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10.1245/s10434-007-9388-6
Annals of Surgical Oncology 14:2069-2077 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Systematic Review on Safety and Efficacy of Repeat Hepatectomy for Recurrent Liver Metastases from Colorectal Carcinoma

Tristan D. Yan, BSc(Med), MBBS1, Junyang Sim, BSc(Med)1, Deborah Black, BSc, DipEd, MStat, PhD2, Rui Niu, BSc(Med)3 and David L. Morris, MD, PhD1

1 Department of Surgery, University of New South Wales, St George Hospital, Sydney, NSW, Australia
2 School of Public Health and Community Medicine, University of New South Wales, Sydney, NSW, Australia
3 School of Medicine, University of New South Wales, Sydney, NSW, Australia

Correspondence: Address correspondence and reprint requests to: David L. Morris, MD, PhD; E-mail: david.morris{at}unsw.edu.au


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We critically appraised the quantity and quality of current clinical evidence to demonstrate the efficacy and safety of repeat hepatectomy for recurrent colorectal liver metastases (CRLM).

Methods: Electronic searches for relevant studies published in peer-reviewed medical journals on repeat hepatectomy for recurrent CRLM before January 2007 were performed on six databases. The quality of each included study was independently assessed. Clinical effectiveness was synthesized through a narrative review with full tabulation of results of all included studies.

Results: Seventeen studies with more than 20 patients were included for quality appraisal and data extraction. All 17 included articles were observational cases series. The overall perioperative morbidity rate ranged from 7% to 30% and mortality rate varied from 0% to 5%. The overall median survival since the repeat hepatectomy ranged from 23 to 56 months, with 3- and 5-year survival of 24% to 68% and 21% to 49%, respectively. The median disease-free survival ranged from 9 to 52 months, with 3- and 5-year disease-free survival of 16% to 68% and 16% to 48%, respectively.

Conclusions: The current literature suggests that repeat hepatectomy is associated with a prolonged survival for recurrent CRLM and is justified in selected patients because there is a lack of evidence for effective alternative treatments.

Key Words: Hepatectomy • Liver resection • Recurrence • Colorectal cancer • Liver metastases


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Hepatectomy has been considered the standard of care for liver metastases from colorectal carcinoma, achieving 5-year survival in the range of 30% to 40%. On January 25, 2006, the American Hepato-Pancreato-Biliary Association convened a consensus conference on the management of colorectal liver metastases (CRLM).1 This conference was timely in bringing together experts in the field in an effort to consolidate current approaches to this disease. The consensus statements emphasized several important patient selection criteria, features affecting resectability and clinical evidence of regional therapy.1 At the same time, it was acknowledged that there have been only modest prospective clinical trial efforts in this population to evaluate long-term benefits in disease-free and overall survival, as well as in patients who have undergone hepatectomy.

It is known that liver recurrence after hepatectomy is common and associated with a reduced survival if not treated aggressively. Liver recurrence may be related to the biological aggressiveness of the disease, inadequate resection margin as a result of technical failure, or in some situations, undetected occult hepatic disease at the time of initial surgery. The treatment for liver recurrence is not standardized and may vary from palliative systemic chemotherapy to aggressive repeat hepatectomy. The modern systemic chemotherapeutic regimens, with or without biological agents, have shown improved response rates in colorectal metastases.2–5 However, the long-term survival remains limited.

Many treatment centers advocate the use of repeat hepatectomy and have claimed that it is safe and that it has similar survival results to initial hepatectomy.6–43 The reported survival advantage may be directly related to the aggressive surgical approach, but it may also be partly the result of patient selection. Currently, the aggressive management remains controversial. The purposes of this study were to critically appraise the quantity and quality of current clinical evidence and demonstrate the efficacy and safety of repeat hepatectomy for recurrent CRLM.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Literature Search Strategy
Electronic literature searches were performed to identify all published peer-review medical articles on repeat hepatectomy for CRLM. The following electronic databases were searched from their inception until December 2006: Medline, PubMed, EMBASE, Cochrane Central Register of Controlled Trials, Cochrane Database of Systematic Reviews, and Database of Abstracts of Review of Effectiveness. The reference lists of all retrieved articles were manually searched for further identification of potentially relevant studies. All relevant articles identified were assessed with application of selection criteria.

