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10.1245/s10434-006-9284-5
Annals of Surgical Oncology 14:1143-1150 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Timing of Resection of Liver Metastases Synchronous to Colorectal Tumor: Proposal of Prognosis-Based Decisional Model

Lorenzo Capussotti, MD, Luca Vigano’, MD, Alessandro Ferrero, MD, Roberto Lo Tesoriere, MD, Dario Ribero, MD and Roberto Polastri, MD

Unit of Surgical Oncology, Institute for Cancer Research and Treatment, Strada Provinciale 142 km 3,95 10060 Candiolo, Torino, Italy

Correspondence: Address correspondence and reprint requests to: Lorenzo Capussotti, MD; E-mail: lcapussotti{at}mauriziano.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Timing of hepatectomy for synchronous metastases of colorectal cancer is still debated. The aim of this retrospective study was to analyze prognostic factors after synchronous and delayed liver resections to define selection criteria for choosing timing of hepatectomy.

Methods: The study was performed on 127 patients with synchronous metastases undergoing radical hepatectomy. We divided patients according to the timing of hepatectomy: 70 synchronous (group A) and 57 delayed (group B).

Results: Overall survival was similar between the two groups (5-year survival 30.8% vs. 32.0% A vs. B, P = .406). The multivariate analysis evidenced four independent prognostic factors in group A: male sex (P = .04), T4 (P = .0035), more than three metastases (P = .0001), and metastatic infiltration of nearby structures (P < .0001). There were no statistically significant prognostic factors in group B. Patients with more than three metastases had a significantly worse survival in group A than in group B (3-year survival, 15.0% vs. 34.3%, P = .007); similarly, borderline significant difference was encountered in patients with T4 primary tumor (3-year survival, 16.7% vs. 60%, P = .064)

Conclusions: Patients with liver metastases synchronous with colorectal cancer with T4 primary tumor, metastasis infiltration of neighboring structures, and especially with more than three metastases should receive neoadjuvant chemotherapy before liver resection.

Key Words: Liver surgery • Colorectal liver metastases • Synchronous liver metastases • Timing of liver resection • Neoadjuvant chemotherapy • Prognostic factors


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Surgical resection is the best treatment for patients with colorectal liver metastases1–3; nevertheless, the timing of hepatectomy for metastases synchronous with the primary tumor is not yet well defined.4,5 Many papers have demonstrated the feasibility of synchronous hepatic and colorectal resection with good short-term results,6–12 even if major hepatectomy is planned.13 Still, no clear data are available concerning long-term outcomes and timing of perioperative chemotherapy. Some authors proposed neoadjuvant chemotherapy before liver resection to select patients that can benefit from surgery, but no prognostic factor has been identified as an indication for this treatment.14,15 The aim of this study was to analyze the prognostic factors of synchronous liver metastases after synchronous and delayed hepatectomy to identify selection criteria for the timing of liver resection.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between January 1985 and December 2004, a total of 385 patients underwent liver resection for colorectal liver metastases at our institution. In 172 cases, liver metastases were synchronous with colorectal cancer, and clinical data of these patients, recorded in a prospective database, were retrospectively reviewed. Patients were divided into two groups according to the timing of liver resection: 88 patients who underwent hepatectomy at the time of colorectal surgery, and 84 who underwent delayed liver resection.

To better evaluate the prognostic factors, the following exclusion criteria were applied: neoadjuvant chemotherapy before liver resection because of no resectable disease (9 patients in the synchronous group and 15 in the delayed); postoperative mortality (1 patient in the synchronous group); no radical resection (4 in the synchronous group and 4 in the delayed group); two-stage hepatectomy (4 in the synchronous group and 2 in the delayed group); preoperative portal vein embolization or portal branch ligature (6 in the delayed group). Therefore, our analysis was performed on data of 127 patients, 70 of whom underwent synchronous liver and colorectal resection and 57 of whom underwent delayed hepatectomy.

Preoperative Evaluation
All patients were preoperatively evaluated by total colonoscopy and thoracoabdominal computed tomographic scan. Every patient was considered for synchronous liver and colon resection. Synchronous hepatic resections were not performed in patients with American Society of Anesthesiologists (ASA) score higher than 3 and in patients with bowel obstruction or perforation, and when all gross disease could not be removed. Until 1992, in the first part of our series, hepatectomy was delayed in case of scheduled major liver resection synchronous with rectal resection.

