Annals of Surgical Oncology 9:204-209 (2002)
© 2002 Society of Surgical Oncology
Staging Laparoscopy for Potentially Resectable Noncolorectal, Nonneuroendocrine Liver Metastases
M. D’Angelica, MD,
W. Jarnagin, MD,
R. Dematteo, MD,
K. Conlon, MD,
L.H. Blumgart, MD and
Y. Fong, MD
From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.
Correspondence: Address correspondence and reprint requests to: William R. Jarnagin, MD, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 917-432-2387; E-mail: jarnagiw{at}mskcc.org
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ABSTRACT
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Background: Carefully selected patients with noncolorectal, nonneuroendocrine (NCNN) liver metastases may benefit from hepatic resection. The incidence of occult unresectable disease and the possible benefits of staging laparoscopy in these patients are not known.
Methods: From December 1997 to July 2000, staging laparoscopy was performed in 30 consecutive patients with NCNN metastases before planned open exploration and resection. Demographics, extent of preoperative imaging, operative and postoperative findings, and factors associated with laparoscopic identification of unresectable disease were analyzed.
Results: Twenty-four patients (80%) had a complete laparoscopic examination, and 23 had laparoscopic ultrasonography. All patients underwent preoperative computed tomography or magnetic resonance imaging, and 21 (70%) patients had 2 or more preoperative radiological studies. Overall, nine patients had unresectable disease, six of whom were identified by laparoscopy. Of the remaining 24 patients believed to have resectable disease at laparoscopy, 21 went on to a potentially curative procedure. Laparoscopy did not identify irresectability because of vascular involvement in three patients. Laparoscopy added a median of 30 minutes of operative time to those patients going on to laparotomy.
Conclusions: Laparoscopy identified the majority of patients with occult unresectable disease, improved resectability, and should be routine in patients being considered for potentially curative hepatic resection.
Key Words: Staging laparoscopy • Liver metastases • Hepatic resection • laparoscopic ultrasound
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INTRODUCTION
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Hepatic resection for metastatic cancer has only recently emerged as a viable and effective treatment option. The therapeutic benefit of partial hepatectomy for metastatic colorectal cancer has been investigated extensively and is now well established.1–3 Similarly, long-term survival after hepatic resection of metastatic neuroendocrine tumors has also been shown,4,5 although the natural history of this disease is long and the effect of resection on long-term survival is more difficult to assess. In a third group of patients with other primary tumors metastatic to the liver, referred to collectively as noncolorectal, nonneuroendocrine (NCNN) hepatic metastases, the role of hepatic resection has been less clear. Patients with NCNN hepatic metastases typically have disease that is not amenable to a potentially curative resection, and experience with this clinical entity has therefore been limited.6,7 Recently, however, two reports have shown that, in carefully selected patients, resection may be of benefit.8,9
For most patients with metastatic liver disease, one must consider carefully the likelihood of a favorable long-term outcome before proceeding with resection. In making these assessments, clinical variables are used as indicators of disease biology, and although such variables are relatively well established in patients with hepatic colorectal metastases,1 reliable data in patients with NCNN hepatic metastases are scant. Once the decision has been made to proceed with resection on clinical grounds, however, it is clear that most patients benefit only from a complete resection in the absence of extrahepatic disease. Preoperative imaging studies thus play a pivotal role in assessing resectability and selecting patients appropriate for operation.
Despite improvements in imaging technology, a large number of patients are found to have unresectable disease at the time of open exploration. Over the past several years, laparoscopy and laparoscopic ultrasound (LUS) have been used increasingly to stage patients with a variety of intra-abdominal malignancies and have emerged as valuable adjuncts for identifying radiologically occult unresectable disease. By sparing such patients an unnecessary laparotomy, laparoscopy decreases hospital length of stay and hospital charges, potentially reduces procedure-related morbidity, and may allow earlier institution of nonoperative therapy. Although there are ample data supporting the use of laparoscopy in patients with pancreatic and gastric carcinoma10–13 and in patients with a variety of hepatic malignancies,14–20 no study has specifically analyzed the utility of staging laparoscopy in patients with potentially resectable NCNN hepatic metastases.
