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The Role of Staging Laparoscopy in Hepatobiliary Malignancy: Prospective Analysis of 401 Cases

From the Departments of Surgery (MD, YF, SW, RPD, KC, LHB, WRJ) and Epidemiology and Biostatistics (MG), 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 Avenue, New York, NY 10021; Fax: 917-432-2387; E-mail: jarnagiw{at}mskcc.org

	ABSTRACT

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Background: Patients with potentially resectable hepatobiliary malignancy are frequently found to have unresectable tumors at laparotomy. We prospectively evaluated staging laparoscopy in patients with resectable disease on preoperative imaging.

Methods: Staging laparoscopy was performed on 410 patients with potentially resectable hepatobiliary malignancy. The preoperative likelihood of resectability was recorded. Data on preoperative imaging, operative findings, and hospital course were analyzed.

Results: Laparoscopic inspection was complete in 291 (73%) patients. In total, 153 patients (38%) had unresectable disease, 84 of whom were identified laparoscopically, increasing resectability from 62% to 78%. On multivariate analysis, a complete examination, preoperative likelihood of resection, and primary diagnosis were significant predictors of identifying unresectable disease at laparoscopy. The highest yield was for biliary cancers, and the lowest was for metastatic colorectal cancer. In patients with unresectable disease identified at laparoscopy, the mean hospital stay was 3 days, and postoperative morbidity was 9%, compared with 8 days and 27%, respectively, in patients found to have unresectable disease at laparotomy.

Conclusions: Laparoscopy spared one in five patients a laparotomy while reducing hospital stay and morbidity. Targeting laparoscopy to patients at high risk for unresectable disease requires consideration of disease-specific factors; however, the surgeons’ preoperative impression of resectability is also important.

Key Words: Staging laparoscopy • Hepatobiliary neoplasms • Laparoscopic ultrasound • Liver resection

	INTRODUCTION

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Complete resection is the only potentially curative treatment for primary and secondary hepatobiliary malignancies.^1–7 In general, however, resection is beneficial only when there is no distant spread of disease and when all tumor can be safely removed with an adequate hepatic remnant for recovery. The aim of preoperative staging is to identify patients who would benefit from resection and to exclude those with findings—such as extrahepatic metastases, additional hepatic disease, or vascular invasion—that would preclude resection. Although the goals of preoperative imaging are clear, rates of unnecessary laparotomy remain high despite advances in hepatobiliary imaging techniques.

Over the last decade, staging laparoscopy has emerged as a powerful tool to identify occult unresectable or metastatic disease in a variety of intraabdominal malignancies. The potential benefits of identifying occult unresectable disease with laparoscopy and avoiding laparotomy include less pain and morbidity, decreased hospital stay, decreased overall cost, and earlier initiation of nonsurgical therapy.^8–10 Several small series, including preliminary reports from this unit, have documented the utility of staging laparoscopy in hepatobiliary malignancy.^11–18 It is apparent from these reports that the yield of laparoscopy varies with the underlying diagnosis. Furthermore, it seems that the yield of laparoscopy has decreased as imaging technology has improved.

This study is a prospective evaluation of the utility of staging laparoscopy in 401 patients with primary and secondary hepatobiliary malignancy. The study was performed in a tertiary care hepatobiliary center in a setting of extensive preoperative imaging and an aggressive approach to resection.

	METHODS

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From November 1997 through April 2001, 401 patients with resectable hepatobiliary malignancy by radiological criteria were submitted to staging laparoscopy with or without laparoscopic ultrasound (LUS) before a planned open exploration and resection. All cases were reviewed before surgery at a biweekly multidisciplinary conference by the surgeon and one or more staff radiologists, and additional radiological studies were obtained if warranted. Patients suspected of having cirrhosis were assessed with Childs’ classification. Patients with benign tumors and those submitted to operation for palliative procedures were excluded. Patients who had laparoscopic or laparoscopic-assisted resections were excluded from this analysis so that all patients considered resectable at laparoscopy underwent an exploratory laparotomy to confirm or refute the laparoscopic results. Previous abdominal surgery, including upper abdominal surgery and hepatic surgery, was not grounds for exclusion.

