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10.1245/s10434-006-9312-5
Annals of Surgical Oncology 14:1161-1169 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Comparison Between Local Ablative Therapy and Chemotherapy for Non-Resectable Colorectal Liver Metastases: A Prospective Study

Theo J. M. Ruers1, Joris J. Joosten1, Bastiaan Wiering1, Barbara S. Langenhoff1, Heleen M. Dekker2, Theo Wobbes1, Wim J. G. Oyen3, Paul F. M. Krabbe4 and Cornelis J. A. Punt5

1 Department of Surgery, Division of Surgical Oncology, Radboud University Nijmegen Medical Centre, P.O. Box 9101, 6500 HB, Nijmegen, The Netherlands
2 Department of Radiology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
3 Department of Nuclear Medicine, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
4 Department of Medical Technology Assessment, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
5 Department of Medical Oncology, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands

Correspondence: Address correspondence and reprint requests to: Theo J. M. Ruers; E-mail: T.Ruers{at}chir.umcn.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENT AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: There is a growing interest for the use of local ablative techniques in patients with non-resectable colorectal liver metastases. Evidence on the efficacy over systemic chemotherapy is, however, extremely weak. In this prospective study we aim to assess the additional benefits of local tumour ablation.

Methods: A consecutive series of 201 colorectal cancer patients, without extrahepatic disease, that underwent laparotomy for surgical treatment of liver metastases, were prospectively followed for survival and HRQoL. At laparotomy three groups were identified: patients in whom radical resection of metastases proved feasible, patients in whom resection was not feasible and received local ablative therapy, and patients in whom resection or local ablation was not feasible for technical reasons and who received systemic chemotherapy.

Findings: Patients in the chemotherapy and in local ablation group were comparable for all prognostic variables tested. For the local ablation group overall survival at 2 and 5 years was 56 and 27%, respectively (median 31 months, n = 45), for the chemotherapy group 51 and 15%, respectively (median 26 months, n = 39) (P = 0.252). After resection these figures were 83 and 51%, respectively (median 61 months, n = 117) (P < 0.001). The median DFS after local ablation was 9 months, HRQoL was restored within 3 months. Patients after local ablation gained far more QALY’s (317) than in the chemotherapy group (165) (P < 0.001).

Interpretation: Although overall survival did not reached statistical significance, the median DFS of 9 months suggests a beneficial effect of local tumour ablation for non-resectable colorectal liver metastases. Moreover, compared with systemic chemotherapy more QALY’s were gained after local ablative therapy.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENT AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In patients with colorectal liver metastases, resection offers the best chance of cure, with 5-year survival rates between 35 and 50%.1–5 In the majority of cases, however, liver metastases prove non-resectable because of the high number of lesions or because of the location of the metastases. To these patients chemotherapy is generally offered, and a median overall survival up to 20 months can be achieved.6–9

In recent years, several techniques for local tumour destruction have emerged as an alternative treatment for patients with non-resectable colorectal liver metastases, e.g. cryoablation or radiofrequen-cy.10–19 Local tumour ablation aims at selective destruction of tumour tissue without significantly intervening with liver anatomy. Initially, these techniques were used by surgeons when confronted with non-resectable metastatic disease at laparotomy. More recently, new techniques have become available for laparoscopic or percutaneous use. Although many methods proved to be safe, the impact on survival of local tumour ablative therapy in case of non-resectable disease is still unclear.10,20 Several uncontrolled studies in patients with colorectal liver metastases showed effective local tumour control and median overall survival could be prolonged to over 30 months.10,12,14,16,21,22 These results were claimed to be superior when compared to historical controls treated by chemotherapy. This may, however, certainly be biased by patient selection. In contrast to the general patient population treated by chemotherapy, patients selected for local tumour ablation have only a limited number of liver metastases without any extrahepatic disease. Hence, the essential question whether there is any benefit of local tumour treatment over systemic chemotherapy in patients with non-resectable colorectal liver metastases is still open for debate.

