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Ann Surg. Jun 2002; 235(6): 863–871.
PMCID: PMC1422517

Second Liver Resections Are Safe and Effective Treatment for Recurrent Hepatic Metastases from Colorectal Cancer

A Bi-institutional Analysis



To determine the value of repeat liver resection for recurrent colorectal metastases to the liver.

Summary Background Data

Liver resection represents the best and a potentially curative treatment for metastatic colorectal cancer to the liver. After resection, however, most patients develop recurrent disease, often isolated to the liver.


This study reports the combined experience of repeat liver resection for recurrent liver metastases at an American and a European surgical oncology center. Patients were identified from prospective databases and records were retrospectively reviewed. A total of 126 patients (American n = 96, 1986–2001; European n = 30, 1985–1999) underwent repeat liver resection. Patient characteristics were similar in the two institutions. Median follow-up from first liver resection was 88 and 105 months, respectively.


Operations performed included 90 minor resections and 36 resections of a lobe or more. The 1-, 3-, and 5-year survival rates were 86%, 51%, and 34%. There were 19 actual 5-year survivors to date. By multivariate regression analysis (proportional hazard model), more than one lesion and tumor size larger than 5 cm were independent prognostic indicators of reduced survival. The interval between the first and second liver resection was not predictive of outcome.


Repeat liver resection for colorectal liver metastases is safe. Patients with a low tumor load are the best candidates for a repeat resection. In well-selected patients, further resection of the liver can provide prolonged survival after recurrence of colorectal liver metastases.

The liver is the most common organ of distant metastases from colorectal cancer. 1 Untreated patients with hepatic colorectal metastases have a poor prognosis, with a median survival of 6 to 12 months. 2,3 Chemotherapy modestly extends median survival to 12 to 18 months, but cure remains unlikely. 4,5 In contrast, surgical resection of liver metastases from colorectal cancer can offer long-term survival and cure in patients with metastatic colorectal cancer isolated to the liver. Five- and 10-year survival rates of 25% to 39% and 22% to 23% after hepatectomy 6–13 have been reported. Therefore, liver resection currently represents the best and a potentially curative treatment for hepatic colorectal metastases.

Unfortunately, 60% to 70% of patients undergoing liver resection for colorectal liver metastases will develop recurrence of the disease. 6,13 Of these, one third will have recurrent metastases isolated to the liver. Since liver resection has become safer through improvements in surgical techniques and perioperative management, repeat hepatic resection is being more frequently performed in patients with isolated hepatic recurrence. 14 Several studies on repeat hepatic resection have been reported during the past decade. 15–25 Most are small, single-institution studies. The purpose of this bi-institutional study was to determine the value of repeat liver resection for recurrent colorectal metastases to the liver.


The present report is the combined experience of repeat liver resection for recurrent liver metastases at an American (Memorial Sloan-Kettering Cancer Center, NY) and a European surgical oncology center (University of Frankfurt, Frankfurt, Germany). From 1985 to 2001, 1,362 patients underwent a first liver resection for colorectal metastases (New York n = 1,128, September 1986 to January 2001; Frankfurt n = 234, May 1985 to July 1999). One hundred twenty-six underwent a second liver resection for recurrent colorectal liver metastases (New York n = 96; Frankfurt n = 30). Follow-up was performed by personal contact with the patient, the patient’s family, or the attending or general physician. The median follow-up time from primary colon surgery was 88 (New York) and 105 months (Frankfurt).

Patients were identified from prospective databases, and office and hospital charts were retrospectively reviewed. Data analyzed included demographics, pathology of primary and metastatic disease, perioperative course of primary and metastatic disease, surgical and adjuvant treatment of primary and metastatic disease, and predictors of outcome and survival.

The extent of liver resection was classified according to the nomenclature by Goldsmith and Woodburne. 26 Wedge, segmental, and bisegmental resections were summarized as minor procedures; lobectomies and extended resections (trisegmentectomies) were considered major procedures. Liver involvement was classified as unilobar if liver metastases at the first and second hepatic resection were restricted to one lobe. The presence of tumor in both the right and left lobe at first or second resection was defined as bilobar involvement.