This study evaluates the utility of staging laparoscopy in patients with NCNN hepatic metastases at a tertiary care hepatobiliary center. The results show that staging laparoscopy is a useful tool for assessing resectability in patients with NCNN hepatic metastases.
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METHODS
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From December 1997 to July 2000, 30 consecutive patients with potentially resectable NCNN hepatic metastases were subjected to staging laparoscopy with or without LUS immediately before planned open exploration and resection. All patients were taken to the operating room with the intention of performing a potentially curative open resection. A laparoscopic cryoablative procedure was the primary intent in one patient. Patients who had palliative procedures as the primary intent of surgery and those with clear radiographical evidence of unresectable disease were excluded. Cases involving previous hepatic resections were excluded. The indications for operation and preoperative imaging studies were reviewed at a multidisciplinary Hepatobiliary Case Management Conference, and additional studies were obtained as warranted. In all patients, the primary tumor had been previously treated, and all were considered to be candidates for complete resection. Patients with metastatic ovarian cancer were included if they were preoperatively considered to have resectable hepatic disease and extrahepatic metastases amenable to optimal debulking in preparation for chemotherapy.
Laparoscopy was performed through upper-abdominal port sites before planned open exploration and resection, as previously described.14 The anterior and posterior surfaces of the right and left hepatic lobes, the gastrohepatic omentum, porta hepatis, pelvis, and peritoneal cavity were inspected. LUS of the liver was performed with an Aloka Ultrasound Imaging System with a 7.5-MHZ flexible laparoscopic probe (Tokyo, Japan). When adhesions limited access to the right or left lobe, a small incision in the falciform ligament allowed insertion of the LUS probe and examination of the contralateral side.
Laparoscopic examination was considered limited if all areas of interest were not amenable to at least partial inspection, and it was considered a failure if no relevant areas could be inspected. Suspicious extrahepatic or hepatic lesions were biopsied and sent for frozen-section histology if the results would alter management. In patients who proceeded to laparotomy, the liver, peritoneal cavity, pelvis, and retroperitoneum were again fully evaluated, and open ultrasonography of the liver was performed. With the exception of ovarian cancer, the finding of extrahepatic disease or additional hepatic tumors not amenable to complete extirpation constituted irresectability. Additional unsuspected tumors in the liver did not necessarily terminate the procedure, and neither the number of tumors nor the presence of bilobar metastases was used as an absolute criterion of resectability, provided that all disease could be resected.
Data were collected prospectively and included demographics, extent of preoperative imaging, extent of the laparoscopic examination, operative findings, procedures performed, length of hospital stay, and operating room time (total and individual times for laparoscopy and any open procedures). The disease-free interval was defined as the time from resection of the primary tumor to the time of the diagnosis of liver metastases. The number of hepatic metastases and the size of the largest metastasis were determined by preoperative imaging. Cross-sectional imaging studies of the abdomen and pelvis, duplex ultrasonography of the liver, and 18-fluorodeoxyglucose positron emission tomography scans obtained within 1 month of operation were considered as preoperative investigations.
Statistical analyses were performed with SPSS for Windows, version 10.0 (SPSS, Inc., Chicago, IL). Factors potentially associated with a laparoscopic examination revealing unresectable disease were evaluated with a 
2 or Fischer’s exact test, as indicated. P values <.05 were considered statistically significant.
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RESULTS
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Demographics
From December 1997 through July 2000, 30 consecutive patients with potentially resectable NCNN hepatic metastases were submitted to staging laparoscopy before planned open resection. The demographics of these patients and the primary tumor histologies are listed in Table 1. The median age of the patients was 63 years, and 43% of the patients were men. All patients had preoperative computed tomography or magnetic resonance imaging, and 21 (70%) had 2 or more preoperative imaging studies. Nine (30%) of the patients had a preoperative positron emission tomography scan. Two patients were ultimately found to have benign tumors. One was diagnosed at laparoscopy, and a laparotomy was avoided. The other benign tumor seemed suspicious at exploration and was diagnosed histologically after complete resection. Of the 28 patients with malignant tumors confirmed at operation, 17 (58%) had a disease-free interval of >24 months.
