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Annals of Surgical Oncology 9:725-737 (2002)
© 2002 Society of Surgical Oncology

EDUCATIONAL REVIEW

Minimally Invasive Surgery in the Diagnosis and Treatment of Upper Gastrointestinal Tract Malignancy

Kevin C. Conlon, MD, MBA and Ross L. McMahon, MD

From the Memorial Sloan-Kettering Cancer Center, Department of Surgery, Minimally Invasive Surgery Program, New York, New York.

Correspondence: Address correspondence and reprint requests to: K. C. Conlon, MD, MBA, Suite C-990, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, NY 10021; Fax: 212-717-3097; E-mail: conlonk{at}mskcc.org

Key Words: Laparoscopy • Surgical oncology • Cancer • Staging

Since the introduction of minimally invasive techniques in general surgery, controversy has existed as to their general applicability to surgical oncological practice. Despite evidence that minimally invasive surgical (MIS) procedures for many benign conditions have led to a reduction in perioperative morbidity and mortality, with a resultant decrease in hospital stay and accelerated return to normal activities, critics have expressed the view that the benefit for patients with cancer is more limited. Staging laparoscopy for diseases such as gastric or pancreatic cancer has been described as somewhat superfluous, given the advances seen in imaging modalities. Additionally, enthusiasm for therapeutic MIS has been somewhat dulled by concerns over possible diminished adherence to surgical oncology principles, as well as by the initial reports of intraperitoneal dissemination of malignancy, most clearly manifested by port site metastases. However, others have argued that for diseases such as upper gastrointestinal cancer, MIS techniques have a clear benefit, not only for diagnosis and staging, but also for palliation and, in selected cases, for therapy.

This article reviews some of the experience collected over the last decade in the management of patients with upper gastrointestinal malignancy and, in so doing, attempts to apply the lessons learnt to the wider population of patients with intra-abdominal malignancy.

GASTRIC CANCER

In the United States, of an estimated 24,000 new cases of gastric cancer, most patients continue to present for treatment with advanced disease.1 Although surgical resection remains the primary therapeutic modality for those patients with localized disease, even those patients with more advanced disease historically have undergone some form of surgical procedure. Recently, improvements in adjuvant therapies, coupled with a better understanding of the natural history of the disease, have resulted in a more selective approach being adopted when considering patients for surgery.2

Patient selection for treatment is facilitated by a sophisticated diagnostic armamentarium (Table 1). Contrast-enhanced computed tomography (CT) currently is the preoperative diagnostic modality of choice. However, as an accurate staging modality it seems somewhat suboptimal, with up to a third of patients considered to have localized disease being noted to have subradiological metastatic disease at the time of surgery.3,4 An argument could be made that the majority of this group would have little to gain from an open procedure and could have benefited from a more accurate staging protocol.


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  		TABLE 1. Diagnostic armamentarium for upper gastrointestinal malignancy
 