The technique for staging laparoscopy of hepatobiliary malignancies has been previously described.¹¹ Briefly, ports were placed along the planned laparotomy incision in the right and left upper quadrant. A 30° laparoscope was used, and at least one additional port was used for retraction, lysis of adhesions, or biopsies, if necessary. A laparoscopic examination was considered complete if all of the following areas were inspected: anterior and posterior surfaces of the right and left hepatic lobes, gastrohepatic omentum, porta hepatis, pelvis, and peritoneal cavity. An examination was considered incomplete if all of these areas were not at least partially examined and was considered a failure if none of the areas could be visualized. In some cases, the liver and porta hepatis were inspected with LUS by using an Aloka Ultrasound Imaging System^TM (Tokyo, Japan) with a 7.5-MHz flexible laparoscopic probe. A full ultrasonic examination of all hepatic segments, portal pedicles, and hepatic veins was performed. Patients with obvious unresectable disease at standard laparoscopy and those with adhesions precluding an adequate examination did not undergo LUS. In a few cases, technical difficulties or unavailability of the LUS equipment precluded the use of this modality.

All suggestive lesions at laparoscopy were biopsied and assessed with frozen-section histology. If unresectability was documented at laparoscopy, the procedure was then terminated, or, in a few cases, open palliative procedures were performed on the basis of an intraoperative assessment of the findings. If the patients were believed to be resectable at laparoscopy, an exploratory laparotomy was performed, and an examination of the liver, porta hepatis, pelvis, and peritoneal cavity was repeated with a combination of inspection, palpation, and open ultrasound. If unresectable disease was encountered at laparotomy, the case was terminated; however, in some cases, palliative procedures were performed on the basis of the intraoperative findings, and intraoperative maneuvers performed to assess resectability.

The criteria for resectability, both general and disease specific, have been previously described.^11,15,17,18 Any patient with cirrhosis whose hepatic remnant was believed to be inadequate for recovery was considered to be unresectable. Patients with hilar cholangiocarcinoma or gallbladder cancer with extrahepatic or discontiguous hepatic metastases, extensive biliary tract involvement precluding a negative margin, or extensive vascular involvement precluding safe anatomical resection were considered unresectable; however, metastatic disease to the porta hepatis lymph nodes did not constitute unresectability, and these lymph nodes were routinely removed as part of the surgical procedure. However, patients with spread to the celiac or retroperitoneal lymph nodes were considered to have unresectable disease. In some cases, tumors adherent to the portal vein may be amenable to resection with portal venous reconstruction,¹⁹ and a few patients were brought to the operating room with this strategy in mind. Patients with secondary intrahepatic malignancy were submitted to resection only if all disease could be extirpated. The presence of additional unsuspected hepatic disease, numerous tumors, or bilobar metastases did not constitute unresectability, provided that all tumor could be safely resected. With the exception of metastatic ovarian cancer, extrahepatic lymph node or peritoneal metastases in patients with secondary tumors were considered unresectable. For hepatocellular carcinoma and peripheral cholangiocarcinoma, extrahepatic or distant intrahepatic metastases constituted unresectability.

Data regarding demographics, preoperative work-up, operative course, outcome of the laparoscopic examination, operative times, length of stay, and morbidity were recorded prospectively and entered into a database. The surgeons were also asked to prospectively document their impression of the likelihood of resectability (probably unresectable, equivocal, probably resectable, or resectable) on the basis of clinical and radiological information. Statistical analysis was performed with SPSS^TM for Windows, version 10.0 (SPSS, Inc., Chicago, IL), and SAS^TM, version 8.0 (SAS Institute, Cary, NC). Postoperative morbidity was compared across types of procedure by using the Cochran-Armitage trend test. Length of stay was compared by using analysis of variance, after log transformations. The preoperative values were subjected to Fisher’s exact test to assess their value in predicting the likelihood of resectability, and a multivariate model was built by using logistical regression. We used stepwise variable selection with likelihood-based methods in arriving at the final multivariate model.

Subsets of patients from this database have been previously reported in separate analyses of the utility of staging laparoscopy for specific hepatobiliary diseases. The group of patients with gallbladder carcinoma and hilar cholangiocarcinoma included patients with uncommon tumor histologies (intraductal, papillary, and squamous cell) not previously analyzed.^11,15,17,18

	RESULTS

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Demographics and Preoperative Evaluation
From November 1997 through April 2001, 401 patients with potentially resectable tumors were prospectively studied. The demographics and diagnoses are listed in Table 1. The most common diagnosis was metastatic colorectal cancer, which accounted for nearly half of the patients. Table 2 summarizes the extent of preoperative imaging, as well as the surgeons’ preoperative clinical impression of the likelihood of resectability. All patients had preoperative computed tomographic and/or magnetic resonance imaging scanning. The other radiological studies were less commonly used and varied by diagnosis. Eighty-seven percent of the group had two or more studies performed, and 46% had three or more studies.