Survival probabilities were estimated using the Kaplan-Meier method. 27 Univariate associations between potential risk factors and survival were assessed using the log-rank test. Independent predictors of survival were determined using a proportional hazards regression model. 28


Patient Demographics and Follow-Up

Sixty-three men and 63 women underwent a second liver resection for colorectal metastases. The median age of patients at time of second liver resection was 62 years (range 34–82). Patient demographics were similar in the two institutions (median age 63 vs. 60 years; gender distribution 50% vs. 50% male) (Table 1).

Table thumbnail

At last follow-up, 28 patients (22%) were alive with no evidence of disease, 24 (19%) were alive with disease, 68 (54%) had died of disease, and 2 (2%) had died of other causes. Four patients (3%) were lost to follow-up. The median follow-up time from primary colonic surgery was 87.5 months. Median follow-up from the second liver resection was 58.8 months.

Pathology and Staging

The site of the primary lesion was colon in 100 patients (79%) and rectum in 26 patients (21%). Metastatic lesions in the liver were found synchronously with the primary tumor in 72 patients (Dukes stage D). Of the 43 patients with metachronous liver metastases, 22 had colorectal lymph node-negative disease (Dukes A and B) and 30 had lymph node-positive disease (Dukes C) at the time of primary surgery. Detailed information of the primary disease is listed in Table 2.

Table thumbnail

The median interval between the first and second liver resection was 13.8 months. Most of the patients had a solitary hepatic lesion at first and second liver resection (59% and 74%). The median size of the largest hepatic lesion was similar at first and second hepatic resection (3.0 vs. 3.0 cm). According to our definition, unilobar involvement was observed in 64 of 123 patients (52%) and bilobar involvement in 59 of 123 patients (48%). Three patients could not be classified due to missing data (Table 2).

Perioperative Course

The median blood loss during the second liver resection was 900 mL (range 15–7,500). Two patients (1.6%) died within 30 days, one from intraoperative bleeding and the other from a pulmonary embolus on the fifth postoperative day. Thirty-four complications occurred in 123 assessable patients (28%). Complications included liver-related complications (perihepatic abscess, n = 3; bile fistula, n = 1; liver failure, n = 1), infections (wound, n = 3; urinary tract, n = 2; sepsis, n = 1), and general complications (pleural effusion, n = 3; intraabdominal bleeding, n = 4; deep venous thrombosis, n = 1; pulmonary embolism, n = 1; fever, n = 10; other, n = 1). The median hospital stay for the second liver resection was 10.5 days (range 5–34).

Surgical and Adjuvant Treatment

Operations performed included 90 minor resections (28 wedge, 53 segmental, 5 left lateral segmentectomies, and 4 right posterior sectorectomies). Eight resections were performed using the cryo-assisted technique. 29 The 36 major resections included 8 left lobectomies, 13 right lobectomies, 3 left trisegmentectomies, and 12 right trisegmentectomies. A third liver resection was subsequently performed in 11 patients. Extrahepatic disease before the second liver resection was present in 19 of 126 patients (15%). Of these, three patients had local colorectal recurrence, nine had pulmonary metastases, and seven had other metastatic lesions. All of them underwent complete resection of extrahepatic local recurrent or metastatic foci.

Excluding the two perioperative deaths, data on adjuvant chemotherapy were available in 111 of 124 patients (90%). Of these, 47 patients (44%) did not receive chemotherapy after the repeat liver resection, whereas 60 patients (56%) did receive adjuvant chemotherapy (see Table 3).

Table thumbnail


Overall survival and survival of subgroups as calculated from time of second liver resection are shown in Figure 1. The actuarial survival rates at 1, 3, and 5 years were 86%, 51%, and 34% (Fig. 1A). The median overall survival was 37 months. There were 19 actual 5-year survivors (15%) at last follow-up. There was a significantly better survival for patients with solitary lesions (Fig. 1B) or with the largest lesion 5 cm or less (Fig. 1C). In further subgroup analysis, patients with solitary lesions and largest lesion 5 cm or less had the best survival (median 59.4 months). The other three groups had comparably worse, but similar to each other (median approximately 28 months), survival profiles. At least one of the survival curves (Fig. 1D) was significantly different from the others (P = .01).

Patterns of Recurrence After Second Liver Resection

The sites of recurrence after second liver resection are listed in Table 3. Of the patients with recurrence, 64% experienced recurrence involving extrahepatic sites, whereas 36% developed metastases isolated to the remnant liver. Liver (67%) and lung (43%) were the most common sites of recurrence.

