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10.1245/ASO.2005.06.034
Annals of Surgical Oncology 12:459-466 (2005)
© 2005 Society of Surgical Oncology
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Original Article

The Role of Liver Resections for Noncolorectal, Nonneuroendocrine Metastases: Experience With 142 Observed Cases

Giorgio Ercolani, MD, Gian Luca Grazi, MD, Matteo Ravaioli, MD, Giovanni Ramacciato, MD, Matteo Cescon, MD, Giovanni Varotti, MD, Massimo Del Gaudio, MD, Gaetano Vetrone, MD and Antonio Daniele Pinna, MD

Department of Surgery and Transplantation, University of Bologna, Hospital Sant’Orsola-Malpighi, Via Massarenti 9, 40138 Bologna, Italy

Correspondence: Address correspondence and reprint requests to: Giorgio Ercolani, MD; E-mail: gercolani{at}aosp.bo.it.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: To evaluate the role of liver resection for noncolorectal, nonneuroendocrine metastases, indications and results were retrospectively reviewed in 142 observed patients.

Methods: A curative liver resection was performed in 83 cases (58.5%), and the remaining 59 patients received palliative treatments. The primary tumor site was gastrointestinal in 18, breast in 21, genitourinary in 15, leiomyosarcoma in 10, and other in 19. The mean number of metastases was 1.4. The mean diameter of the nodules was 5.7 cm. Liver metastases were synchronous in 11 (13.3%) cases and metachronous in the remaining 72 (86.7%).

Results: There was no operative mortality. Postoperative morbidity was 20.5%. The median postoperative stay was 9.5 days. The 3- and 5-year actuarial survival rate was 49.5% and 34.3% in resected cases, respectively, whereas there were almost no survivors 3 years after diagnosis in unresected cases (P < .05). The 3- and 5-year disease-free survival was 41.4% and 23.8%, respectively. Among the 83 resected cases, the 3- and 5-year actuarial survival was 17.3% and 8.6% for metastases from gastrointestinal tumors, 53.9% and 24.6% from breast cancer, 63.7% and 36.4% from leiomyosarcoma, 50.4% and 37.8% from genitourinary neoplasms, and 55.6% and 42.4% from other sites, respectively. Fifteen patients (18.1%) survived longer than 5 years.

Conclusions: Liver resection is an effective treatment for noncolorectal, nonneuroendocrine metastases; it allows satisfactory long-term survival with an acceptable operative risk in selected patients. Hepatic metastases from gastrointestinal carcinoma have the worst prognosis; those from genitourinary tumors show a better outcome. Patient selection is the key to achieving encouraging results.

Key Words: Liver neoplasms • Neoplasm metastasis • Hepatectomy • Treatment outcome • Prognosis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Liver resection is the treatment of choice for isolated colorectal hepatic metastases; it leads to a 5-year survival of 30% to 45%.1–3 Because chemotherapy provides responses in only a minority of cases, with no chance of cure, aggressive surgery has been advocated for advanced colorectal hepatic metastases, with satisfying results.4,5 In the case of isolated neuroendocrine metastatic tumors, an aggressive surgical approach is considered the treatment of choice; liver transplantation has been applied in selected cases, and debulking surgery may play a role in prolonged survival.6–9 Operative mortality in liver surgery has decreased to <5% because of improvements in surgical technique and in perioperative and postoperative management.10,11

The role of liver resection for noncolorectal, non-neuroendocrine hepatic metastases (NCNNM) is still a matter of discussion. There is a lack of controlled, randomized, prospective studies, and most published series report only a small number of cases; therefore, final conclusions should be analyzed with caution.12–16 Clear guidelines about the indications for and limits of surgery for NCNNM are not currently available. We retrospectively reviewed our experience with 142 patients with NCNNM to evaluate the role of liver resection in early and long-term outcome, factors that might affect prognosis, and which subsets of patients should be selected for surgery.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From November 1990 to March 2003, 142 patients with NCNNM were admitted to the Department of Surgery and Transplantation, University of Bologna. Thirty-two (22.5%) patients were not candidates for liver resection because a curative partial hepatectomy was not possible on the basis of preoperative evaluation, 22 (15.5%) underwent exploratory laparotomy because extrahepatic disease was not detected at the preoperative work-up, and in 5 (3.5%) a palliative resection was performed.