Diagnosis and Staging
A number of recent studies have demonstrated that laparoscopy is highly accurate in detecting peritoneal and hepatic metastases in patients with gastric cancer. A summary of these articles is presented in Table 2. Gross et al.5 examined the use of laparoscopy in gastric cancer and found evidence of unresectability in 27 (59%) of 46 patients. Of these 27 unresectable patients, only 2 subsequently required operative bypass as a palliative procedure. A laparotomy was avoided in 52% of patients. Kriplani and Kapur6 reported the use of staging laparoscopy in 40 patients with potentially resectable gastric cancer. In that study, laparoscopy detected metastatic disease in 12.5% of patients. Possik et al.7 reported a study of staging laparoscopy in 360 patients. Staging laparoscopy was 89.4% accurate in detecting peritoneal disease and 96.5% accurate in detecting liver metastasis. In an earlier article from our institution, Burke et al.3 examined 104 patients with potentially resectable gastric adenocarcinoma who underwent staging laparoscopy. All patients were preoperatively staged with noninvasive imaging studies. Laparoscopic exploration was successful in 99% of patients and accurately staged 94% with respect to metastatic disease, with a sensitivity of 84% and a specificity of 100%. Occult metastatic disease was detected in 37% of patients. These data is similar to those reported by Lowy et al.,4 from the M. D. Anderson Cancer Center, who studied 70 patients considered to have resectable disease after radiological imaging. Laparoscopy detected occult metastasis in 23% of patients, only one of whom required a laparotomy for palliative purposes. In a more recent study, Feussner et al.8 analyzed the effect of extended laparoscopic staging after CT and endoscopic ultrasound (US) staging. They found that laparoscopy altered the preoperative staging in 51 of 111 patients, leading to a change in management in 45 (41%) of them. Overall, 17 patients had their disease downstaged, and in 28 the stage of disease was increased. Of the latter group, 26 (23%) were noted to have unsuspected peritoneal disease. Yano et al.9 examined a cohort of patients with biopsy-proven T3 or T4 disease as diagnosed by preoperative CT, US, or magnetic resonance imaging. Overall, 50% had their disease stage altered by the laparoscopic examination: 16% were downstaged and 34% upstaged. Of the 32 patients in this prospective study, 13 (41%) were found to have unsuspected peritoneal disease (Fig. 1).


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  		TABLE 2. Summary of staging laparoscopy studies in gastric cancer
 


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  		FIG. 1. Peritoneal carcinomatosis at laparoscopy for gastric cancer.

 
Laparoscopy, by nature, is a two-dimensional modality with severely limited tactile and depth perception. The use of laparoscopic ultrasonography (LUS) overcomes this constraint to some degree and has potential benefits in gastric cancer, in which the knowledge of T stage may have therapeutic implications. This is of particular importance in centers where a neoadjuvant approach for locally advanced disease is practiced. LUS also allows hepatic lesions undetected by conventional imaging modalities to be identified and biopsied under image guidance. Our initial experience with a high-frequency probe (7–10 MHz) suggested that in pT3 lesions, a concordance of 75% occurred when compared with pathologic findings.10 In the study reported by Feussner et al.,11 LUS seemed to provide additional decisive information in eight patients. Romijn et al.,12 in a small study of 20 patients with adenocarcinoma of the gastric cardia, noted that LUS doubled the number of patients noted to have metastatic disease (from 4 to 8). It is somewhat difficult from the literature to separate whether the benefit of LUS lies in the laparoscopy or the LUS examination itself. Smith et al.13 designed a prospective study to address this issue with a cohort of patients with esophagogastric cancer. In this study, 52 patients with gastric cancer underwent laparoscopic staging. Of those, nine were found to have unsuspected peritoneal disease, and a further three had additional disease detected by LUS alone. This suggests that for detection of metastatic disease, the yield of LUS may be quite limited, with most information being obtained at simple laparoscopy. However, if knowledge of the precise T stage would affect the therapeutic algorithm, LUS seems to have a real role.

Laparoscopy also affords the opportunity to perform peritoneal lavage and obtain specimens for cytological analysis. The presence of free cancer cells in the peritoneal cavity, even in the absence of gross metastatic disease, is a poor prognostic finding.14 We reported a series of 127 patients who had cytology obtained at the time of staging laparoscopy.15 In patients with no evidence of macroscopic metastatic disease, the prevalence of positive cytological washings was 4%, compared with 59% in those who had gross evidence of disease. Irrespective of stage, the presence of positive lavage cytology was associated with a poor survival that was similar to that of patients with stage IV disease. Ribeiro et al.16 noted that patients with intraperitoneal free cancer cells will experience disease recurrence in the peritoneal cavity and have diminished postresection survival compared with those patients noted to be negative for intraperitoneal free cancer cells at the time of resection. Others have reported similar results.14,17–20

Resection
Although laparoscopic staging is now an accepted modality in the assessment of gastric cancer, the same cannot be said for minimally invasive gastric resection. Concern has been expressed as to (1) the adequacy of the resection margin, (2) the ability to obtain appropriate nodal clearance, (3) the potential for malignant dissemination, and (4) appropriate patient selection. Although no randomized data exist, preliminary work has help clarify some of the issues raised.