Predictors of Outcome

A number of potential risk factors were considered, and after univariate analysis the following were taken forward to a multivariate model (Table 4): number of tumors in the first liver resection, number of tumors in the second resection, size of the largest tumor in the second resection, positive margins in the second resection, and bilobar involvement. Multivariate analysis identified two independent risk factors: number of lesions (P = .01) and size of the largest lesion (P = .04), both at the second resection. Patients who had multiple lesions at the second resection were at more than twice the risk of those who had solitary lesions (relative risk = 2.82). In addition, the presence of at least one lesion larger than 5 cm at the second operation doubled the risk of death (relative risk = 1.89). None of the variables related to the primary tumor or the first liver metastatic disease were significant predictors of outcome after the second resection.

Table thumbnail


Liver resection represents the best and only potentially curative treatment for metastatic colorectal cancer to the liver. Repeat liver resection for colorectal recurrence to the liver is increasingly performed due to recent advances in hepatic resection and growing evidence of survival benefit. 14,18,20,22,23 Because only 5% to 10% of patients who undergo liver resection will develop hepatic recurrence that is amenable to a further liver resection, experience and data on results after repeat resections are sparse. Therefore, most reports on repeat resections are based on small populations or on combined populations from many different institutions (Table 5). All are retrospective studies. The present study reports a large experience of 126 second liver resections for colorectal liver metastases from an American and a European surgical oncology center. Characteristics of patients from both institutions were similar: median age (63 vs. 60 years), gender distribution (50% vs. 50% male), and median time from first to second resection (13.8 vs. 13.5 months). This suggests that patient selection for second liver resections is similar in these two geographically disparate institutions. The current data also indicate that second liver resections are safe and effective in the treatment of recurrent metastatic disease.

Table thumbnail

Because repeat liver resections are technically more demanding and difficult, there was concern that re-resections may be associated with higher rates of death and complications than first resections. Most series report an in-hospital death rate of less than 5% for first hepatic resections. 6–13 Results of studies on repeat liver resection show a similar range of death rates compared with those reported for primary hepatic resections (see Table 5). The 30-day death and complications rates of 1.6% and 28% in our series are similar to those of other studies on repeat liver resection and are not significantly higher than those of first hepatic resections. This shows that patients selected for repeat liver resections have comparable perioperative risk to those undergoing first resections.

Five-year survival rates of 25% to 39% have been reported for first hepatic resections for colorectal liver metastases. Similar favorable 5-year survival rates can be achieved through repeat hepatic resection in well-selected patients with recurrent hepatic disease. 6–13,17,20–23,25 The median survival and 5-year survival rate of the current study are 37 months and 34% and are equivalent to that of initial hepatic resection. Therefore, liver resection has become the treatment of choice for primary and recurrent resectable liver metastases from colorectal cancer because neither chemotherapy nor other nonsurgical therapies can achieve such favorable results.

Several studies had attempted to find predictors of outcome that could identify patients with a favorable prognosis after repeat liver resection. The only two studies that identified independent prognostic parameters by multivariate analysis comes from a French and a Japanese hepatobiliary center. 22 Disease-free interval between the first and second liver resection and the curative nature of the second resection were associated independently with survival after second liver resection for recurrent colorectal liver metastases in the French study. Tumor number ≥ 4, positive lymph nodes, extrahepatic disease, and the curative nature of the second resection were prognostic variables in the Japanese study. 23 Interestingly, the presence of resectable extrahepatic disease did not influence survival in this multivariate analysis. In our study, we identified number (one vs. more than one) and largest tumor size (≤5 vs. >5 cm) of hepatic lesions as independent risk factors related to the second liver resection. Both of these are also established risk factors for recurrence after first liver resection. 13,30 Interestingly, no tumor factor related to the first resection predicted outcome after repeat resection. This is consistent with all previous studies on repeat liver resection, which failed to identify independent prognostic parameters of the initial metastatic liver disease by multivariate analysis. 15–25 Thus, in selecting patients for repeat resection, medical fitness, small solitary tumors, ability to clear all disease, and possibly disease-free interval are the most important criteria for consideration.

