg 2003;90 (9) 1131- 1136
PubMed
Couinaud  C Leading principles for controlled hepatectomies [author's transl] [in French]. Chirurgie 1980;106 (2) 136- 142
PubMed
Aramaki  MKawano  KKai  T  et al.  Postoperative complications of repeat hepatectomy for liver metastasis from colorectal carcinoma. Hepatogastroenterology 2000;47 (32) 478- 480
PubMed
Elias  DLasser  PHoang  JM  et al.  Repeat hepatectomy for cancer. Br J Surg 1993;80 (12) 1557- 1562
PubMed
Elias  DDe Baere  TSmayra  TOuellet  JFRoche  ALasser  P Percutaneous radiofrequency thermoablation as an alternative to surgery for treatment of liver tumour recurrence after hepatectomy. Br J Surg 2002;89 (6) 752- 756
PubMed
Adam  RPascal  GCastaing  D  et al.  Tumor progression while on chemotherapy: a contraindication to liver resection for multiple colorectal metastases? Ann Surg 2004;240 (6) 1052- 1064
PubMed
Elias  DOuellet  JFBellon  NPignon  JPPocard  MLasser  P Extrahepatic disease does not contraindicate hepatectomy for colorectal liver metastases. Br J Surg 2003;90 (5) 567- 574
PubMed

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