Improved operative techniques and surgical instrumentation have facilitated the development of MIS gastric surgery. In 1992, Goh et al.21 were the first to report a laparoscopic Billroth II resection for benign disease. Kitano et al.22 are credited with the first reported case of a laparoscopically assisted Billroth I gastrectomy and associated lymphadenectomy for early gastric cancer.

The surgical technique has evolved from these early reports with lessons learnt from experience obtained in laparoscopic bariatric surgery.23 Total and subtotal gastrectomies with associated D1 and D2 lymphadenectomies have now been described. In most cases of subtotal resection, a standard Billroth II gastrectomy is performed with a D1 lymphadenectomy. Newer instrumentation, such as the Harmonic Scalpel® (Ethicon Endo-Surgery, Inc., Cincinnati, OH) or LigasureTM (Valleylab, Boulder, CO), have facilitated hemostatic dissection. Vessel control is achieved by use of an endoscopic vascular stapler and gastric transection performed by multiple firings of the endoscopic stapler (Fig. 2). Reconstruction is performed in a standard fashion in either an antecolic or retrocolic fashion. After resection, the stomach can be placed in an extraction device and removed either piecemeal or by extending one of the port sites en masse.



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  		FIG. 2. Transection of the stomach.

 
In 1997, Goh et al.24 collated multi-institutional data from 118 laparoscopic resections performed, 38% of which were performed for gastric cancer. In this series, the operative procedure was performed totally intracorporeally in 79% of cases. The average duration of the operation was 215 minutes (range, 90–360 minutes), with a mean hospital stay of 8 days (range, 3–30 days). More recent work has confirmed the technical feasibility of the procedure in the hands of surgeons who are experienced in both advanced laparoscopic and open surgery.25–31 Azagra et al.32 reported their experience with 13 patients who had a laparoscopic gastrectomy for gastric cancer. Nine patients underwent a total gastrectomy with D1 nodal dissection, three underwent a total gastrectomy with D2 nodal dissection, and one had a laparoscopically assisted distal gastrectomy. Margins were negative in all cases, with the average number of examined nodes being 31 (range, 25–53). Perioperative mortality related to the procedure was 7%.

Several reports from Japan have detailed experience with laparoscopic resections for early gastric cancer.25,26,28,29,32–42 Shimizu et al.38 retrospectively compared 21 patients undergoing a laparoscopic distal gastrectomy for early gastric cancer with a matched group of 31 patients who underwent a standard open operation during the same time period. Whereas operative time was significantly longer in the laparoscopic group, times to ambulation, return of bowel function, and hospital stay were significantly reduced. More extensive nodal dissections were performed in open surgery, but there was no difference in the number of nodes examined between groups. Although the indication for laparoscopic resection was confined to patients presumed to have intramucosal carcinoma in this study, postoperative histological examination revealed submucosal invasion in six patients (29%). Of these, two patients with poorly differentiated tumors had nodal metastases in the perigastric region. None of the other patients in either group with true intramucosal cancers had nodal involvement. Asao et al.26 also highlighted the importance of preoperative staging. In their report of 49 laparoscopically assisted gastrectomies, the depth of invasion was underestimated in five patients, three of whom had positive perigastric nodes.