Since 1998, every patient scheduled for a major hepatectomy underwent computed tomography–volumetry of future remnant liver. Patients with estimated future remnant liver >25% underwent liver resection without preoperative portal vein embolization.

Adjuvant Chemotherapy and Follow-up
Before 1990, no adjuvant chemotherapy was administrated. Since 1990, a progressively larger number of patients were treated with postoperative fluorouracil. Since 1998, oxaliplatin-based adjuvant chemotherapy was routinely planned for all patients. In the last years, postoperative chemotherapy with irinotecan was performed in selected patients.

After liver resection, all patients were followed every 3 months. Follow-up consisted of serum carcinoembryonic antigen and cancer antigen 19–9 detection and abdominal ultrasonography; computed tomographic scan and total colonoscopy were performed every year.

Follow-up was performed by outpatient clinics or by contacting the general practitioner of the patients, and data were updated to December 2005. Survival was computed from the date of liver surgery.

Definitions
Rectal adenocarcinoma was defined as tumor sited within 15 cm from the anal verge. Synchronous metastases were defined as liver metastasis diagnosed before colorectal resection or at the time of laparotomy. Major hepatectomy was defined as resection of three or more Couinaud segments. Resection was considered radical when all tumors were resected with a microscopically free surgical margin.

Statistical Analysis
Continuous variables were compared between groups by the unpaired t-test; categorical variables were compared by the {chi}2 test or Fisher’s exact test, as appropriate. Patients’ overall survival was calculated by the Kaplan-Meier method, and patient comparison was performed by the log rank test. A P value of less than .05 was considered significant for all tests. A multivariate analysis was performed that included in a Cox regression model all significant variables (P < .05) at the univariate analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Patient Characteristics
Patients undergoing synchronous liver and colorectal resection were significantly older (64.9 vs. 60.8 years, P = .010), and they had a lower rate of major hepatectomy (34.3% vs. 56.1%, P = .019). The other pre- and intraoperative characteristics were similar between the two groups (Table 1Go). The number of patients with more than three metastases was similar between the two groups (11.4% vs. 17.5%, P = .444). Resection of structures infiltrated by liver metastases was associated in eight patients: diaphragm in six patients (five in the delayed group), portal vein in one, and rib in one (both in the synchronous group) (4.2% vs. 8.8%, P = .504). Postoperative results were similar into the two groups: one patient died in the synchronous group (his data were excluded from analysis), and overall morbidity rates were 35.7% in the synchronous group and 36.8% in the delayed group (P = .895).


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  		TABLE 1. Patient characteristics
 
Among the 57 patients with delayed liver resection, 44 were referred to our institution after primary tumor resection. In the remaining 13 patients, liver resection was delayed for the following reasons: ASA score higher than 3 in six cases, rectal resection combined with planned major hepatectomy before 1992 in six, and emergency surgery for bowel obstruction in one.

In the delayed group, 39 patients received chemotherapy before liver resection: fluorouracil in 14 patients, oxaliplatin in 19, irinotecan in 4, and oxaliplatin-irinotecan in 2. There was a partial response to chemotherapy in 21 cases (53.8%), stable disease in 16 (41.0%), and tumor progression in 2 (5.2%). In the delayed hepatectomies, median interval between colon and liver resection was 6 months (range, 1–36 months).

Median follow-up was similar between the two groups: 38.2 months in the synchronous resections (range, 3.0–184.3 months) versus 33.7 months in the delayed group (range, 5.9–86.2 months) (P = .348). After liver resection, 82 patients received adjuvant chemotherapy: 44 in the synchronous group and 38 in the delayed group (62.8% vs. 66.7%, P = .655). Chemotherapy regimens were similar between the two groups.

Overall survival was similar between the two groups: 1-, 3- and 5-year survival rates were 91.4%, 44.7%, and 30.8% in the synchronous group versus 93.0%, 54.6%, and 32.0% in the delayed group (P = .406) (Fig. 1Go).


Figure 1
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  		FIG. 1. Overall survival actuarial curves of patients undergoing synchronous versus delayed liver resection for colorectal liver metastases synchronous to primary colorectal tumor (P = .406).

 
Prognostic Factors in the Synchronous Resection Group
Univariate analysis found 5 of 15 examined variables to be statistically significant prognostic factors: sex, single versus multiple metastases, number of metastases (three or fewer versus more than three), associated resection of structures infiltrated by liver metastases, and T stage of primary colorectal tumor (T2–3 vs. T4) (Table 2Go). Four of five variables significant at the previous analysis were identified by multivariate analysis as independent prognostic factors: sex, number of metastases (three or fewer versus more than three), associated resection of structures infiltrated by liver metastases, and T stage of primary colorectal tumor (Table 3Go).