Technical Success
Fifteen (50%) of the 30 patients had undergone a previous laparotomy. A complete laparoscopic examination of the liver and abdominal cavity was successfully performed in 24 (80%) of the 30 patients. Of the six examinations that were incomplete because of extensive adhesions, one was a complete failure in that no relevant area could be visualized. Twenty-three (77%) of the 30 patients underwent LUS in addition to standard laparoscopy. LUS was not performed in one patient because extensive adhesions limited access to the liver and in another patient because peritoneal disease was identified during laparoscopic inspection. Five patients did not have an attempt at the examination.
Operative Findings
The results of staging laparoscopy are summarized in Fig. 1. Of the 30 patients who were submitted to staging laparoscopy, 6 (20%) were found to have unresectable disease. Five of these were spared a laparotomy; the remaining patient required a small laparotomy incision because adhesions precluded safe placement of a biopsy port. The specific diagnoses of the patients spared a laparotomy were ovarian carcinoma (n = 2), medullary thyroid carcinoma (n = 1), sarcoma (n = 1), squamous cell carcinoma of the anus (n = 1), and melanoma (n = 1). Of the 24 patients considered to have resectable disease at laparoscopy, 1 underwent a preoperatively planned laparoscopic cryoablation, and the remaining 23 underwent formal laparotomy. Twenty (87%) of these 23 patients underwent a complete resection; 3 patients had unresectable disease, yielding a 13% false-negative rate for staging laparoscopy.
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FIG. 1. Flowchart demonstrating the utility of staging laparoscopy and operative findings. bx, Biopsy; Lap cryo, laparoscopic cryoablation.
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The operative findings that precluded resection are listed in Table 2. Laparoscopy identified all patients with extrahepatic disease or additional hepatic tumors that precluded resection but did not identify three patients with unresectable disease secondary to vascular involvement. One of these patients had a large caudate tumor that was found to involve the main portal vein. LUS was not used in this case. The other two cases were similar in that they both involved large tumors known to invade the right and middle hepatic veins. Left hepatic vein involvement could not be documented laparoscopically despite the use of LUS and was found at laparotomy. In one of these cases, the left hepatic vein could not be adequately visualized secondary to adhesions. By identifying 6 (67%) of 9 patients with unresectable disease, laparoscopy improved resectability from 70% (21 of 30) to 88% (21 of 24).
Twenty-three patients underwent LUS in addition to standard laparoscopy. LUS confirmed the laparoscopic findings in 19 (83%) patients and added new information in 4 (17%) patients. Three of these patients underwent resection with a modification in the operative plan, whereas in one patient the findings at LUS alone precluded resection. Thus, LUS was primarily responsible for one (17%) of the six patients found to have unresectable disease at laparoscopy.
Analysis of Factors Potentially Predictive of Outcome
Several patient, tumor, and operative factors were analyzed in an effort to identify patients most likely to have occult unresectable disease. None of the factors studied predicted the outcome of staging laparoscopy (Table 3).
Perioperative Considerations
There were no intraoperative complications secondary to the laparoscopic examination. Six patients had postoperative complications, yielding a 20% in-hospital morbidity rate. There were two abscesses, one biloma, one episode of atrial fibrillation, one deep venous thrombosis, and one pneumonia. No complication were directly attributable to laparoscopy, and there were no complications in the six patients who had a laparoscopic procedure only. There were no mortalities. For the 23 patients who underwent a laparotomy after staging laparoscopy, the laparoscopic examination added a median of 30 minutes of operating time (range, 10–90 minutes). Of interest, there was no significant difference in laparoscopic operative times between patients with or without a previous laparotomy (data not shown). The five patients who had a laparoscopic biopsy stayed a median of only 1 day in the hospital (range, 1–2 days), whereas the three patients who had a laparotomy and biopsy stayed a median of 4 days (range, 4–9 days). The median stay was 8 days (range, 6–15 days) in the 20 patients submitted to resection.