In this comparative prospective study we opted to assess the additional benefit of local tumour ablation in a well-defined patient population. For this purpose we prospectively evaluated survival and health related quality of life from a consecutive cohort of patients that were selected for laparotomy and surgical treatment of their colorectal liver metastases. Patients that showed non-resectable liver metastases at laparotomy received either local tumour ablation or, when this was not feasible for technical reasons, systemic chemotherapy.


   PATIENT AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENT AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study Design and Treatment Algorithm
Between November 1995 and November 2004, a consecutive series of 201 patients received their first laparotomy in an attempt to cure metastatic disease confined to the liver. Patients were considered eligible for resection or local tumour ablation based on preoperative work-up by multislice CT of chest and abdomen, and colonoscopy or barium enema to exclude a new colorectal primary.

All patients were treated and followed at the Radboud University Nijmegen Medical Centre according to standardized institutional protocols.

Following the application of a strict treatment algorithm, three major groups could be identified at laparotomy: (1) Patients treated by resection. Resection was always considered the treatment of choice whenever negative resection margins could be obtained. Essentially, resection was performed for any number or location of metastases (unibilobar) as long as not more than 70% of liver needed to be removed. (2) Patients treated by local tumour ablation. Local treatment (by cryosurgery or radiofrequeny) was only performed when resection alone could not result in adequate treatment of all liver lesions. Local tumour ablation, either alone or in combination with resection, was only considered when complete tumour eradication of all liver lesions was judged possible. (3) Patients treated by systemic chemotherapy. Patients with metastases confined to the liver that could not be treated by resection or local tumour ablation because of purely technical reasons were further assigned to chemotherapy. Technically, resection was refrained from when negative resection margins could not be obtained or when more than 70% of the liver tissue had to be removed. Technical reasons to refrain from local tumour ablation were lesions too close to large vessels or main hepatic ducts, or lesions not accessible for local ablation. During the study period systemic chemotherapy consisted of 5-fluorouracil (5-FU) and leucovorin in the first line and irinotecan in the second line. Oxaliplatin became part of first line treatment in 2001 and since 2005 bevacizumab was added to the standard chemotherapy regimen.

Patients that were diagnosed with extrahepatic disease at laparotomy were excluded from further analysis since comparison to other patients groups was judged to be inappropriate (Fig. 1Go).


Figure 1
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  		FIG. 1. Study design and distribution of treatment groups.

 
Patients treated by resection or local tumour ablation did not receive any subsequent chemotherapy, unless non-resectable disease recurrence was encountered during follow-up.

Surgical Procedure
When resection was performed, a tumour free margin of at least 10 mm was aimed for. For local tumour ablation, cryoablation (n = 18) was used until 1999, thereafter local tumour ablation was performed by radiofrequency (n = 27). All ablative procedures were performed using an open surgical approach. Cryosurgery was performed with a LCS 2000 apparatus (Spembly Medical Hampshire, England; Candela Corporation, Eindhoven, The Netherlands). Radiofrequency was performed using a Radionics RF generator, model CC-1 (Radionics, Burlington, MA, USA) according to manufacturer’s guidelines. During all ablative procedures, tumour destruction was directly monitored by ultrasound. Local tumour ablation was considered successful when all tumour tissue and a rim of normal tissue of about 1 cm was included in the treated area.

Follow Up
All patients were followed prospectively and documented for disease recurrence or death. No patients were lost to follow up. Follow up after resection or local tumour ablation consisted of a 3 monthly CEA test and abdominal CT and 6 monthly chest CT until 3 years after resection. Thereafter, follow up was reduced to a CEA test and ultrasound of the liver every 6 months. Patients that were treated by systemic chemotherapy, were followed according to the chemotherapy regimen used but received at least 3 monthly evaluations. In case of disease recurrence after resection or local tumour ablation, surgical treatment was considered the first choice for liver recurrence or pulmonary recurrence. In case surgical intervention was not feasible chemotherapy was started. After resection or local tumour ablation, disease recurrence was defined as any lesion on CT scan suspicious for recurrence of disease. Overall and disease free survival were defined as the time interval from the date of laparotomy to the date of death or disease recurrence, respectively. All deaths within hospital or within 30 days of surgery were considered as surgery-related mortality.