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  		TABLE 2. Univariate analysis of prognostic factors in synchronous resection group
 

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  		TABLE 3. Multivariate analysis of prognostic factors in synchronous resection group
 
Prognostic Factors of Survival in the Delayed Resection Group
At the univariate analysis (Table 4Go), none of the 16 examined variables were found to be statistically significant prognostic factors. Neoadjuvant chemotherapy was not correlated with prognosis.


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  		TABLE 4. Univariate analysis of prognostic factors in delayed resection group
 
Comparison of the Two Groups
Long-term results of synchronous and delayed groups were compared considering the prognostic factors identified at the multivariate analysis. Patients with more than three metastases in the delayed group had a significantly better prognosis, with a 3-year survival rate of 34.3% vs. 15% (P = .007; Fig. 2Go). Patients with T4 colorectal tumor in the delayed group had a borderline statistically significant better survival with a 3-year survival rate of 60.0% vs. 16.7% (P = .064, Fig. 3Go). Patients who required associated resection of structures infiltrated by liver metastases in the delayed group had a better 3-year survival, but this difference was not statistically significant: 60.0% vs. 0% (P = .168; Fig. 4Go). Male patients had similar survival in both groups (Table 5Go).


Figure 2
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  		FIG. 2. Overall survival actuarial curves of patients with more than 3 liver metastases undergoing synchronous versus delayed liver resection (P = .007).

 

Figure 3
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  		FIG. 3. Overall survival actuarial curves of patients with T4 colorectal tumor stage undergoing synchronous versus delayed liver resection (P = .064).

 

Figure 4
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  		FIG. 4. Overall survival actuarial curves of patients with associated resection of structures infiltrated by liver metastases undergoing synchronous versus delayed liver resection (P = .168).

 

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  		TABLE 5. Comparison of survival between two groups considering patients with bad prognostic factors at multivariate analysis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Timing of liver resection for metastases synchronous with primary colorectal cancer should be decided according to technical and oncological considerations.7,15 The first aspect has been clarified by some papers suggesting feasibility and safety of synchronous liver and colorectal resections,6–12 even if major liver resection is planned.13 But at present, no oncological criteria for choosing timing of hepatectomy are available in the literature.

Some authors proposed a "time-test" approach to assess biological behavior of the neoplasm, to treat potentially occult disease, and to avoid operation in patients with rapidly progressing tumors.16 Furthermore, neoadjuvant chemotherapy can be administrated. Adam et al.17 analyzed multiple and bilobar metastases, and they reported response to chemotherapy to be an important prognostic factor. Allen et al.15 reported similar results in synchronous liver metastases: in 106 patients with synchronous liver metastases undergoing delayed hepatectomy, patients whose disease did not progress while they received chemotherapy had a far better prognosis compared with those who did not receive chemotherapy. Anyway, many series reported similar survival rates after synchronous and delayed liver resections,6,8,9,11,18 and no clear benefit from a time-test approach was defined. Similarly, in our series, no difference in survival was encountered between the two groups of patients, and treatment with neoadjuvant chemotherapy or patient response to it did not correlate with survival. Moreover, the tumor can progress and become unresectable, especially in patients with large liver metastases or nodules located in critical positions, but that were resectable at first presentation. Hence, we believe it is important to define oncological criteria for choosing patients with synchronous liver metastases who could benefit from neoadjuvant chemotherapy.

In 2001, Sugawara et al.19 compared prognostic factors of synchronous metastases to those of metachronous ones, but no differences were identified between the two groups. In 2003, Fujita et al.18 analyzed patients undergoing synchronous liver and colorectal resection and reported the presence of six or more metastatic lymph nodes as a poor prognostic factor; survival rates in these patients were similar to those who did not undergo resection. This can be considered the only selection criteria available in the literature, but its usefulness is limited because it cannot be preoperatively evaluated.

