Japanese Journal of Clinical Oncology Advance Access published online on October 10, 2007
Japanese Journal of Clinical Oncology, doi:10.1093/jjco/hym113
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© 2007 Foundation for Promotion of Cancer Research
Liver Resection for Metastatic Gastric Cancer: Experience with 42 Patients Including Eight Long-term Survivors
Department of Gastrointenstinal Surgery, Cancer Institute Hospital, Tokyo, Japan
For reprints and all correspondence: Rintaro Koga, Department of Gastrointenstinal Surgery, Cancer Institute Hospital, 3-10-6 Ariake, Koto-ku, Tokyo 135-8550, Japan. E-mail: rintaro.koga{at}jfcr.or.jp
Received March 19, 2007; accepted July 8, 2007
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Abstract |
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 TOP Abstract INTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONReferences |
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Background: The indication for liver resection for gastric metastases remains controversial and few previous studies have reported the outcome of surgery in the treatment of liver metastases of gastric cancer. The aim of this study is to clarify the effectiveness of surgical resection for liver metastases arising from gastric cancer.
Methods: A retrospective analysis was performed on the outcome of 42 consecutive patients with synchronous (n = 20) or metachronous (n = 22) gastric liver metastases that were curatively resected.
Results: The overall 1, 3 and 5 year survival rates after hepatic resection were 76, 48 and 42%, respectively, and the median survival was 34 months. Univariate analysis revealed that survival significantly differed between cases of solitary and multiple metastases (P = 0.03). Multivariate analysis revealed that solitary liver metastasis and the absence of serosal invasion by primary gastric cancer were favorable independent prognostic factors (P = 0.005 and P = 0.02, respectively). All eight patients who survived for more than 5 years after initial hepatectomy had a solitary metastasis, and six of these had no serosal invasion by the primary gastric cancer. No patient with multiple metastatic diseases survived beyond 3 years.
Conclusions: Patients with a solitary liver metastasis are good candidates for surgical resection, whereas those with multiple gastric liver metastases should be treated by multimodal approaches.
Key Words: gastric cancer • liver metastases • hepatectomy • prognostic factor
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INTRODUCTION |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONReferences |
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Gastric cancer is the second-most common malignancy in the world. In Japan, cancer of the stomach is second only to lung cancer as the cause of death due to cancer (1). Early tumor detection, standardized surgical treatment including lymph node dissection and appropriate adjuvant therapy have improved the survival of patients with primary gastric cancer in Japan (2). However, distant synchronous or metachronous metastases of gastric cancer to the liver jeopardize the likelihood of a cure for this disease. Liver resection has been widely accepted as an effective treatment for metastatic colorectal cancer, and the indications for this procedure have been expanded to include all technically resectable metastases numbering four or more (3–5). However, the benefits of surgical approach to metastatic gastric cancer remain debatable and have been rarely studied (6,7). Accordingly, we reviewed 42 patients who underwent liver resection for metastatic gastric cancer to clarify the surgical outcome and clinicopathological features of favorable prognosis in such patients.