Health-Related Quality of Life (HRQoL)
Patients were at random asked to consent in a prospective evaluation considering HRQoL. The study was approved by the local ethical committee. The instruments were completed preoperatively, 2–3 weeks after the operation (discharge from the hospital is usually within 10 days), and then every 3 months until 1 year after the operation.

Two validated (self-report) instruments were used, the EuroQol-5D (EQ-5D) and the European Organization for Research and Treatment of Cancer core questionnaire (EORTC QLQ C-30).23 Based on the scores of the EQ-5D index quality-adjusted life years (QALYs) were computed. Here, QALYs are expressed as quality-adjusted days instead of years.

Statistical Analysis
All data were analysed with SPSS statistical software (version 12.0.1 for Windows, SPSS, Chicago).

Patient survival rates were estimated using Kaplan–Meier analysis, evaluation of differences between two groups was performed with the log-rank test. Differences between groups were tested with Student’s t test or ANOVA in case of continuous variables, differences of proportions were tested with Fisher exact test. P values of less than 0.05 were considered statistically significant.

For HRQoL analysis mean scores with standard deviations were computed. For the QALY estimations we used the actual dates of completion of the EQ-5D instrument to compute the time intervals between successive measurements. These intervals were multiplied with the mean value of the derived index scores of the EQ-5D instrument of the time period involved (approximation of the trapezium rule).24


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENT AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In total 213 patients underwent laparotomy for surgical treatment of liver metastases. Twelve patients were found to have extrahepatic disease at laparotomy and were excluded from further analysis. Of the remaining 201 eligible patients, 117 (58.2%) patients underwent resection of the metastases, 45 (22.4%) patients with non-resectable lesions were treated by local tumour ablation and 39 (19.4%) patients, not eligible for resection or local tumour ablation because of technical reasons, were treated by chemotherapy. Patients and tumour characteristics of the different treatment groups are given in Table 1Go.


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  		TABLE 1. Patient and tumour characteristics according to treatment group
 
The local ablation group and the chemotherapy group were comparable for all prognostic indicators. The resection group differed significantly from the local ablation group and the chemotherapy group with regard to the number of metastases. The median number of lesions in the resection group was 1 versus 4 in both other groups. For further comparison, the different treatment groups were analysed according to the prognostic scoring system of Fong et al.25 The resection group showed a significantly better prognostic score compared to both other groups. No significant differences in prognostic scores were found between the local ablation group and the chemotherapy group, thereby allowing a direct comparison of outcome parameters between these groups.

Overall Survival
At the time of analysis (median follow up 61 months) 49 patients (42%) in the resection group had died, as compared with 30 patients (67%) in the local ablation group and 28 (72%) patients in the chemotherapy group. According to Kaplan Meier survival analysis, the 2 and 5-year overall survival in the resection group was 83 and 51%, respectively (Fig. 2Go). In the local ablation group these figures were 56 and 27% respectively, and in the chemotherapy group 51 and 15%, respectively. Median overall survival was 61 months (95% CI 41–81 months) in the resection group, 31 months in the local ablation group (95% CI 20–42 months) and 26 months in the chemotherapy group (95% CI 17–35 months). The difference in overall survival between the resection group and both other groups was statistically significant (P < 0.001). The difference in overall survival between the chemotherapy group and the group of patients treated by local tumour ablation did not reach statistical significance (P = 0.252).


Figure 2
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  		FIG. 2. Kaplan–Meier analysis of overall survival according to treatment group.

 
Peri-operative mortality in the 162 patients undergoing surgical treatment of the liver metastases was 3.7%. Four patients in the resection group died, one patient due to cardiac failure and three patients due to postoperative sepsis. Two patients in the local tumour ablation group died, one patient after radiofrequency plus extended resection due to postoperative sepsis and one patient due to acute myocardial infarction 14 days after an uncomplicated cryosurgical procedure.