A curative liver resection was performed in the remaining 83 cases (58.5%), which represent the study population of this retrospective analysis. There were 35 men (42.2%) and 48 women (57.8%). Patients were aged (mean ± SD) 54.6 ± 11.4 years (range, 18–76 years). For statistical analysis, on the basis of anatomical location, the site of the primary tumor was grouped as gastrointestinal (n = 18), breast (n = 21), genitourinary (n = 15), soft tissue (n = 10), and others (n = 19; Table 1Go).


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  		TABLE 1. Site of the primary tumor among the 83 patients with resection for noncolorectal, nonneuroendocrine metastases
 
Selective diagnostic work-up for patients with liver metastases included the evaluation of liver function, measurement of serum tumor markers (depending on the location of the primary tumor), ultrasonography, chest x-ray, abdominal spiral computed tomography (CT) scan (bone scintigraphy and cerebral CT scan, depending on the primary tumor), and, in a few patients, liver biopsy to confirm the presence of secondary disease. In the most recent years, positron emission tomography scanning has been used to detect extrahepatic tumors. The presence of extrahepatic disease at the preoperative evaluation was considered an absolute contraindication to surgery.

The number of nodules (mean ± SD) was 1.4 ± .8 (range, 1–4). A single metastasis was present in 58 (69.8%) patients. The diameter (mean ± SD) of the nodules was 5.7 ± 3.8 cm (range, 1–10 cm).

In 11 (13.3%) patients, the discovery of metastatic disease was synchronous with the primary tumor. In 72 (86.7%) patients, liver metastases were metachronous. Disease-free survival after resection of the primary tumor was longer than 1 year in 49 (59%) patients.

Thirty-five patients (42.2%) received postoperative chemotherapy after excision of the primary tumor. Adjuvant chemotherapy was administered in 26 (31.3%) patients after liver resection without randomization. The chemotherapy protocol was selected according to the primary tumor.

The surgical technique of liver resections and different methods of vascular control to reduce intraoperative bleeding have already been described.10 Major hepatectomies were defined as the removal of three or more segments according to Couinaud’s classification.17 Only in selected cases with involvement of the inferior vena cava or main hepatic vein was total vascular exclusion applied.18 A curative procedure was defined as a free surgical margin of >1 cm and confirmed as free from tumor invasion by pathologic examination and the absence of extrahepatic disease.

Operative results (intraoperative blood transfusion, operative time, and postoperative morbidity and mortality) and long-term survival were evaluated to define whether liver resection should be applied in patients with NCNNM.

Among the 83 patients with resected disease, the following prognostic factors were analyzed to establish which patients could be the best candidates for surgery and which patients should be expected to be long-term survivors: synchronous versus metachronous presentation, single versus multiple metastases, maximum diameter <5 or >5 cm, percentage of liver involvement (on the basis of preoperative imaging and, more recently, CT volumetry), requirement for intraoperative transfusion, disease-free survival in patients with metachronous lesions <1 or >1 year, adjuvant chemotherapy, and total tumor volume (TTV). As already reported elsewhere, this last variable (calculated by assuming that all metastases were sphere shaped) seems to be related to long-term survival in patients with hepatic metastases.5 These are listed in Table 2Go. Finally, long-term outcome on the basis of different sites of primary tumor was also evaluated in the group of patients with resected disease.


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  		TABLE 2. Median survival time (and P value) of clinico-pathologic prognostic factors in 83 patients who underwent resection
 
Postresection Follow-Up
Follow up ended in September 2003. Patients were followed up every 3 months after liver resection for recurrence with biochemical tests including tumor markers, hepatic ultrasonography, and chest x-ray film during the first year and every 6 months thereafter. A CT scan was performed whenever a local or distant recurrence was suspected on the basis of the other examinations.

Statistical Analysis
Operative mortality was defined as death within 30 days of surgery. Survival was considered from the day of liver resection for metastases to the day of death or the most recent follow-up visit. Patients undergoing exploratory laparotomy or palliative resection were considered as a control group for comparison with the resected group.