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DISCUSSION
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Unlike surgical therapy for colorectal or neuroendocrine hepatic metastases, the study of NCNN metastases has largely been anecdotal.6,7 Two recent reports have shed light on this subject and demonstrate that long-term survival is possible in well-selected patients. Harrison et al.8 studied 96 patients and found a 37% overall 5-year survival. Primary tumor type (genitourinary tumors in this study), long disease-free interval (>36 months), and complete gross resection predicted better outcome in this study. Some patients in this series underwent concomitant resection of extrahepatic disease; however, the majority of such patients had ovarian cancer that was amenable to optimal tumor debulking, involvement of contiguous organs by the hepatic tumor, or simultaneous resection of a primary lesion. In a series from the Institut Gustave Roussy, Elias et al.9 reported on a group of patients undergoing liver resection that included 120 with NCNN metastases. The 5-year survival in this group was 36%. The authors found no clinical variables associated with outcome but showed that 5-year survival rates >20% could be achieved in well-selected patients with hepatic metastases from genitourinary, breast, and sarcoma primary tumors. In both series, patients with metastases from gastrointestinal origin did not benefit. Although these studies provide some guidelines, the indications for hepatic resection of NCNN hepatic metastases continue to evolve.
Similarly, data regarding the resectability of hepatic NCNN metastases are sparse. Neither the report from Harrison et al. nor that from Elias et al. addresses the issue of resectability. In a study of hepatic metastases from sarcoma, Jaques et al.21 found an overall resectability rate of 38% (14 of 37 submitted to operation). Two separate studies on liver resection for metastatic breast cancer reported very different rates of resectability. In one, 6 (33%) of 18 patients had resectable disease,22 and in the other, 21 (78%) of 27 had resectable disease.23 Although preoperative imaging has improved greatly over the last decade, it is likely that a significant number of patients with NCNN hepatic metastases undergo an unnecessary laparotomy because of occult unresectable disease found at open exploration. As the indications for hepatic resection broaden, efforts to accurately assess disease extent and reduce the number of unnecessary laparotomies are clearly warranted.
The role of staging laparoscopy in patients with gastrointestinal malignancies is growing and is considered routine by some in the preoperative evaluation of pancreatic and gastric cancer.10–13 Recent studies evaluating the use of staging laparoscopy for the staging of hepatobiliary tumors are listed in Table 4.14–20 Although the percentage of patients spared an unnecessary laparotomy is variable, the results show that staging laparoscopy improves resectability in patients with primary and secondary hepatic malignancies. Ten percent to 40% of patients in these reports avoided the prolonged hospitalization, pain, and morbidity associated with a nontherapeutic laparotomy. The results of this study show that, as with other hepatobiliary malignancies, there was a significant incidence of radiographically occult unresectable disease in patients submitted to resection of NCNN hepatic metastases. The results confirm the utility of laparoscopy in these patients, identifying two thirds of those with unresectable disease and sparing 20% an unnecessary open exploration. Not surprisingly, laparoscopic identification of unresectable disease markedly reduced hospital stay. Additionally, although this was not addressed in this study, we have previously shown that patients undergoing staging laparoscopy for a variety of hepatobiliary malignancies have decreased hospital charges compared with a group that did not undergo staging laparoscopy.14 The principle reason for laparoscopic failures in this report was inability to confirm vascular involvement in three patients, despite the use of LUS in two. It is important to point out that none of these patients had vascular encasement, which would probably be easier to detect laparoscopically.
In summary, this is the first study to specifically analyze the role of staging laparoscopy in patients with NCNN hepatic metastases. Twenty percent of the patients were spared a nontherapeutic laparotomy, and laparoscopy identified two thirds of patients with unresectable disease. In addition, laparoscopy added little additional operative time, was associated with no morbidity, and decreased the length of hospital stay in those with identified unresectable disease. Staging laparoscopy should be routine for patients with potentially resectable NCNN hepatic metastases.
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Footnotes
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Presented in part at the 54th Annual Meeting of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.
Received for publication March 16, 2001.
Accepted for publication September 20, 2001.
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ABSTRACT
INTRODUCTION