Disease Free Survival
At the time of analysis, 73 patients (62%) in the resection group had relapsed or died, as compared with 37 patients (82%) in the group treated by local tumour ablation. Disease free survival at 2 and 5 years in the resection group was 43 and 32%, respectively, in the group treated by local tumour ablation these figures were 17 and 11%, respectively (Fig. 3Go). Median disease free survival in the resection group was 18 months (95% CI 13–23 months) as compared with 9 months (95% CI 3–15 months) in the group treated by local tumour ablation (P < 0.001).


Figure 3
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  		FIG. 3. Kaplan–Meier analysis of disease free survival. According to treatment group.

 
The distribution of the first site of recurrence was similar in both groups (Fig. 4Go). Most recurrences occurred elsewhere in the liver outside the treated area or at extrahepatic sites. In the group treated by local tumour ablation, five patients developed a local recurrence at the ablated site (11%), compared with one patient that showed local recurrence at the resection site after resection (0.9%) (P < 0.004). Analysed on a lesion basis, local recurrence after local tumour ablation was 4.1%. Six lesions (in five patients) out of 146 lesions treated by local tumour ablation showed a local recurrence.


Figure 4
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  		FIG. 4. Site of primary recurrence according to treatment group.

 
None of the patients that were initially treated by chemotherapy or ablation underwent secondary resection of the liver metastases. After chemotherapy, in 2 out of the 39 patients complete response was observed without any surgical intervention afterwards

Health-Related Quality of Life
In total 109 patients participated in the Health-related quality of life (HRQoL) analysis. At baseline, the resection group consisted of 53 patients, the local ablation group of 29 patients and the chemotherapy group of 27 patients. At baseline the mean total scores in the different groups were similar. Figure 5Go presents the HRQoL as measured by the EQ-5D VAS score and the EORTC physical functioning score. The latter comprises an objective score on physical functioning while the EQ-5D VAS score represents overall HRQoL from the patient perspective. Both scores show a clear decrease 3 weeks after operation compared to baseline. Three months after operation, patients treated with local tumour ablation and resection returned to baseline levels. For patients treated by chemotherapy, HRQoL scores on EQ-5D VAS and on EORTC QLQ physical functioning remained lower as compared with the two other groups until the end of the assessment (12 months). For both scores, the difference between the local ablation group and the chemotherapy group was statistically significant (P < 0.05) on all time points, except for the first time point after surgery (3 weeks). Other HRQoL scores showed an identical pattern to the EQ-5D VAS score and the EORTC physical functioning score (data not shown).


Figure 5
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  		FIG. 5. EQ-5D VAS (patients’ perspective) scores and EORTC QLQ physical functioning scores. (Statistical significance between the groups local ablation and chemotherapy are depicted by "asterisk").

 
During the first year after laparotomy, the number of QALYs generated for the resection, the local ablation and the chemotherapy groups were 283, 317 and 165, respectively (expressed in days in full health instead of years). For the chemotherapy group the number of QALY-days was significantly lower in comparison with the other two groups (P < 0.01).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENT AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the present study we evaluated the efficacy of local tumour ablation in patients with non-resectable colorectal liver metastases. Within the limitations of the study design, in a group of patients with non-resectable colorectal liver metastases and comparable prognostic parameters, we observed a trend towards improved survival for the treatment with local tumour ablation compared to treatment with chemotherapy, although this difference was statistically not significant. In patients treated by local tumour ablation median overall survival was 31 months, compared with 26 months for patients treated by chemotherapy. In this well-defined patient population treated by local tumour ablation without subsequent chemotherapy, median disease free survival was 9 months. After local tumour ablation, HRQoL scores were restored to baseline values within 3 months after the procedure, while the number of QALYs gained was substantially higher in the local ablation group compared with the chemotherapy group. These data are suggestive for a beneficial effect of local tumour treatment in patients with non-resectable disease.