Selection Criteria
Experimental and observational studies that used repeat hepatectomy for recurrent CRLM with a curative intent were searched for inclusion. Studies were classified into four levels of evidence, as follows: level 1, randomized controlled trials; level 2, controlled clinical trials; level 3, observational studies with matched control groups; and level 4, observational case series. Because randomized trials comparing repeat hepatectomy versus a nonsurgical approach have never been attempted, all relevant prospective and retrospective series reporting the outcomes of repeat hepatectomy with curative intent for recurrent CRLM were included. All studies selected were human trials published in English. Studies that included other liver cancer diagnoses when reporting aggregate outcomes were excluded. Abstracts, letters, editorials, and expert opinions were excluded. Studies reporting the effectiveness of ablative techniques, be it cryotherapy or radiofrequency for recurrent CRLM, were excluded. It is acknowledged that all of the studies included in the present review aimed to demonstrate the efficacy of hepatectomy for recurrent CRLM. However, a few studies also used additional ablative techniques for a few patients whose disease cannot be completely resected. It is acknowledged that it is impossible to isolate the data on just hepatectomy in these studies.

Data Extraction and Critical Appraisal
To ensure that the series reviewed reflect consistent surgical approach and supportive care, only articles reporting the outcomes of at least 20 patients were included for qualitative appraisal and efficacy assessment. When centers have published studies with accumulating numbers of patients or increased lengths of follow-up, only the most recent and complete reports were included for qualitative appraisal and efficacy assessment. Two investigators (one clinical [T.D.Y.] and one nonclinical [J.S.]) independently reviewed each included article by means of a critical appraisal checklist. Discrepancies between the two reviewers were resolved by discussion and consensus. The final results were reviewed by two senior investigators (one clinical [D.L.M.] and one nonclinical [D.B.]).

For the purpose of this review, nine items relevant to the quality appraisal for uncontrolled case series were combined from two check lists,44,45 to determine whether (1) the objective of the study was clearly described; (2) the priori inclusion criteria were explicitly described; (3) the patient characteristics included in the study were clearly described; (4) the distribution of the principal confounders were clearly described; (5) the patients in the study were representative of the target population; (6) the patients were at a similar stage of disease progression at the time of treatment; (7) the main outcomes to be measured were clearly defined and objective; (8) the length of follow-up was reported; and (9) additional surgical procedures were performed in the study.

The outcomes were searched for morbidity, mortality, hospital stay, survival (median, 1-, 2-, 3-and 5-year survival), disease-free survival (median, 1-, 2-, 3- and 5-year survival), disease status, quality of life, and cost effectiveness. Survival and disease-free survival were determined from the time of repeat hepatectomy. A meta-analysis was not appropriate because all studies lack a comparator. All data were extracted from the relevant articles’ texts, tables, and figures. Clinical effectiveness was synthesized through a narrative review with full tabulation of results of all included studies.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Quantity of Evidence
Initial electronic searches identified 642 references. After exclusion of duplicate or irrelevant references, 114 potentially relevant abstracts were obtained for assessment. As a result, 48 potentially relevant publications were retrieved for further evaluation. Manual search of the reference lists identified another six potentially relevant publications. When the selection criteria were applied to all 54 publications, 38 articles remained for assessment (Table 1Go).6–43 Seventeen studies comprising a total of 1049 patients were included for quality appraisal and data extraction.12,15,17,18,21,23,29,32–35,37,39–43 Nineteen studies involving a total of 209 patients were excluded because the number of patients in each study was fewer than 20 (median, 10; range 8–16).6–11,13,14,16,19,20,22,25,27,28,30,31,36,38 Two studies of an earlier publication from the same institution was also excluded.24,26


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  		TABLE 1. Summary of outcomes reported in 38 relevant publications on repeat hepatectomy for recurrent colorectal liver metastases
 
Of the included 17 studies, five studies had more than 100 patients, including two multi-institutional studies,17,18 one bi-institutional study,33 and two single-institutional studies.35,43 Two studies had more than 50 but fewer than 100 patients.41,42 The remaining 10 studies had fewer than 50 patients.12,15,21,23,29,32,34,37,39,40