Here, we compared patients with resectable liver metastases undergoing synchronous liver and colorectal resection to those with delayed hepatectomy. This is a retrospective analysis of prospectively collected data, and some bias could be partly related both to the length of the examined period (20 years) with variability of surgical approach and chemotherapy regimen and to selection criteria. Nevertheless, it is important to emphasize that timing of liver resection was mainly chosen according to technical reasons (primary tumor treated in other hospital, ASA score, rectal cancer), and no oncological selection criteria were applied. We identified four prognostic factors in the synchronous group that had no influence on survival in the delayed resections: more than three liver metastases, T4 primary colorectal tumor, presence of liver metastases infiltrating neighboring structures, and male sex.

Considering the first variable, many series reported the number of liver metastases number as an important prognostic factor20–26; in addition, Fong et al.20 included this parameter (single vs. multiple) in his prognostic risk score. Different numbers of nodules were chosen as the cutoff in other series, but in many reports, three nodules were considered a threshold for a good prognosis.24–26 Tanaka et al.14 described a benefit from neoadjuvant chemotherapy in patients with five or more metastases. To date, no specific analysis of chemotherapy was performed for synchronous liver metastases. In our series, for the first time, the presence of more than three metastases was confirmed to be a prognostic factor in the synchronous group, but it was not related to survival in patients who underwent delayed hepatectomy. Moreover, when we consider only patients with more than three metastases, prognosis was far worse in the synchronous group than in the delayed group. These data suggest that patients with four or more liver metastases synchronous with primary colorectal cancer have to be carefully evaluated before resection because they can have a dismal prognosis due to rapidly progressing disease. Immediate resection may not be radical because of other occult hepatic and/or extrahepatic metastases.16 In these cases, neoadjuvant chemotherapy allows assessment of biological behavior of the neoplasm and discovery of potentially occult disease; as a consequence, patients with highly aggressive tumors can be excluded from surgery.16 In our series, the better prognosis of patients with four or more metastases undergoing delayed hepatectomy compared with those treated synchronously can be justified by this selection: time-test strategy and neoadjuvant chemotherapy probably led to avoid surgery in patients with rapidly progressing disease and to perform liver resection in selected patients who could really benefit from surgery. According to these data, patients with more than three metastases synchronous with primary colorectal cancer should be scheduled for neoadjuvant chemotherapy before liver resection.

Aggressive tumor behavior is commonly considered a negative prognostic factor, and this can be characterized by infiltration of contiguous structures by primary tumor or by liver metastases.20,22,24,27,28 T4 stage was borderline significant in the univariate analysis of Fujita et al.,18 but it was not confirmed by the multivariate analysis. On the contrary, to our knowledge, no studies considered infiltration of close structures by liver metastases. In our series, both factors were statistically significantly related to prognosis, but only in the synchronous group. Moreover, considering patients with T4 tumors, a borderline statistically significant better survival was evidenced in the delayed group compared with the synchronous one. Therefore, as suggested for number of metastases, tumor infiltration of neighboring structures could be considered an indication for neoadjuvant chemotherapy, to select the best candidates for liver surgery, and to exclude rapidly progressing neoplasm.

The last variable with a prognostic role in synchronous resections was the patient’s sex: male patients had a statistically significantly worse prognosis. Some authors previously reported a better prognosis after hepatectomy for colorectal liver metastases in female patients,29,30 but this finding has never been clearly explained. A hormonal influence may be hypothesized, but further studies are necessary to confirm and clarify these data.

The parameters identified in our series have an important characteristic: they can be clearly assessed before or during surgery, thus allowing easy patient management. Some papers suggested that patients with synchronous liver metastases should receive synchronous liver and colorectal resection,6–12 even if major liver resection is planned.13 In the presence of the oncologic prognostic factors identified by this study, patients should be evaluated for neoadjuvant chemotherapy to assess biological behavior of the neoplasm and to exclude from surgery patients with rapidly progressing disease. If neoadjuvant chemotherapy is planned, timing of colorectal resection should be decided according to symptoms of primary tumor: many papers31–34 have demonstrated that patients with asymptomatic colorectal tumor do not need immediate colorectal resection and that they can safely receive chemotherapy with a low morbidity rate; at the end of the therapy, they can undergo synchronous colorectal and hepatic resection.

In conclusion, timing of liver resection in patients with liver metastases synchronous with colorectal cancer should be decided according to oncological reasons, and selection criteria for neoadjuvant chemotherapy are needed. We suggest that patients with T4 primary tumor, liver metastases infiltrating nearby structures, and especially with more than three hepatic nodules receive neoadjuvant chemotherapy before liver resection.