Within this study we complied with the widely accepted definition of surgical resectability of colorectal liver metastases, defined as essentially any number of metastases (unibilobar) as long as not more than 70% of liver needs to be removed.26 Only patients who did not fulfil these requirements were treated by local tumour ablation or chemotherapy. The decision to perform either local tumour ablation or chemotherapy was taken only on the basis of technical feasibility to perform local tumour treatment. In this way, we defined the best possible control group for local tumour ablative therapy. Patient characteristics, tumour load and the prognostic scores of the patients treated by local tumour ablation were fully identical to the group treated by chemotherapy. Moreover, patients treated by local tumour ablation did not receive subsequent chemotherapy until non-resectable recurrent disease was observed.

Our data on overall survival after resection or local tumour ablation are comparable to others. Five-year survival rates after resection of colorectal liver metastases has been reported between 35 and 50%.2,3,5 Studies on long term survival after local tumour ablation, either by radiofrequency or cryo-ablation, report 4 year overall survival rates varying from 25 to 35%,10,12,18,19,27 with a median overall survival between 29 and 35 months. These results are mainly dependent on the number and size of the lesions treated rather than on the technique used.11,27,28,29,30,31

To our knowledge only one other study has made a direct comparison between results of local tumour ablation and chemotherapy.10 In this study by Abdalla et al.,10 radiofrequency of colorectal liver metastases was compared with chemotherapy in patients not eligible for surgical treatment at laparotomy. Survival after radiofrequency was significantly better than for chemotherapy but survival curves of radiofrequency and chemotherapy were converging and the authors questioned whether with longer follow up and with better chemotherapy the advantage would sustain. Our results demonstrate that in patients treated with local tumour ablation, without subsequent chemotherapy, a median disease free survival of 9 months is obtained. It is likely that such preferential effect of local tumour ablation on overall survival will continue to sustain even with improvements in systemic chemotherapy.

For patients treated within the chemotherapy, the median overall survival was 26 months. This figure is obviously biased by the fact that it concerns a group of patients with better prognostic factors compared to the general population of patients with advanced colorectal cancer, i.e. limited hepatic metastases without extrahepatic involvement. Although it is likely that more recent forms of chemotherapy may further improve the results in these patients, it should be realized that these improvements will also apply for patients treated by local ablation once these patient show recurrence of disease. The impact of chemotherapy given after recurrence of disease may even be substantial, given the marked difference between the median disease free survival (9 months) and the median overall survival (31 months) after local tumour ablation.

Ten percent of the patients treated by local tumour ablation showed local recurrence at the site of treatment. This is in agreement with literature in which local recurrence rates vary from 0 to 50%.10,14–16,21,22,27,31,32 On a lesion basis, only 4.1% of the lesions treated by local ablation showed local recurrence. This low percentage may well be due to the fact that 95% of the lesions treated were smaller than 4 cm. It has well been described that local tumour ablation by either radiofrequency or cryoablation is far less efficient for lesions larger than 3–4 cm.12,31,33 Although technical advances are rapidly evolving, it seems reasonable with the present equipment to limit local tumour destruction to tumours smaller than 4 cm.

Worldwide there is a fast and growing interest for the use of local ablative techniques in patients with colorectal liver metastases. Conclusive evidence is, however, still remarkably weak for the large scale on which these procedures are used at present. Only one randomized trial is currently being performed investigating the effcacy of radiofrequency for the treatment of unresectable colorectal liver metastases. In this EORTC study (CLOCC) overall survival after radiofrequency plus chemotherapy is compared with chemotherapy alone. Advocates of radiofrequency ablation often criticize such randomized studies pointing to the successful results of radiofrequency with regard to local tumour control. In the present study we were able to identify two comparable patients groups that were either treated by chemotherapy or by local tumour ablative therapy. We show that for patients with unresectable colorectal liver metastases, the advantages of local tumour control by radiofrequency may be subtle and may not inevitably lead to large and significant differences in overall survival. This observation strongly underlines the urge for randomized trials, especially at a time when purchases of health care are looking for evidence based therapy. In the absence of data from such randomized controlled trials, we provide the best evidence possible on the effcacy of local tumour ablative therapy in patients with non-resectable colorectal liver metastases.