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PATIENTS AND METHODS |
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Patients
A total of 5520 patients with gastric cancer underwent surgery at the Department of Gastrointestinal Surgery, Cancer Institute Hospital, Tokyo, Japan between January 1985 and May 2005. Of these, 121 patients (2.2%) had synchronous liver metastases and 126 patients (2.3%) developed metachronous liver metastases after resection of the primary gastic cancer. Among these 247 patients, 42 consecutive patients (30 men, 12 women; median age 64 years; range 44–89 years) who underwent initial hepatic resection with intent to cure metastatic gastric cancer were selected for this study. Our criteria for hepatic resection of liver metastases from gastric cancer were: the absence of other distant metastases such as peritoneal dissemination; extensive lymph node metastases or lung metastasis; and feasible macroscopically complete removal of liver deposits. However, during the first decade, the decisions for resection were made on a case-by-case basis, depending on individual surgeon's preference. Liver resection was contraindicated in 205 patients for the following reasons: disseminated multiple liver metastases in 64 patients; extrahepatic metastases in 58 patients (peritoneal dissemination in 24, fairly distant lymph node metastases in 26 and lung in 8); systemic dissemination in 38 patients; poor radicality of the primary resection in 11 patients; and absence of detail information in 38 former patients. All patients positive at the second echelon underwent gastrectomy with standard (D2) or extended (D3 or D2+ sampling) dissection of lymph nodes. Nonanatomically limited liver resection was principally the standard surgical procedure for the resection of gastric liver metastases and proceeded in the same manner as that for previously described resection of colorectal liver metastases (8,9). Synchronous en bloc resections of gastric cancer directly invading the liver were excluded from this study. Overall resectability was therefore 17% (42/247) for all 247 patients, 17% (20/121) for those with synchronous metastases and 17% (22/126) for those with metachronous diseases. Patients were followed up at 3–6 month intervals using ultrasonography, abdominal computed tomography and by measuring levels of serum carcinoembryonic antigen (CEA) and carbohydrate antigen 19-9 (CA19-9). Follow-up ranged from 1 to 86 months (median 16 months).
Methods
The following clinicopathological information was obtained from a review of the medical charts of the 42 patients: age; gender; histological differentiation; depth of serosal invasion, extent of lymph node metastases and lymphatic and venous invasion of the primary gastric cancer; size and number of liver metastases; time of appearance of liver metastases; type of hepatic resection; and serum CEA level before hepatectomy. The primary cancer was pathologically diagnosed and classified according to the General Rules for Gastric Cancer Study, 13th edn (10). Patients were separated into two subgroups for each variable to evaluate significant prognostic factors.
Data Analysis
The actuarial overall survival rates from the date of the first liver resection were calculated using the Kaplan–Meier method, and differences were compared between subgroups according to univariate analysis in the resulting distributions using the log-rank test. Based on the results of univariate analysis, we performed a multivariate stepwise Cox regression analysis to identify factors that were independently associated with prognosis. Statistical significance was defined as a P-value below 0.05. All statistical analyses were performed using the package SPSS 9.0 (SPSS Inc., Chicago, IL, USA).
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RESULTS |
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Clinicopathological Data
We examined 42 consecutive patients who underwent 48 hepatectomies. Twenty patients had synchronous liver metastases and 22 patients had metachronous liver metastases. One patient with synchronous metastasis underwent staged hepatectomy 2 months after gastrectomy for primary cancer and one patient with a metachronous lesion had simultaneous regional lymph node recurrence. The median interval between gastric and hepatic resection in the 22 patients with metachronous metastases was 11 months (range 2–43). The number of metastatic nodules at the time of the first hepatectomy was one in 29 patients, two in five patients, three in three patients, and more than four in five patients, with a maximum of seven nodules. Surgical procedures for the initial hepatectomy comprised 35 nonanatomical minor resections; there were seven hemihepatectomies or more extended resections. All patients had pathologically proven adenocarcinoma in the primary gastric location. Pathology revealed that all primary tumors resected at our hospital were advanced gastric cancer that had invaded beyond the muscularis propria. The depth of invasion was known in all patients except for one, who had undergone gastrectomy at another hospital. Serosal invasion was absent in 27 and present in 14 patients, and was detected more commonly in those with synchronous liver metastases (10/22) than those with metachronous metastases (4/21), although the difference was not statistically significant. Gastric cancer involved the lymph nodes of 37 (88%) of the 42 patients, among whom five had paraaortic lymph node metastases. Macroscopically curative resection proceeded for all patients. After the initial hepatectomy, 13 patients were postoperatively administered with either oral or intravenous systemic chemotherapy.
Patient Outcome
None of the patients died within 1 month of surgery, but one died in hospital of liver failure and another of respiratory insufficiency on postoperative days 43 and 68, respectively. The overall 1, 3 and 5 year survival rates after hepatic resection were 76, 48 and 42%, respectively (Fig. 1). The median survival time (MST) was 34 months (range 1–86 months).