Results are expressed as mean ± SD. The {chi}2 test was used for categorical variables. Student’s t-test was used to compare continuous variables. Overall survival and disease-free survival curves were estimated by means of the Kaplan-Meier method. Comparisons of curves were made with the log-rank test. A multivariate analysis using the Cox proportional hazards model was used between the prognostic factors analyzed at univariate analysis. A statistically significant difference was defined as P < .05. Statistical analysis was performed with SPSS (SPSS Inc., Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Operative Procedure and Early Outcome
Among the 83 curative liver resections, a wedge resection was performed in 11 patients (13.3%), segmentectomy in 38 (45.8%), and major hepatectomy in 34 (41%). The amount of blood transfusion (mean ± SD) was 373.7 ± 167.5 mL (range, 0–1500 mL), which is equivalent to 1.3 ± 1.1 units of packed red cells (range, 0–5 units). The amount of fresh frozen plasma transfusion (mean ± SD) was 168.5 ± 35.8 mL. In 49 patients (59%), intraoperative transfusion was not required.

Bleeding was controlled through intermittent clamping of the hepatic pedicle in 27 (32.5%) patients; total vascular exclusion was required in 2 (2.4%) patients. In 54 (65.1%) patients, there was no need for vascular occlusion.

The operative time (mean ± SD) was 225.6 ± 111.4 minutes (range, 60–660 minutes). There was no operative or in-hospital mortality in this series. Postoperative complications appeared in 17 (20.5%) patients; 2 required a relaparotomy for hemoperitoneum. The median hospital stay was 9 days (range, 7–40 days).

Long-Term Survival
The median length of follow-up was 36 ± 20 months (range, 6 months to 14 years). The overall actuarial survival rate at 1, 3, and 5 years was 84%, 49.5%, and 34.3% for 83 resected cases (Fig. 1AGo). The 1-year survival was 66.6% and 30.1% after palliative resection or exploratory laparotomy, respectively (Fig. 1B and 1CGo). The difference between curative liver resection and other procedures was statistically significant (P < .05). There was no difference in long-term outcome between palliative resection and exploratory laparotomy: in both groups, there was only 1 survivor 3 years after surgery, and there were no survivors after 4 years. Similar results were obtained in patients not amenable to resection at the preoperative work-up (Fig. 1DGo).


Figure 1
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  		FIG. 1. (A) Survival curve of 83 patients with resected disease for noncolorectal, nonneuroendocrine hepatic metastases. (B) Survival curve of patients who underwent palliative resection. (C) Survival curve of patients who underwent exploration. (D) Survival curve of patients who were excluded at the preoperative evaluation because of extension of the disease.

 
Tumor recurrence appeared in 37 (44.6%) patients and was the main cause of death. The 1-, 3-, and 5-year disease-free survival was 63.1%, 41.4%, and 23.8%, respectively. Fifty-three (63.9%) patients died during follow-up, whereas 33 (36.1%) are still alive. Fifteen (18.1%) patients survived >5 years after curative liver resection (Table 3Go).


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  		TABLE 3. Clinical characteristics of 15 patients who survived more than 5 years after resection
 
Analysis of Prognostic Factors
On univariate analysis, tumor diameter, percentage of hepatic tumor replacement, and TTV were significantly related to long-term survival (P < .01 for each one). Number of lesions, type of hepatic resection, blood transfusion, and adjuvant chemotherapy did not affect prognosis. There was a tendency to a better survival in patients with a disease-free survival >1 year after resection of the primary tumor, but this difference was not statistically significant. The median survival time for each prognostic factor is reported in Table 2Go.

On multivariate analysis, considering the variables that were significant on univariate analysis and including the disease-free survival, which showed a significant tendency, only the TTV was statistically significant (P<.01; the survival curve of the 83 patients with resected disease depending on TTV is reported in Fig. 2Go). The relative risk of an unsuccessful outcome was 2.87 (95% confidence interval, 1.37–7.7) in patients with a TTV of 125 to 380 cc3, and it was 3.01 (95% confidence interval, 1.42–8.87) with a TTV >380 cc3 compared with a TTV <125 cc3.