Quality of Evidence
All 17 included articles were case series without control groups and were classified as level 4 evidence (Table 2Go).12,15,17,18,21,23,29,32–35,37,39–43 No prior systematic review or meta-analysis on this topic was identified. Study objectives were clearly described in all studies.12,15,17,18,21,23,29,32–35,37,39–43 The priori inclusion criteria were explicitly described in 12 studies.17,21,23,29,32,34,35,37,40–43 The patient characteristics were clearly described in 14 studies.12,15,17,18,21,23,29,33,35,39–43 The distribution of the principal confounders was clearly described in 16 studies.15,17,18,21,23,29,32–35,37,39–43 The patients in the study were representative of the target population in all studies, except one study mainly reported patients undergoing third-time hepatectomy, with the outcomes of second hepatectomy separately analyzed.35 Four studies included patients with intra-hepatic recurrence only15,34,39,42; 12 studies included patients with extrahepatic metastases,12,17,18,21,29,32,33,35,37,40,41,43 and the stage of disease at the time of repeat hepatectomy was not specified in one.23 Sixteen studies reported morbidity results.15,17,18,21,23,29,32–35,37,39–43 All studies reported mortality and survival results. Seven studies reported disease-free survival results.12,15,23,32,34,37,39 Eight studies reported disease status after repeat hepatectomy.12,15,17,29,32,33,39,43 Fourteen studies reported the length of follow-up.12,15,17,18,21,33–35,37,39–43 Additional surgical procedures were performed in five studies, mainly cryoablation in addition to hepatectomy for a minority of patients with unresectable disease.15,32,33,42,43


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  		TABLE 2. Results of quality assessment in 17 studies with more than 20 patients undergoing repeat hepatectomy for recurrent colorectal liver metastases
 
Assessment of Morbidity and Mortality
Table 3Go demonstrated the morbidity and mortality results of each included study. The overall perioperative morbidity rate ranged from 7% to 30% (median, 22%), and mortality rate varied from 0% to 5% (median, 0).12,15,17,18,21,23,29,32–35,37,39–43 The rates of intra-abdominal abscess, wound infection, bile leak, hepatic failure, and pleural effusion ranged from 2.4% to 8%,15,17,21,23,29,33,35,40,42,43 .9% to 11%,15,33,34,39,42,43 .8% to 10%,15,17,21,29,33–35,39,40,42,43 0% to 4.5%,15,17,32–34,41,42 and 2.4% to 9.5%,15,17,29,32,33,35,39,40,42,43 respectively. The median blood loss varied from 450 to 913 mL23,33,41,43 and the mean transfusion requirement was .5 to 2.7 units.35,37,42 Three studies reported operation duration, which ranged from 5 and 9.5 hours.29,37,40 The duration of hospital stay ranged from 8 to 22 days (median, 12 days).15,21,29,32,33,35,37,41


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  		TABLE 3. Assessment of morbidity and mortality on repeat hepatectomy for recurrent colorectal liver metastases
 
Assessment of Survival
Table 4Go lists the effectiveness of repeat hepatectomy on survival of patients with recurrent CRLM. The median and mean follow-up after repeat hepatectomy were 19 to 59 months12,15,18,33,34,37,39–43 and 20 to 25 months,17,21,35 respectively. The overall median survival since initial hepatectomy (OS1) was 26 to 73 months, as reported in seven studies.15,33,34,39–42 The overall median survival since the repeat hepatectomy (OS2) ranged from 23 to 56 months, with 1-, 2-, 3-, and 5-year survival of 77% to 100%, 52% to 89%, 24% to 68%, and 21% to 49%, respectively.12,15,17,18,21,23,29,33–35,39–43


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  		TABLE 4. Assessment of survival on repeat hepatectomy for recurrent colorectal liver metastases
 
Significant Prognostic Factors for Survival
Several statistically significant prognostic factors have been shown to be associated with an improved survival outcome after repeat hepatectomy. Factors related to initial hepatectomy included the following: low serum carcinoembryonic antigen levels (<50 ng/mL34 or <5 ng/mL40,42); small liver metastases (≤ 4 cm)42; complete initial hepatectomy42; long disease-free interval between initial and repeat hepatectomy (>6 months29,43 or >12 months39,42), and absence of vessel invasion.43 Factors related to repeat hepatectomy included the following: absence of extrahepatic disease at the time of repeat hepatectomy,18 complete repeat hepatectomy,18,42 low serum carcinoembryonic antigen levels (≤30 ng/mL32 or ≤5 ng/mL42), solitary lesion,32,33,43 and small recurrence lesions (≤5 cm).33,40