   FOOTNOTES
 
Paul F.M. Krabbe and Cornelis J.A. Punt equally contributed to this study.

Received for publication September 28, 2006. Accepted for publication November 15, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENT AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Fernandez FG, Drebin JA, Linehan DC, Dehdashti F, Siegel BA, Strasberg SM. Five-year survival after resection of hepatic metastases from colorectal cancer in patients screened by positron emission tomography with F-18 fluorodeoxyglucose (FDG-PET). Ann Surg 2004; 240(3):438–47.[CrossRef][Medline]
  2. Fong Y, Cohen AM, Fortner JG, Enker WE, Turnbull AD, Coit DG, et al. Liver resection for colorectal metastases. J Clin Oncol 1997; 15(3):938–46.[Abstract/Free Full Text]
  3. Nordlinger B, Guiguet M, Vaillant JC, Balladur P, Boudjema K, Bachellier P, 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(7):1254–62.[CrossRef][Medline]
  4. Ruers T, Bleichrodt RP. Treatment of liver metastases, an update on the possibilities and results. Eur J Cancer 2002; 38(7):1023–33.[CrossRef][Medline]
  5. Minagawa M, Makuuchi M, Torzilli G, Takayama T, Kawasaki S, Kosuge T, 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):487–99.[CrossRef][Medline]
  6. Goldberg RM, Sargent DJ, Morton RF, Fuchs CS. Ramanathan RK, Williamson SK, et al. A randomized controlled trial of fluorouracil plus leucovorin, irinotecan, and oxaliplatin combinations in patients with previously untreated metastatic colorectal cancer. J Clin Oncol 2004; 22(1):23–30.[Abstract/Free Full Text]
  7. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 2004; 350(23):2335–42.[Abstract/Free Full Text]
  8. Punt JCA. New options and old dilemmas in the treatment of patients with advanced colorectal cancer. Ann Oncol 2004; 15:1453–59.[Abstract/Free Full Text]
  9. Folprecht G, Grothey A, Alberts S, Raab HR, Kohne CH. Neoadjuvant treatment of unresectable colorectal liver metastases: correlation between tumour response and resection rates. Ann Oncol 2005; 16:1311–9.[Abstract/Free Full Text]
  10. Abdalla EK, Vauthey JN, Ellis LM, Ellis V, Pollock R, Broglio KR, et al. Recurrence and outcomes following hepatic resection, radiofrequency ablation, and combined resection/ablation for colorectal liver metastases. Ann Surg 2004; 239(6):818–25.[CrossRef][Medline]
  11. Adam R, Hagopian EJ, Linhares M, Krissat J, Savier E, Azoulay D, et al. A comparison of percutaneous cryosurgery and percutaneous radiofrequency for unresectable hepatic malignancies. Arch Surg 2002; 137(12):1332–9.[Abstract/Free Full Text]
  12. Berber E, Pelley R, Siperstein AE. Predictors of survival after radiofrequency thermal ablation of colorectal cancer metastases to the liver: a prospective study. J Clin Oncol 2005; 23(7):1358–64.[Abstract/Free Full Text]
  13. Bilchik AJ, Faries M. Radiofrequency ablation of hepatic malignancies: inexpensive and minimally invasive but should it replace resection? Ann Surg Oncol 2003; 10(9):1002–4.[Free Full Text]
  14. Bleicher RJ, Allegra DP, Nora DT, Wood TF, Foshag LJ, Bilchik AJ. Radiofrequency ablation in 447 complex unresec-table liver tumors: lessons learned. Ann Surg Oncol 2003; 10(1):52–8.[Abstract/Free Full Text]
  15. Bowles BJ, Machi J, Limm WM, Severino R, Oishi AJ, Furumoto NL, et al. Safety and efficacy of radiofrequency thermal ablation in advanced liver tumors. Arch Surg 2001; 136(8):864–9.[Abstract/Free Full Text]