The utility and overall yield of staging laparoscopy are summarized in Fig. 1. Eighty-four (20.9%) patients were found to be unresectable at laparoscopy, and of these, 79 (19.7%) of 401 were spared a laparotomy. Five patients with unresectable disease at laparoscopy were submitted to open procedures on the basis of intraoperative findings. Two had a palliative biliary bypass, one underwent hepatic artery pump placement, one had a colostomy, and one required a small laparotomy for a safe biopsy. Of the 317 patients believed to be resectable at laparoscopy, 69 had unresectable disease at open exploration, yielding a 21.8% false-negative rate. Overall, laparoscopy identified 84 (55%) of 153 patients with unresectable disease and increased resectability from 61.8% (248 of 401) to 78.2% (248 of 317). Table 3 lists the operative findings that precluded resection. Laparoscopy correctly identified the vast majority of patients with unsuspected cirrhosis and peritoneal disease and most patients with additional hepatic tumors, but it commonly failed to identify lymph node metastases and vascular invasion when these were the cause of unresectability.

View larger version (17K): [in this window] [in a new window]   FIG. 1. Flow chart demonstrating the utility and overall yield of staging laparoscopy in 401 patients with potentially resectable hepatobiliary malignancy. bx, biopsy.

Predicting Laparoscopic Identification of Unresectable Disease
Factors applicable to all of the diseases were analyzed in a univariate and multivariate fashion to determine whether any factors could help to predict laparoscopic identification of unresectable disease (Table 4). The three patients with intraductal papillary biliary tumors and the one patient with a primary hepatic sarcoma were excluded from this analysis so that the other six major diagnostic groupings could be accurately analyzed. For the purposes of this analysis, the surgeons’ preoperative prediction of the likelihood of resectability was divided into two groups: "probably unresectable" and "equivocal" versus "probably resectable" and "resectable." After multivariate adjustments, diagnosis, preoperative likelihood of resectability, and a complete laparoscopic examination were all predictive of finding unresectable disease. Figure 2 graphically illustrates the influence of the preoperative likelihood of resection and the completeness of the laparoscopic examination on the yield of laparoscopy. The surgeon’s preoperative clinical impression was a remarkably predictive factor. Specifically, when the surgeon believed that the tumor was probably unresectable (24 patients), the yield of laparoscopy was nearly 60%, and when the surgeon believed that the tumor was resectable (46 patients), the yield was 0.

View larger version (26K): [in this window] [in a new window]   FIG. 2. Chart demonstrating the yield of staging laparoscopy in patients with and without a complete laparoscopic examination, as well as the effect of the preoperative clinical impression on the yield of laparoscopy. Prob, probably.

View larger version (44K): [in this window] [in a new window]   FIG. 3. Chart demonstrating the rate of occult unresectable disease and the proportion identified by laparoscopy in all patients and stratified by diagnosis. GB, gallbladder; CC, cholangiocarcinoma; Periph, peripheral; met, metastatic; HCC, hepatocellular carcinoma.

Postoperative morbidity, laparoscopic operative time, and length of stay stratified by the extent of the operative procedure are listed in Table 5. The first group of patients are those who had unresectable disease documented at laparoscopy. The second group of patients are those who had unresectable disease documented at laparotomy, and the third group are those who underwent laparotomy and resection. The overall morbidity rate was 27.9% (112 of 401). In patients who underwent laparoscopy alone, the morbidity was 9.5% (8 of 84), and this significantly increased as the magnitude of the procedure increased (P < .001). There were five postoperative deaths, yielding a 1.2% operative mortality. Four of the deaths were in patients who had undergone resection; however, one patient with hepatocellular carcinoma died of postoperative biliary sepsis and respiratory failure after metastatic disease was identified in a portal lymph node at laparotomy. The operative time dedicated to laparoscopic exploration is listed in Table 5. In general, laparoscopy added 30 minutes of operative time to those going on to laparotomy. Patients who underwent only laparoscopy had a significantly decreased postoperative length of stay (P < .001). Of note, the mean length of stay for those undergoing only laparoscopy was 3 days. This was largely due to patients who required percutaneous biliary drainage or internalization of existing biliary catheters, although some patients also had minor complications that extended the stay.

	DISCUSSION

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Over the last decade, laparoscopic techniques have emerged as a very powerful tool in many aspects of both therapeutic and diagnostic abdominal surgery. Staging laparoscopy for abdominal malignancies has rapidly become a standard technique and is considered by some to be standard for operable pancreatic and gastric cancer.^10,20–22 The benefits of identifying unresectable disease with laparoscopy include less pain, decreased time in the hospital, decreased recovery time, less morbidity, and more rapid and increased use of other therapies.^8–10