So far, all reports of laparoscopic gastric resection for gastric cancer suffer from uncontrolled design, small numbers, and limited follow-up. A number of randomized, controlled trials are ongoing, and the results are awaited with interest. Until the data from these trials become available, laparoscopic gastrectomy should be considered only in select cases. Patients with early mucosal disease seem to be candidates for MIS procedures given the low (<2%) risk of nodal disease. In addition, those patients with advanced disease in whom a palliative resection is considered are also suitable candidates. For the remainder of patients, who currently constitute the majority of our practice, laparoscopic gastrectomy, although it seems safe and oncologically sound, should be recommended only within the confines of investigational trials.

PANCREATIC CANCER

Notwithstanding recent improvements in preoperative, operative, and postoperative care, the prognosis of pancreatic cancer remains bleak. Actual 5-year survival is between 2% and 3%, with surgical resection offering the only chance of cure.43 Most patients continue to present clinically with advanced disease. Despite the recent advances in pancreatic imaging and the development of nonoperative techniques for relief of biliary obstruction, many of these patients still undergo laparotomy for staging and palliation.44 The use of minimally invasive techniques for staging and palliation for this patient population has been described as the most utilitarian application of this technology because it avoids potentially unnecessary surgery. However, considerable controversy currently exists, and consensus is lacking as to its true role.45

Diagnosis and Staging
As with gastric cancer, a myriad of diagnostic modalities are available (Table 1). Of these imaging tests, dynamic multiphase contrast-enhanced thin-cut CT of the pancreas is currently the investigation of choice for preoperative staging. High-quality CT can identify the primary tumor and accurately assess its relationship to major peripancreatic vasculature (Fig. 3). However, it is less sensitive in detecting small-volume hepatic or peritoneal disease. Most of the controversy that exists regarding the role of laparoscopic staging for pancreas cancer revolves around the latter issue. Proponents of laparoscopic staging argue that its added value is between 20% and 30% and that it spares most of these patients unnecessary surgery.43,46–52 Critics dispute this figure, often extrapolating from open surgical data that the yield of laparoscopic staging should be <10% and that it is thus not a cost-efficient use of resources (Table 3). 53–56



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  		FIG. 3. Computed tomographic angiogram of the pancreas, demonstrating an uncinate process tumor in close approximation to the superior mesenteric vein.

 

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  		TABLE 3. Utility of laparoscopy in predicting resectability in pancreatic cancer
 
The aim of laparoscopic staging is to mimic open exploration, allowing patients with resectable disease to proceed to open exploration with a high likelihood of resection and avoiding laparotomy for the group of patients who would not benefit. We favor a multiport technique, which allows for a thorough examination of the peritoneal cavity. A biopsy of peritoneal or hepatic lesions suggestive of disease can readily be performed and, if the results are positive, the procedure is terminated at this point. The liver and hepaticoduodenal ligament and periportal lymph nodes can be biopsied if suspicious. The transverse colon is elevated and the mesocolon and ligament of Trietz examined for tumor infiltration. After this, the left lobe of the liver is elevated and the gastrohepatic omentum divided, facilitating entry into the lesser sac and exposing the caudate lobe, vena cava, and celiac axis (Fig. 4). Celiac, hepatic, portal, and perigastric nodes are sampled if suspicious. Finally, LUS is used to systematically evaluate the liver and the pancreas to evaluate the tumor’s relationship to the major peripancreatic vessels. Patients are considered to have irresectable disease if histological proof is obtained of (1) metastasis (hepatic, serosal, and peritoneal), (2) extrapancreatic extension of the tumor (i.e., mesocolic involvement), (3) celiac or high portal node involvement, (4) invasion or encasement of the celiac or hepatic artery, or (5) tumor involvement of the superior mesenteric artery. Portal or superior mesenteric venous involvement is often a relative contraindication to resection, depending on the degree and extent of involvement.



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  		FIG. 4. Lesser sac and identification of the gastric pillar (left gastric artery and vein).