   ACKNOWLEDGMENTS
 
Study conception and design: Luca Viganò, Alessandro Ferrero, Lorenzo Capussotti; acquisition of data: Roberto Lo Tesoriere, Dario Ribero; analysis and interpretation of data: Luca Vigano’, Alessandro Ferrero, Roberto Lo Tesoriere; drafting of manuscript: Luca Vigano’, Dario Ribero, Roberto Polastri; critical revision: Lorenzo Capussotti, Alessandro Ferrero, Roberto Polastri; supervision: Lorenzo Capussotti.

Received for publication August 4, 2006. Accepted for publication November 1, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Adam R, Pascal G, Azoulay D, Tanaka K, Castaing D, Bismuth H. Liver resection for colorectal metastases: the third hepatectomy. Ann Surg 2003; 238:871–83; discussion 883–4.[CrossRef][Medline]
  2. D’Angelica M, Brennan MF, Fortner JG, Cohen AM, Blumgart LH, Fong Y. Ninety-six five-year survivors after liver resection for metastatic colorectal cancer. J Am Coll Surg 1997; 185:554–9.[CrossRef][Medline]
  3. Ferrero A, Polastri R, Muratore A, Zorzi D, Capussotti L. Extensive resections for colorectal liver metastases. J Hepatobiliary Pancreat Surg 2004; 11:92–6.[CrossRef][Medline]
  4. Belghiti J. Synchronous and resectable hepatic metastases of colorectal cancer: should there be a minimum delay before hepatic resection? Ann Chir 1990; 44:427–9; discussion 429–32.[Medline]
  5. Elias D, Detroz B, Lasser P, Plaud B, Jerbi G. Is simultaneous hepatectomy and intestinal anastomosis safe? Am J Surg 1995; 169:254–60.[CrossRef][Medline]
  6. de Santibanes E, Lassalle FB, McCormack L, et al. Simultaneous colorectal and hepatic resections for colorectal cancer: postoperative and longterm outcomes. J Am Coll Surg 2002; 195:196–202.[CrossRef][Medline]
  7. Martin R, Paty P, Fong Y, et al. Simultaneous liver and colorectal resections are safe for synchronous colorectal liver metastasis. J Am Coll Surg 2003; 197:233–41; discussion 241–2.[CrossRef][Medline]
  8. Lyass S, Zamir G, Matot I, Goitein D, Eid A, Jurim O. Combined colon and hepatic resection for synchronous colorectal liver metastases. J Surg Oncol 2001; 78:17–21.[CrossRef][Medline]
  9. Chua HK, Sondenaa K, Tsiotos GG, Larson DR, Wolff BG, Nagorney DM. Concurrent vs. staged colectomy and hepatectomy for primary colorectal cancer with synchronous hepatic metastases. Dis Colon Rectum 2004; 47:1310–6.[Medline]
  10. Jaeck D, Bachellier P, Weber JC, et al. Surgical strategy in the treatment of synchronous hepatic metastases of colorectal cancers. Analysis of a series of 59 operated on patients. Chirurgie 1999; 124:258–63.[CrossRef][Medline]
  11. Weber JC, Bachellier P, Oussoultzoglou E, Jaeck D. Simultaneous resection of colorectal primary tumour and synchronous liver metastases. Br J Surg 2003; 90:956–62.[CrossRef][Medline]
  12. Tanaka K, Shimada H, Matsuo K, et al. Outcome after simultaneous colorectal and hepatic resection for colorectal cancer with synchronous metastases. Surgery 2004; 136:650–9.[CrossRef][Medline]
  13. Capussotti L, Ferrero A, Viganò L, Ribero D, Lo Tesoriere R, Polastri R. Major liver resections synchronous with colorectal surgery. Ann Surg Oncol (in press).
  14. Tanaka K, Adam R, Shimada H, Azoulay D, Levi F, Bismuth H.. Role of neoadjuvant chemotherapy in the treatment of multiple colorectal metastases to the liver. Br J Surg 2003; 90:963–9.[CrossRef][Medline]
  15. Allen PJ, Kemeny N, Jarnagin W, DeMatteo R, Blumgart L, Fong Y. Importance of response to neoadjuvant chemotherapy in patients undergoing resection of synchronous colorectal liver metastases. J Gastrointest Surg 2003; 7:109–15; discussion 116–7.[CrossRef][Medline]
  16. Lambert LA, Colacchio TA, Barth RJ Jr. Interval hepatic resection of colorectal metastases improves patient selection. Arch Surg 2000; 135:473–9; discussion 479–80.[Abstract/Free Full Text]