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Table 1 shows the results of univariate analysis of prognostic factors. The 5 year survival rate for the 29 patients with a solitary metastasis was 55% (Fig. 2), whereas 13 patients with multiple metastases did not survive beyond 3 years after hepatectomy. Survival between solitary and multiple metastases differed significantly (P = 0.03). Patients without serosal invasion of the primary tumor tended to live longer than those with such invasion, with marginal significance (P = 0.06).
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The variables listed in Table 1 were entered into a stepwise Cox regression analysis. Multivariate analysis revealed that the number of liver metastases and the status of serosal invasion of the primary gastric cancer were independent prognostic factors (P = 0.005 and P = 0.02, respectively, Table 2).
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Twenty-five of 42 patients remain alive at the time of this report. Eight patients survived for over 5 years after the initial hepatectomy (Table 3), all of whom had a solitary liver metastasis. Six patients did not have serosal invasion by the primary gastric cancer. Two patients had distant lymph node metastasis at the third echelon. Half of the patients had synchronous metastatic diseases. The disease recurred in three patients after hepatectomy. In two of the three, it appeared in the remnant liver; both patients underwent a second hepatectomy and remain alive with no further recurrence. The remaining patient developed multiple lung metastases and died at 71 months after the initial hepatectomy.
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Metastatic gastric cancer recurred after the initial hepatectomy in 28 of 42 (67%) patients, among whom recurrence was limited to the remnant liver in 21. Six of 21 patients were administered with oral systemic chemotherapy and one was administered with intravenous systemic chemotherapy. The disease recurred in the lymph nodes of five patients, in whom peritoneal dissemination and skin metastasis were evident. Lung and brain metastasis were each found in one patient. Six of 21 patients in whom recurrence was limited to the remnant liver underwent a second hepatectomy.
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DISCUSSION |
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TOPAbstractINTRODUCTIONPATIENTS AND METHODSRESULTSDISCUSSIONReferences |
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Although the post-resection outcome for primary gastric cancer has improved, this has not been followed by an improvement in survival for these patients with distant metastases (11). The liver is a major site of treatment failure (12,13). Significantly fewer patients with gastric liver metastases are good candidates for resective therapy compared with patients with metastases from colorectal cancer (7,14). This is because of their increased rates of multiple bilateral liver lesions, concurrent extrahepatic diseases and advanced cancer progression such as peritoneal dissemination or extensive lymph node metastases (15,16). Recent studies on the groups of over 20 patients have described the outcome of liver resection for the treatment of metastases arising from gastric cancer (6,17); a few of these patients have survived long-term (18–20). These reports indicate that the 5 year survival and MST after hepatectomy for metastases from gastric cancer ranges from 18 to 38.3% and from 12 to 21.4 months, respectively, and that several factors significantly influence the prognosis.
Our study reported here showed the benefits and limits of hepatic resection for gastric metastases. In this study, solitary liver metastases and the absence of serosal invasion of the primary tumor were proved as independent favorable prognostic factors, whether they were synchronous or metachronous. And none of the patients with multiple gastric liver metastases survived beyond 3 years, whereas the 5 year survival rate for the patients with solitary liver metastasis was 55% with eight long-term survivors. According to the analysis of the eight long-term survivors, faithful lymph node dissection up to the second echelon appeared to have contributed to the chance of cure for the patients with lymph node metastases, if they had solitary liver metastasis.
Several authors have described a solitary liver metastasis as a significant prognostic factor (6,17,20). In the present series of 42 patients, eight of those who survived 5 years or longer had developed a solitary metastasis at the time of the first liver resection. Thus, we confirmed that the number of liver metastases (solitary or multiple) is a significant predictive factor; in contrast, no patients with multiple liver metastases survived beyond 3 years. Shirabe et al. (21) described the presence of three or more tumors as an independent poor prognostic factor according to both univariate and multivariate analysis; however, all four patients who survived beyond 5 years in their study also had solitary tumors, and almost all patients described as long-term survivors (6,17,18,20) had a solitary liver metastasis. The number of liver metastases arising from colorectal cancer is no longer considered an important predictor of long-term survival (4,22); however, a single liver metastasis arising from gastric cancer is considered an important predictor, as it indicates the limit of possible control by local treatment. In the present series, 69% (29/42) of patients had a solitary nodule. One of the reasons for the improved 5 year survival rate in this series might be the higher proportion of patients with solitary nodules.