 
The initial report of our experience with laparoscopic staging of peripancreatic malignancy cited an improvement in resectability, from 50% on the basis of CT scanning alone to >90% when staging laparoscopy was added.57 Since that article, improvements in CT technique, better patient selection, and refinements in surgical technique have reduced the benefit somewhat. However, the yield remains in excess of 25% for patients with adenocarcinoma of the pancreas.43 The predominant sites for subradiological occult metastatic disease remain the liver and peritoneal cavity. Similar results were recently reported by Jimenez et al.,48 who found that 31% of patients undergoing staging laparoscopy had unsuspected metastasis. In their study, laparoscopic staging had a sensitivity of 97% and specificity of 100%. Andren-Sandberg et al.46 suggested that both CT and laparoscopy reliably predicted unresectability. For patients considered resectable after CT examination, 38% were deemed unresectable at the subsequent laparoscopy.

As with gastric cancer, LUS has been advocated as a means to improve on the results of simple laparoscopy. Bemelman et al.58 reported their initial experience with LUS in pancreatic staging, with an improvement in predictive value from 41% with CT alone to 95% when combined with laparoscopy and LUS. Hunerbein et al.59 reported similar results. In this study, of 389 patients with upper gastrointestinal malignancies, laparoscopy and LUS improved staging in 41% of patients; 36% of patients were spared a nontherapeutic laparotomy as a result. Our initial study confirmed the feasibility of the technique but suggested that the added yield was somewhat less than had been previously reported.60 A subsequent prospective study examined the role of LUS in staging pancreatic malignancies in patients deemed to have either resectable or potentially resectable disease on the basis of CT evaluation.61 LUS identified the primary tumor in 98% of patients, the portal vein in 97%, the superior mesenteric vein in 94%, and the superior mesenteric artery in 93%. However, the added value was limited to the group of patients with questionable CT scans identifying four of five patients who were ultimately resected. Others have suggested that LUS should be an integral part of laparoscopic staging because it reliably predicts tumor unresectability, offsetting the tendency of CT and abdominal surface US to overestimate T stage,49 and improves the overall predictive value for defining resectable disease.52

Most of the studies cited previously refer to adenocarcinoma of the pancreas. For other cell types, including neuroendocrine tumors, intraductal papillary mucinous neoplasm, and cystadenocarcinoma, the data are sparse. A review of our experience with laparoscopy in nonfunctioning islet cell tumors found a high incidence of occult metastases.62 CT followed by laparoscopy was significantly more sensitive than CT alone in predicting resectability (93% vs. 50%, P = .03). This resulted from a high false-negative rate on CT for small-volume metastatic disease, with hepatic disease being the most common. The predictive value for tumor resectability was also much higher for CT followed by laparoscopy than for CT alone (95% vs. 74%).

Palliation
Because most patients with pancreatic cancer have unresectable disease at the time of presentation, palliation to minimize symptoms and maximize quality of life has a major goal in the care of these patients. Palliation most often is required for one of three problems: biliary obstruction, gastric outlet obstruction (GOO), and pain.

Obstructive jaundice may occur in up to 70% of patients.63 Before the widespread availability of noninvasive imaging modalities and nonoperative endoscopic means of biliary decompression, relief of biliary obstruction was accomplished at the time of laparotomy. Currently, nonoperative biliary decompression via trans-hepatic or endoscopically placed endobiliary prosthesis has now gained widespread acceptance, with a success rate >90%.44,64 Randomized, prospective trials comparing endoscopic with surgical drainage have shown that endoscopic drainage is associated with a lower early morbidity and mortality, shorter hospital stay, and comparable long-term results.65,66 However, long-term complications of biliary stents, including occlusion, dislodgement, and cholangitis, occur in 13% to 60% of cases.67–70 The use of coated and larger stents has reduced this morbidity.71–74

Although both cholecystoenteric and choledochoenteric bypasses have been performed laparoscopically, the latter is much more difficult technically and requires a high level of laparoscopic skill. A sufficient length of common duct needs to be exposed and a difficult intracorporeal anastomosis between the small bowel and the common duct performed. Cholecystojejunostomy is the more commonly performed laparoscopic procedure (Fig. 5). Patient selection is critical. A low insertion of the cystic duct into the common bile duct and tumor impingement within 1 cm of the duct are predictors of early technical failure. The anastomosis can be performed with either a stapled or hand-sewn technique. Shimi et al.75 reported the first series of five patients who underwent laparoscopic cholecystojejunostomy for advanced pancreatic cancer. Complete relief of jaundice was achieved in 80%.