Recent technologic advances have also made ablative treatments for liver tumors, such as cryoablation or radiofrequency ablation, accessible and safe options for therapy. Certainly, in our practice, many patients with small central recurrences after a prior major liver resection are often treated by ablative therapy. These ablations can often be performed percutaneously, avoiding the complications associated with open surgery. Whether such ablations will be equivalent to resection for tumors that are easily resectable warrants direct clinical comparison with short-term complications as well as long-term cancer-related outcome as endpoints.

In conclusion, our data show that repeat hepatic resection for colorectal liver metastases is safe. Rates of death and complications and survival of second liver resection are similar to those of initial hepatic resection. Patients with a low tumor load (small number and size) are the best candidates for a re-resection. In well-selected patients, further resection of the liver can provide prolonged survival and is currently the treatment of choice after recurrence of resectable colorectal liver metastases.


Dr. Robert M. Beazley (Boston, MA): Dr. Fong and his coauthors have presented the treatment results of a highly selected group of colorectal cancer patients with recurrent liver metastases. Considering approximately 10% to 15% of patients with liver mets will be resectable initially, of those resected the authors found that only 8.5% could be successfully re-resected. Indeed, this is a highly selected population. Experience of this type and caliber could only come from a few centers in the world or a very large multi-institutional trial. I think Dr. Brennan is to be congratulated on having the vision to encourage and support the development of a unit at Memorial which is capable of doing this type of work. This paper clearly defines prognostic criteria, size and number of metastases, while demonstrating both a low mortality and morbidity. Additionally, I think it also suggests that such a re-resection resets the survival clock back to that of the original lesion. I have a few questions.

Dr. Fong, intuitively it seems that it would be of value to identify a liver recurrence as early as possible in your resection group. The reported interval between resections was 13.8 months. What was the follow-up protocol in those patients following their original resection. Have you any experience with some of the newer modalities, in particular PET scan, and what would be your opinion of that as a follow-up modality? Second, in the manuscript, 11 patients are reported to have had a third resection. What happened to this small, select group? Lastly, extrahepatic disease was noted in 15 individuals before re-resection. What was the ultimate outcome of this group? Did extrahepatic disease influence things one way or the other? Do you recommend resection of extrahepatic or extraabdominal metastases in patients who have had a liver resection? I guess the backside of that question is, what are the selection criteria for re-resection?

This year marks the 50th anniversary of the first successful right hepatectomy. The last couple of papers of yesterday’s program and this paper demonstrate that there are still questions to be answered in hepatic surgery. I think the Southern Surgical Association is to be congratulated on providing a forum for discussion of such questions. I certainly enjoyed your paper and appreciate the opportunity to comment on it.

Dr. J. Nicolas Vauthey (Houston, TX): The study presented by Dr. Fong and coauthors identified two predictors of survival after repeat resection (i.e., tumor number and tumor size). Importantly, the authors did not find that the interval between the first and the second resection was affecting subsequent survival. This is in contrast with two recent reports from Suzuki in Japan and from Adam in France reporting that re-resection within 6 or 12 months after the first resection affects prognosis. The absence of significance of the interval variable, which is important regarding decision-making, may reflect the proper selection of patients for re-resection at two cancer institutions. Alternatively, it may reflect the fact that most of the first resections were, in fact, incomplete resections that were not performed at specialized centers. These patients typically have incomplete imaging at the time of first resection, substandard resection margins, and no intraoperative ultrasound. I have two questions for Dr. Fong.

First, how many patients among the re-resected patients were primarily resected at your two institutions? Did you analyze these patients separately for prognosis interval? Second, if one of your patients returns with a resectable recurrence within 6 months of your first hepatic resection, do you give this patient a test of time with or without chemotherapy, or do you re-resect immediately?

Dr. Layton F. Rikkers (Madison, WI): This paper represents another pace-setting analysis from the group at Memorial Sloan-Kettering regarding the management of colorectal metastases to the liver. It follows an excellent 1999 report by this group in which they developed a prognostic index consisting of six factors that were significantly related to survival after primary resection of colorectal liver metastases. However, not mentioned in the manuscript or in the presentation was the serum CEA level, which was a powerful prognostic factor in that first report. Was CEA analyzed in these patients, and was it a factor prognostically? When we contemplate a second liver resection for colorectal metastases in our institution, we have found PET scanning to be useful to rule out extrahepatic disease. Have you found PET scanning useful in your experience?