  16. Pawlik TM, Izzo F, Cohen DS, Morris JS, Curley SA. Combined resection and radiofrequency ablation for advanced hepatic malignancies: results in 172 patients. Ann Surg Oncol 2003; 10(9):1059–69.[Abstract/Free Full Text]
  17. Poston GJ. Radiofrequency ablation of colorectal liver metastases: where are we really going? J Clin Oncol 2005; 23(7):1342–4.[Free Full Text]
  18. Ruers TJ, Joosten J, Jager GJ, Wobbes T. Long-term results of treating hepatic colorectal metastases with cryosurgery. Br J Surg 2001; 88(6):844–9.[CrossRef][Medline]
  19. Seifert JK, Junginger T, Morris DL. A collective review of the world literature on hepatic cryotherapy. J R Coll Surg Edinb 1998; 43(3):141–54.[Medline]
  20. Mulier S, Mulier P, Ni Y, Miao Y, Dupas B, Marchal G, et al. Complications of radiofrequency coagulation of liver tumours. Br J Surg 2002; 89(10):1206–22.[CrossRef][Medline]
  21. de Baere T, Elias D, Dromain C, Din MG, Kuoch V, Ducreux M, et al. Radiofrequency ablation of 100 hepatic metastases with a mean follow-up of more than 1 year. AJR Am J Roentgenol 2000; 175(6):1619–25.[Abstract/Free Full Text]
  22. Solbiati L, Livraghi T, Goldberg SN, Ierace T, Meloni F, Dellanoce M, et al. Percutaneous radio-frequency ablation of hepatic metastases from colorectal cancer: long-term results in 117 patients. Radiology 2001; 221(1):159–66.[Abstract/Free Full Text]
  23. Dolan P. Modeling valuations for EuroQol health states. Med Care 1997; 35(11):1095–108.[CrossRef][Medline]
  24. Pham B, Cranney A, Boers M, Verhoeven AC, Wells G, Tugwell P. Validity of area-under-the-curve analysis to summarize effect in rheumatoid arthritis clinical trials. J Rheumatol 1999; 26(3):712–6.[Medline]
  25. 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(3):309–18.[CrossRef][Medline]
  26. Alberts S. "OncoSurge: a strategy for long-term survival in metastatic colorectal cancer. Poston G Colorectal Dis 2005; 5:20–28.
  27. Bilchik AJ, Wood TF, Allegra D, Tsioulias GJ, Chung M, Rose DM, et al. Cryosurgical ablation and radiofrequency ablation for unresectable hepatic malignant neoplasms: a proposed algorithm. Arch Surg 2000; 135(6):657–62.[Abstract/Free Full Text]
  28. Joosten J, Jager G, Oyen W, Wobbes T, Ruers T. Cryosurgery and radiofrequency ablation for unresectable colorectal liver metastases: a comparison of long term results. Eur J Surg Oncol 2005; August 26.
  29. Pearson AS, Izzo F, Fleming RY, Ellis LM, Delrio P, Roh MS, et al. Intraoperative radiofrequency ablation or cryoablation for hepatic malignancies. Am J Surg 1999; 178(6):592–9.[CrossRef][Medline]
  30. Benoist S, Nordlinger B. Radiofrequency ablation in liver tumors. Ann Oncol 2004; 15(suppl iv):313–7.
  31. Mulier S, Ni Y, Jamart J, Ruers T, Marchal G, Michel L. Local recurrence after hepatic radiofrequency coagulation: multivariate meta-analysis and review of contributing factors. Ann Surg 2005; 242(2):158–71.[CrossRef][Medline]
  32. Adam R, Akpinar E, Johann M, Kunstlinger F, Majno P, Bismuth H. Place of cryosurgery in the treatment of malignant liver tumors. Ann Surg 1997; 225(1):39–8.[CrossRef][Medline]
  33. Seifert JK, Junginger T. Prognostic factors for cryotherapy of colorectal liver metastases. Eur J Surg Oncol 2004; 30(1):34–40.[CrossRef][Medline]



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