A number of small series have addressed the role of staging laparoscopy for hepatobiliary malignancy. Two early series, both published in 1994, looking at small numbers of patients (29 and 52) showed that approximately 40% of patients could be spared a laparotomy and that resectability rates could be significantly improved.^12,13 In the years after these early reports, the technique and accuracy of radiological techniques such as computed tomography and magnetic resonance imaging have improved greatly.^23,24 Additionally, newer modalities of identifying metastatic disease with physiologic scans, such as positron emission tomography scan, have become available.²⁵ Other research on the use of staging laparoscopy has focused on specific diagnoses. Lo et al.¹⁴ published a series of 91 patients with hepatocellular carcinoma in 1999 in which 16% of the patients were spared a laparotomy by staging laparoscopy. Two other recent studies (one including some patients from this series) have shown that staging laparoscopy in metastatic colorectal cancer can spare 10% to 36% of patients a nontherapeutic laparotomy.^15,16 Our group has previously published studies from subsets of this database on extrahepatic biliary malignancies (gallbladder cancer and hilar cholangiocarcinoma) and noncolorectal, nonneuroendocrine hepatic metastases demonstrating that 19% and 35%, respectively, of these patients were spared a laparotomy.^17,18

The results of these previous studies suggest that the benefits of staging laparoscopy have become more modest over time and show that most patients do not benefit from staging laparoscopy. Additionally, there is significant variability in the yield of laparoscopy among the different hepatobiliary malignancies. These data prompted this comprehensive review of our prospective laparoscopic database of 401 patients with hepatobiliary malignancy.

The data clearly show that one in five patients with hepatobiliary malignancy can be spared a laparotomy. Laparoscopy was able to identify 55% of patients with unresectable disease, suggesting that there is much room for improvement. On review of the successes and failures of laparoscopy, it is apparent that laparoscopy is most accurate for identifying peritoneal disease (80% accurate) and additional hepatic disease (63% accurate) and is the least accurate for vascular invasion (18% accurate) and lymph node metastases (7% accurate). Clearly, if staging laparoscopy for hepatobiliary malignancy is to be improved, efforts must be directed at better identifying vascular invasion and metastatic disease in lymph nodes. Vascular invasion is a difficult issue, because most of the patients do not have encasement of vessels on imaging studies or laparoscopy, but rather have only a suggestion of vessel contact, which can often be assessed only at operation. Persistence at finding lymph node metastases requires some level of advanced laparoscopic skills and would probably require additional operative time. Unfortunately, size alone is not a good indicator of whether a lymph node is harboring metastatic disease, and this limits the utility of anatomical radiological techniques. Newer physiologic imaging, such as positron emission tomography scanning, however, may be able to detect hypermetabolic activity and diagnose metastatic disease in lymph nodes or, at least, guide specific laparoscopic exploration.²⁵

Although overall, 20% of patients with primary or secondary hepatobiliary malignancy can be spared a laparotomy with staging laparoscopy, clearly certain factors influence the yield. LUS was responsible for 10% of the cases that were unresectable at laparoscopy. The benefit of LUS was largely in finding additional hepatic tumors and vascular invasion, and when these factors are the major issue, LUS should be used. The surgeons’ preoperative judgment about the likelihood of resectability was remarkably predictive in this study. Although the experience and expertise of the surgeon making these judgments will alter this predictability, clearly, the surgeon’s clinical judgment can have profound effects on the yield of laparoscopy. Finally, along the spectrum of hepatobiliary neoplasms, our data demonstrate that there is wide variability in the yield of staging laparoscopy. Patients with gallbladder cancer and cholangiocarcinoma benefit the most, and indeed, staging laparoscopy should be routine for patients with these diseases. In patients with other metastatic disease and hepatocellular carcinoma, the benefit is moderate, and although most of these patients should undergo staging laparoscopy, clinical judgment can help guide its selective use. Patients with metastatic colorectal cancer clearly benefit the least, and clinical judgment should be used to utilize laparoscopy selectively in these patients.

Staging laparoscopy remains a powerful diagnostic tool in patients with hepatobiliary malignancy. However, with extensive preoperative imaging, most patients do not benefit from the procedure, which argues for a selective approach. By using factors such as diagnosis and clinical impression, laparoscopy can be targeted to patients who are at the highest risk of having occult unresectable disease. Ultimately, the clinician will have to decide the threshold of yield for staging laparoscopy that is acceptable and worthwhile clinically and financially.

	Footnotes

 
This study evaluated the effect of staging laparoscopy on 401 patients with potentially resectable hepatobiliary malignancy. Laparoscopy identified most unresectable cases and spared 79 (20%) patients a laparotomy.

Received for publication April 1, 2002. Accepted for publication September 19, 2002.

	REFERENCES

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by D’Angelica, M. Articles by Jarnagin, W.R. Search for Related Content PubMed PubMed Citation Articles by D’Angelica, M. Articles by Jarnagin, W.R. Related Collections Surgery