  17. Adam R, Pascal G, Castaing D, et al. Tumor progression while on chemotherapy: a contraindication to liver resection for multiple colorectal metastases? Ann Surg 2004; 240:1052–61; discussion 1061–4.[CrossRef][Medline]
  18. Fujita S, Akasu T, Moriya Y. Resection of synchronous liver metastases from colorectal cancer. Jpn J Clin Oncol 2000; 30:7–11.[Abstract/Free Full Text]
  19. Sugawara Y, Yamamoto J, Yamasaki S, Shimada K, Kosuge T, Makuuchi M. Estimating the prognosis of hepatic resection in patients with metastatic liver tumors from colorectal cancer with special concern for the timing of hepatectomy. Surgery 2001; 129:408–13.[Medline]
  20. Fong Y, Fortner J, Sun RL, Brennan MF, Blumgart LH. Clinical score for predicting recurrence after hepatic resection for metastatic colorectal cancer: analysis of 1001 consecutive cases. Ann Surg 1999; 230:309–18; discussion 318–21.[CrossRef][Medline]
  21. Foster JH. Survival after liver resection for secondary tumors. Am J Surg 1978; 135:389–94.[CrossRef][Medline]
  22. Hughes KS, Rosenstein RB, Songhorabodi S, et al. Resection of the liver for colorectal carcinoma metastases. A multi-institutional study of long-term survivors. Dis Colon Rectum 1988; 31:1–4.[Medline]
  23. Cady B, Stone MD, McDermott WV Jr, et al. Technical and biological factors in disease-free survival after hepatic resection for colorectal cancer metastases. Arch Surg 1992; 127:561–8; discussion 568–9.[Abstract/Free Full Text]
  24. Nordlinger B, Guiguet M, Vaillant JC, et al. Surgical resection of colorectal carcinoma metastases to the liver. A prognostic scoring system to improve case selection, based on 1568 patients. Association Francaise de Chirurgie. Cancer 1996; 77:1254–62.[CrossRef][Medline]
  25. Ekberg H, Tranberg KG, Andersson R, et al. Determinants of survival in liver resection for colorectal secondaries. Br J Surg 1986; 73:727–31.[Medline]
  26. Stephenson KR, Steinberg SM, Hughes KS, Vetto JT, Sugarbaker PH, Chang AE. Perioperative blood transfusions are associated with decreased time to recurrence and decreased survival after resection of colorectal liver metastases. Ann Surg 1988; 208:679–87.[Medline]
  27. Scheele J, Stangl R, Altendorf-Hofmann A, Gall FP. Indicators of prognosis after hepatic resection for colorectal secondaries. Surgery 1991; 110:13–29.[Medline]
  28. Doci R, Gennari L, Bignami P, Montalto F, Morabito A, Bozzetti F. One hundred patients with hepatic metastases from colorectal cancer treated by resection: analysis of prognostic determinants. Br J Surg 1991; 78:797–801.[Medline]
  29. Adson MA. Resection of liver metastases—when is it worthwhile? World J Surg 1987; 11:511–20.[CrossRef][Medline]
  30. Hohenberger P, Schlag PM, Gerneth T, Herfarth C. Pre- and postoperative carcinoembryonic antigen determinations in hepatic resection for colorectal metastases. Predictive value and implications for adjuvant treatment based on multivariate analysis. Ann Surg 1994; 219:135–43.[Medline]
  31. Benoist S, Pautrat K, Mitry E, Rougier P, Penna C, Nordlinger B. Treatment strategy for patients with colorectal cancer and synchronous irresectable liver metastases. Br J Surg 2005; 92:1155–60.[CrossRef][Medline]
  32. Scoggins CR, Meszoely IM, Blanke CD, Beauchamp RD, Leach SD. Nonoperative management of primary colorectal cancer in patients with stage IV disease. Ann Surg Oncol 1999; 6:651–7.[Abstract]
  33. Tebbutt NC, Norman AR, Cunningham D, et al. Intestinal complications after chemotherapy for patients with unresected primary colorectal cancer and synchronous metastases. Gut 2003; 52:568–73.[Abstract/Free Full Text]
  34. Stelzner S, Hellmich G, Koch R, Ludwig K. Factors predicting survival in stage IV colorectal carcinoma patients after palliative treatment: a multivariate analysis. J Surg Oncol 2005; 89:211–7.[CrossRef][Medline]



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