Figure 2
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  		FIG. 2. Survival curve of 83 patients with resected disease for noncolorectal, nonneuroendocrine hepatic metastases according to

 
Survival Depending on the Site of the Primary Tumor
As reported in Patients and Methods, the types of primary tumor were grouped on the basis of anatomical locations. These included gastrointestinal, breast, soft tissue, genitourinary, and other rare type of tumors. The 3- and 5-year survival rates were 17.3% and 8.6%, 53.9% and 24.6%, 63.7% and 36.4%, 50.4% and 42.4%, and 55.6% and 37.8%, respectively (Fig. 3Go). The median survival time after curative liver resection is listed in Table 4Go. The 3- and 5-year disease-free survival was 16.8% and 8.6%, 42.6% and 17.1%, 44.4% and 22.2%, 46.1% and 34.6%, and 47.8% and 30.4%, respectively.


Figure 3
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  		FIG. 3. Survival curve of patients with resected disease according to the site of the primary tumor (squares, metastases from breast tumors; circles, metastases from gastrointestinal tumors; triangles, metastases from soft tissue tumors; bold dashes, metastases from other tumors; stars, metastases from genitourinary tumors).

 

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  		TABLE 4. Median survival time on the basis of the site of the primary tumor
 
Gastrointestinal tumors had a significantly worse prognosis compared with each of the other groups (P < .05 for each correlation). Liver resection for genitourinary metastases had the best outcome, with a median survival time >5 years.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The role of liver resection for NCNNM is still quite controversial. Available data indicate a poor survival in patients with unresectable metastases.12 However, we have reported a 5-year survival close to 35% and a 5-year disease-free survival of 24% in the case of curative hepatic resection for NCNNM, compared with the dismal prognosis of patients undergoing palliative procedures and almost no survivors 3 years after diagnosis. A 5-year survival rate between 20% and 37% might be expected in these patients after curative liver resection.13,19,20

These survival rates are similar to those achieved after surgical treatment of colorectal hepatic metastases in recent series and in our experience.1,2,5 We believe that as hepatic resection is considered the treatment of choice for colorectal metastases, it should be considered the gold standard in selected patients with NCNNM.

One of the most important results in this series is that approximately 20% of patients were alive 5 years after surgical treatment. In the literature, the actuarial survival rate is usually reported, but there is a lack of data regarding long-term survivors, because most reported series consisted of just a few cases. This very satisfying result should allow oncologists and surgeons to consider a more aggressive policy when faced with NCNNM confined to the liver. It is interesting to note that 86.6% of patients who survived >5 years after liver resection showed one single nodule at the final pathologic examination; only two patients had multiple nodules (Table 3Go). In the entire study population, the mean number of resected nodules was 1.4, and almost 70% of patients had a single metastasis. Therefore, patient selection should probably be considered the key point in obtaining acceptable long-term results.

In this series, the resectability rate was close to 60%. The main reason for exclusion from curative resection was the presence of extrahepatic disease. This point was considered an absolute contraindication to liver resection for NCNNM and was the main reason for unresectability. In five patients, a palliative resection was performed with dismal results; all of them died within 3 years from operation. This observation is consistent with data reported in the literature.12–14,16,20 Therefore, the surgical option should be indicated only when a curative procedure can be performed; otherwise, alternative treatments must be proposed.

These encouraging results were obtained with a low postoperative morbidity and without mortality. The refinements in preoperative work-up, anesthesiologist management, perioperative care, and surgical technique have significantly improved the safety of liver surgery, and operative mortality has decreased to approximately 1% in tertiary referring centers.5,11,21 For these reasons, in the last 10 years, liver resection has been proposed not only for colorectal and neuroendocrine metastases, but also for metastatic tumors from other sites. Because most NCNNMs arise in the liver without chronic damage, hepatic resection can be safely applied with an acceptable operative risk. Surgical results for NCNNM are reported in very few studies of the 1990s, and clear guidelines do not yet exist; in the largest published series of NCNNM, Elias et al.20 concluded that there is a substantial absence of known prognostic factors.