Assessment of Disease Recurrence
Table 5Go lists the effectiveness of repeat hepatectomy on disease-free survival of patients with recurrent CRLM. The median disease-free survival ranged from 9 to 52 months, with 1-, 2-, 3-, and 5-year disease-free survival of 39% to 85%, 21% to 81%, 16% to 68%, and 16% to 48%, respectively.12,15,23,32,34,37,39 Twenty-four percent to 48% of patients had no evidence of disease, as reported in seven studies.15,17,29,32,33,39,43 Eight percent to 28% of patients were alive with disease, as reported in five studies.15,32,33,39,43 Thirty-eight percent to 56% of patients died from disease, as reported in six studies.12,15,32,33,39,43 After repeat hepatectomy, the rates of disease recurrence in the liver and at an extrahepatic site were 15% to 67%12,15,17,23,32–34,37,42,43 and 27% to 64%,12,15,17,23,33,34,42,43 respectively. No studies on quality of life and cost effectiveness were identified.


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  		TABLE 5. Assessment of disease recurrence on repeat hepatectomy for recurrent colorectal liver metastases
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Although there are no randomized trials comparing the efficacy of hepatectomy with systemic chemotherapy, hepatectomy has been recognized as the standard of care in the management of CRLM, with a superior long-term survival of 30% to 40%, when compared with historical controls in unresected patients.1 The modern systemic chemotherapy regimens with or without biological agents have been associated with improved response rates (approximately 50%) and achieved median survival of 20 months in patients with colorectal metastases.2–5 However, the long-term survival after chemotherapy alone remains limited. Recently, advances in chemotherapy have allowed resection in 10% to 30% of patients with initially unresectable disease.46–48 It is estimated that 50% to 70% of patients will experience recurrent disease after initial hepatectomy and isolated liver recurrences accounts for approximately 25% to 30% of these surgical treatment failures.6,18,24,49 Management of hepatic recurrence has been a continuous challenge for liver surgeons. It is important to note that there is a lack of data on the efficacy of modern systemic chemotherapy specifically for patients with recurrent CRLM in the current literature.

Given the localized nature of the recurrent disease in selected patients and the regenerative capacity of the liver, several centers have advocated an aggressive surgical approach to hepatic recurrence. In 1994, Que and Nagorney12 published the first report on more than 20 patients who underwent repeat hepatectomy. They demonstrated a median survival of 41 months and 4-year survival of 43%, with no marked morbidity and mortality.12 These results were surprising and nearly identical to the results of patients undergoing initial hepatectomy. In 1994, a multi-institutional study from the Association Francaise de Chirurgie showed a median survival of 30 months, 3-year survival of 33%, morbidity rate of 25%, and mortality rate of .9%, after repeat hepatectomy.17 Nearly at the same time, another multi-institutional study involving 170 patients from 20 international centers demonstrated similar treatment outcomes.18 Subsequently, several single-institutional studies with accumulative numbers of patients also reported consistent results.19–43 These data suggest that repeat hepatectomy seems justified because surgical resection remains the only potentially curative treatment, with acceptable morbidity and mortality, and because of a lack of effective alternatives to treat recurrence of disease in the liver.

In the present systematic review, a quantitative and qualitative assessment of the published series was performed to summarize the available clinical evidence for the effectiveness and safety of repeat hepatectomy. Thirty-eight relevant articles were identified.6–43 Seventeen reports with more than 20 patients were included for appraisal and data extraction.12,15,17,18,21,23,29,32–35,37,39–43 Repeat hepatectomy of liver recurrence can be performed safely in most patients. The overall perioperative morbidity rate ranged from 7% to 30%, and mortality rate varied from 0% to 5%. Repeat hepatectomy is more technically challenging than initial resection because of problems with reexposure of the liver, the friable regenerated liver parenchyma, and the postchemotherapy changes. However, on the basis of the reported data, the incidence of bile leak and hepatic failure and the transfusion requirement were similar to initial hepatectomy. Several studies compared their perioperative outcomes after initial and repeat hepatectomy and did not find any statistically significant difference.24,32,34,35,37,40 No studies have presented information on recovery of patients’ functional status or quality of life after discharge.