The absence of serosal invasion was another influential factor for a good prognosis after hepatectomy. The dissemination of malignant cells to the abdominal cavity is as fatal and uncontrollable as extensive lymph node metastases and scattered liver lesions. Serosal invasion of primary gastric cancer is the first step in the advancement to peritoneal dissemination (23) and is reportedly a significant poor prognostic factor following resection of gastric liver metastases (18). Six of eight long-term survivors in our series did not have serosal invasion. Thus, a patient without serosal invasion of primary gastric cancer and who has a high likelihood of avoiding peritoneal recurrence is a promising candidate for liver resection. It is important to precisely understand the depth of invasion of the primary lesion, particularly in the case of synchronous metastases, which do not allow an observation period for the development of peritoneal recurrence after resection of the primary disease. Peritoneal lavage cytology may be of use when considering liver resection (24–26).
In Japan, D2 or greater extended lymphadenectomy has conventionally been performed for advanced gastric cancer with good outcomes (12,27,28) and the incidence of lymph node recurrence is relatively low (11,16). We also performed wide lymph node dissection, including paraaortic nodes, during radical resection of gastric cancer and precise staging of the primary tumor. We have three long-term survivors with lymph node metastases in the second or further echelons; two patients had positive third echelon node metastases in the posterior surface of the pancreatic head. In contrast, patients with positive paraaortic metastases have poor survival rates following liver resection. Few reports have described long-term survival in patients with both paraaortic lymph nodes and liver metastasis (29). Thus, we consider that liver resection for gastric metastasis is not indicated in patients with paraaortic lymph node metastasis. Meanwhile systematic lymph node dissection up to second echelon should be performed if the liver lesion can be completely removed, because six of eight long-term survivors had positive lymph node metastases up to second echelon, even among gastric cancer patients with liver metastases.
Sakamoto et al. (17) previously reported the outcome of resection for gastric liver metastases from our institution. In that study, significant prognostic factors were the number and the size of liver tumors, the results being somewhat different from the present study. These differences are likely to be due to the increased number of patients and difference of the analytic criteria. Thanks to the improvement of the safety of liver resection, the patients who were the candidates for liver resection of gastric metastases have recently increased. Among 42 patients, 20 underwent hepatectomy during the last 5 years of whole period. In the previous study, the cut-off size to categorize the liver tumor was set as 5 cm, whereas it was set as 3 cm in the present study, because the median size of liver tumor was 3 cm. There was no significant difference in both univariate and multivariate analysis, when the analysis of size of liver tumors categorized by 5 cm was done.
Although there were several long-term survivors in the present study, the post-resection survival of other patients was poor, especially those with multiple metastases. Novel chemotherapeutic agents for colorectal cancer can reportedly downstage hepatic tumors to enable resection in subsets of patients who were previously unresectable (30). The present study indicates that the effect of surgical resection is limited in patients with multiple gastric liver metastases. For such patients, the selection of good surgical candidates or down-staging of unresectable disease using various nonsurgical approaches might extend the indications for hepatic resection of gastric metastases without jeopardizing the outcome. Several prospective randomized controlled trials have proven the effectiveness of systemic chemotherapy (31–33) following gastrectomy. Hepatic arterial infusion chemotherapy can be effective for gastric liver metastases (34,35).
To the best of our knowledge, the present study comprises the largest number of patients with liver metastasis of gastric cancer investigated to date. We conclude that surgery including wide dissection of lymph nodes of the primary tumor with curative intent should be considered when a patient has a solitary metastatic tumor.
Conflict of interest statement
None declared.
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References |
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