Finally, you make the statement that liver resection is the only potentially curative treatment for metastatic colorectal cancer to the liver. I assume, therefore, that you do not consider ablative therapies as potentially curative. Liver resection has several advantages over ablative therapy in that margins can be measured, it has a much longer track record, and it is less likely to be compromised technically than liver resection. In our institution, we have had the benefit of a group of radiologists who became interested in cryoablation both in the animal laboratory and while working with us in the operating room. Cryoablation is done meticulously, always with a radiologist involved and carefully monitoring the freeze ball, to make certain that margins are adequate. With fairly long-term follow-up, we have found local recurrences in only 11% to 12% of those patients undergoing cryoablation. For a second liver recurrence we will frequently use cryoablation rather than resection. Do you consider cryoablation or radiofrequency ablation as potentially curative therapies? Do you use them for patients who are not acceptable candidates for resection or as adjuvant to resection?

Dr. Yuman Fong (New York, NY): Thank you, Drs. Beazley and Rikkers. In terms of the questions that were asked: How do we follow these patients postoperatively? We measure the CEA every 3 months and obtain a CT scan every 6 months. How important is it to identify early recurrences? I think as we become more and more comfortable with ablative therapy, it becomes more important to identify the early recurrences. That is because with ablative therapy it is potentially possible to do a smaller operation than resection that can kill tumor completely. We write in the manuscript that resection is the only therapy that is curative—I mean it is the only proven therapy with long enough follow-up to show that it is curative. I believe that there is a role for ablation in the future. With that, the earlier we find the tumors, the much more likely it is that we will be able to ablate them completely, because the smaller the tumor, the more complete the ablation.

Do we use PET scanning in following these patients? We use that in an experimental setting. That is because the PET scanner is good and it is bad. In certain regions of the body, it is better than others. Inside the liver it is actually not very good. That is because of the high FDG uptake of the hepatocyte. In fact, in a current prospective funded trial that we have, we have been doing PET scanning on everybody, as well as CT photography, and CT scanning, using helical CT techniques. Then we resect the patients and bread-loaf slice the specimen to see how many tumors we find and how many we miss by each scanning modality. Because of the high background of FDG uptake in the hepatocytes, if you have a centimeter tumor or smaller, your chance of finding it inside the liver by current FDG PET scanning is less than 20%. And if that person has recently had chemotherapy, your chance of finding it is even less. Therefore, for the liver, I don’t look at the PET scan as a great technique for following the patients. For extrahepatic disease, I think it is very good. That prospective trial is ongoing and we should have some data to report shortly.

In terms of extrahepatic sites that Dr. Beazley asked about, in some of these patients, they had extrahepatic disease sites before we even went to a second liver resection. Some of these patients during the first liver resection had lymph node involvement in the porta hepatis. Some of these patients had lung tumors that were resected before the second liver resection. And there was a patient with an ovarian tumor that was resected. But all of these patients had a long disease-free interval before we operated on them again. As we analyze that group of patients, the long-term outcome doesn’t look any different, but they are a highly selected group. They are a small subset of the people for whom we resected other extrahepatic disease along with liver the first time. So I think it is a matter of patient selection and other things about the biology that tell us that it is reasonable to do such resections.

Dr. Rikkers asked about CEA. Only two of the patients in the current series actually had a CEA above 200 before we did a further resection, so it is hard to analyze CEA as a single factor. But just to put this series in perspective, Dr. Rikkers mentioned our prognostic score for selecting patients for first-time liver resections, which includes node positivity of the primary tumor, CEA level, size and number of the liver tumors, and the disease-free interval between the primary and the liver disease. When you look at this population, over 90% of the people had three points or less on that scale. This is a very favorable group. This is a highly selected group of patients that we have chosen to do a liver resection the second time. Dr. Vauthey asked about the interval and why we might or might not have found a significance to the interval between the first and second liver resection. As the paper and the presentation stated, the median time between the first and second liver resection was 13.8 months. There was a long disease-free interval. Most of the patients did not recur immediately. And I am convinced that is why we were unable to find a difference. It is again a matter of patient selection.


Correspondence: Yuman Fong, MD, Hepatobiliary Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York 10021.

E-mail: fongy@mskcc.org

Presented at the 113th Annual Session of the Southern Surgical Association, December 3–5, 2001, Hot Springs, Virginia.

Accepted for publication December 2001.


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