The overall median survival since the repeat hepatectomy ranged from 23 to 56 months, with 5-year survival of 21% to 49%. The median disease-free survival ranged from 9 to 52 months, with 5-year disease-free survival of 16% to 48%. It seems that these results are not different from that of initial hepatectomy. Several studies showed that there was no marked difference in survival after the initial and repeat hepatectomy.17,24,34,35,37,39,40,42 One relatively large series also demonstrated similar efficacy of third-time hepatectomy.35 This may be related to reselection of patients to undergo a potentially curative treatment in an already selected group of patients. Perhaps the most important thing in first, second, and even third liver resections is complete cytoreduction.18,21,26 Twelve of the 17 studies included patients with extrahepatic metastases.12,17,18,21,29,32,33,35,37,40,41,43 Although the current clinical evidence is immature, it suggests that the presence of extrahepatic disease should be not be regarded as an absolute contraindication to repeat resection provided the patient is carefully selected and a complete cytoreduction can be potentially achieved. The rationale for resection of resectable extrahepatic disease has been based on the lack of nonsurgical curative therapies.

It seems clear that acceptable benefits in terms of long-term survival were achieved with repeat hepatectomy. However, these results should be interpreted with caution for several reasons. First, all reports were case series, and the overall level of clinical evidence is low. Surgical resection and non-surgical management have not been compared directly, but it would be difficult to recruit patients to compare a potentially curative treatment versus a palliative approach with no evidence of long-term survival. Second, all studies focused on carefully selected patients, whereas in reality, most patients with recurrent disease may not be amenable to surgery. Patients undergoing surgery may have a better prognosis than others with metastatic colorectal cancer because their disease is confined to the liver and the patients are more likely to be of good performance status. Although complete agreement regarding selection criteria has not occurred, consensus for initial hepatectomy may also apply to repeat hepatectomy. Currently, most liver surgeons support consideration of hepatectomy in patients, whereby a margin-negative resection is achievable, with preservation of two contiguous hepatic segments and >20% functional liver remnant, sufficient vascular supply, and biliary drainage.50 Fourth, considering these reports over a 15-year period, it is important to realize that the results were influenced by the temporal factor and treatment bias. There have been evolutions of the treatment plans and increased surgical aggressiveness over the study period. The treatment protocols vary among the institutions. Recent strategies, including the use of positron emission tomography in selection of surgical patients, neoadjuvant chemotherapy for tumor downstaging, preoperative portal vein embolization to induce hypertrophy of the liver remnant, and additional ablative techniques for marginal nonsurgical candidates may allow complete resection in patients that in years past would have been considered unresectable. The impact of these technical advances in the treatment of liver recurrence with repeat hepatectomy has yet to be determined.

Radiofrequency ablation and cryotherapy are locoregional ablative techniques that have been used in selected nonsurgical candidates.51–54 The recurrence rates after these ablative techniques are higher than with hepatectomy. At present, ablative techniques are used not as an alternative but as an adjunct to hepatectomy for CRLM. However, in the management of local recurrence, as a result of the less invasive nature of ablative techniques, some authors have reported that percutaneous radiofrequency ablation may increase the scope of patients eligible for a curative intent treatment and have suggested that repeat hepatectomy is indicated only when percutaneous radiofrequency ablation is contraindicated or fails.55 The role of neoadjuvant and adjuvant systemic chemotherapy in patients undergoing repeat hepatectomy for liver recurrence is not well defined. The use and timing of these therapies should be individualized and planned as part of a multidisciplinary approach.

In this systematic review, two multi-institutional, one bi-institutional, and 14 single-center observational studies were evaluated. The current literature suggests that repeat hepatectomy is associated with a prolonged survival for recurrent CRLM and is justified in selected patients because there is a lack of evidence for effective alternative treatments.

Received for publication January 6, 2007. Accepted for publication February 7, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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