In this series, the type of resection, blood transfusion, and the time of appearance (synchronous or metachronous) did not affect survival. The same result was found for the role of chemotherapy. However, patients were enrolled over 15 years. Both chemotherapy protocols and referring oncologists varied greatly in this period. Therefore, definitive conclusions on the role of adjuvant treatments cannot be assumed from our analysis. Some authors reported a correlation between a disease-free interval longer than 1 or 3 years after resection of the primary tumor and long-term outcome.13,14 These data were not confirmed in other studies.16,20 We observed a tendency to a better outcome in patients with a disease-free interval of >1 year after removal of the primary tumor, but this did not reach statistical significance, probably because of the small number of patients.

We have already reported that number and location do not affect the prognosis after liver resection for colorectal metastases; on the contrary, TTV seems to be strongly related to prognosis.5 Similarly, in this series, tumor diameter, percentage of hepatic replacement, and TTV significantly affected long-term outcome; however, on multivariate analysis, only TTV showed a significant relation to survival. One of the main points of this study is that the total amount of tumor seems to be the strongest indicator of survival in patients with resected disease for NCNNM. In fact, the greater is the tumor mass, the more is the angiogenesis and the possibility of hematogenous dissemination. TTV is a reliable indicator of the tumor mass; it synthesizes and adds more statistical relevance to the variables of tumor number and tumor diameter. Therefore, even if single nodules in patients without extrahepatic disease are the optimal indication for liver resection, multiple small metastases might not be considered an absolute contraindication to operation.

Regarding the influence on survival of the site of the primary tumor, liver resection for metastases from gastrointestinal tumors showed the worst prognosis. Actually, a dismal prognosis in this group of patients due to very aggressive tumor biology has already been reported.16,20,22,23 In the present series, one patient survived 5 years after resection for gastric metastases, and a few long-term survivors are also described.23,24 Nonsurgical treatments do not achieve satisfactory results, with a median survival time ranging from 2 to 11 months.24,25 We believe that hepatic resection may be justified in a highly selected group of patients with metastases from gastric cancer; a very careful evaluation of patients with metastases from other gastrointestinal carcinomas is mandatory.

In the case of unresectable hepatic metastases from breast carcinoma, the median survival time is shorter than 1 year.26 In our experience, the median survival time was close to 40 months, with a 5-year survival of 20% after curative hepatectomy for breast metastases. Similar results have been achieved in other series.13,26–28 Even if this is a systemic disease and systemic adjuvant chemotherapy plays an essential role in the control of the disease, liver resection for isolated breast metastases can be associated with long-term outcome in selected patients.

In the case of hepatic metastases from soft tissue sarcoma, curative resection is the only reasonable treatment in the absence of effective chemotherapy.29 The most prevalent histological type is leiomyosarcoma (from 85% to 100%, as in this series). Among the nine resected cases for metastases from leiomyosarcoma, the median survival time was quite acceptable, and one patient has survived for longer than 5 years. Because of the small number of patients, no definitive conclusions can be assumed.

There is a general consensus about the encouraging results in selected resected cases for metastases from genitourinary tumors.13,16,30,31 Almost one third of patients who survived >5 years were in this group. Five-year survival rates close to 50% have been reported; in particular, prolonged survival is described for patients with testicular and renal cell cancers.19,31,32 The combination of curative resection with adjuvant chemotherapy (multidisciplinary treatment) produces the best results. An aggressive policy seems to be the best strategy, as for colorectal and neuroendocrine metastases.

Among patients in the miscellaneous group, definitive conclusions on the effectiveness of surgery cannot be assumed, because of the heterogenicity of the patients. However, because of the absence of operative mortality and long-term results in this report, it can be assumed that whenever a curative hepatic resection can be performed with an acceptable operative risk, it should be considered. In fact, the expected results are nevertheless superior to those with palliative therapies.

In conclusion, liver resection is an appropriate treatment for NCNNM. Satisfactory long-term results with a low operative risk can be achieved in highly selected patients when a curative resection is possible. Hepatic metastases from genitourinary tumors seem to show a better prognosis compared with the other histologies and sites, and patient selection is the key to obtaining encouraging results.


   ACKNOWLEDGMENTS
 
The authors thank Dr. Murray Brennan for editing the manuscript.

Received for publication June 22, 2004. Accepted for publication January 19, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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