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  		FIG. 5. Completed laparoscopic jejunostomy anastomosis.

 
The true incidence of symptomatic GOO remains unclear. Traditionally, it was considered that >25% of patients would develop GOO during the course of their illness, and therefore, prophylactic gastric bypass was recommended at the time of exploratory laparotomy. However, as the need for open exploration for staging purposes has decreased, the need for prophylactic bypass has been questioned. Espat et al.76 examined, in a prospective study, 155 patients undergoing laparoscopic staging. In that cohort, 40 patients had locally advanced disease, and 115 patients had metastatic disease. After laparoscopic staging, only 3% of patients required a subsequent open operation for biliary drainage or GOO. A subsequent update of our experience by Brooks et al.77 has confirmed these data. The low incidence of patients requiring operation for symptomatic GOO is consistent with the data seen from the nonoperative groups in the randomized trials of endoscopic biliary drainage versus surgery. In contrast, a recently completed randomized trial from Johns Hopkins78 found that in 8 (19%) of 43 patients randomized to no prophylactic gastroenterostomy, late GOO developed that required therapeutic intervention. These data suggest that the issue remains unresolved and requires further study.

A laparoscopic gastroenterostomy is a relatively straightforward procedure. Wilson and Varma79 reported the first laparoscopic gastric bypass in two patients with malignant duodenal obstruction. Nagy et al.80 reported a series of laparoscopic antecolic loop gastrojejunostomies. Nine of ten patients in this series had GOO from pancreatic malignancy. The laparoscopic method was successful in 90%. There was no postoperative morbidity or mortality associated with the laparoscopic technique.

Resection
In contrast to gastric resection, laparoscopic surgical resection of the pancreas remains purely investigational. The morbidity and mortality associated with pancreaticoduodenal resection have decreased over the last decade. Most specialized centers now report mortality figures <5%. However, morbidity remains quite high. In a recent randomized, prospective trial assessing the role of intra-abdominal drainage after pancreatic resection, we noted a complication rate of 57%. The majority of noncardiac complications could be related to the pancreaticojejunal anastomosis. Given the difficulty associated with performing this anastomosis in an open setting and the relatively crude laparoscopic instruments, it is unclear what, if any, benefit a laparoscopic approach would have. Gagner and Pomp81 are credited with performing the first laparoscopic pancreaticoduodenectomy in 1993 for chronic pancreatitis. Jossart and Gagner82 subsequently reported their further experience with 10 attempted laparoscopic procedures. Eight of these procedures were for malignant disease (four pancreatic cancers, three ampullary carcinomas, and one cholangiocarcinoma). The open conversion rate was 40%. Comparing those cases completed laparoscopically with those converted, the average operating time was 8.5 vs. 4.6 hours, and the average hospital stay was 22.3 vs. 20.1 days. Three of the laparoscopic group had complications (50%) versus none in the converted group.

HEPATIC CANCER

Diagnosis and Staging
As with gastric and pancreatic cancer, surgical resection remains in most instances the most effective modality for both primary and metastatic disease of the liver. Although hepatocellular carcinoma (HCC) is one of the most common malignancies worldwide,83 currently in the United States the most frequent presentation to the surgical oncologist is that of metastatic colorectal carcinoma (CRC). An estimated 135,400 new cases of CRC are seen annually.84 Of these, it is expected that 50,000 will develop metastatic disease to the liver.85 Approximately 5% to 10% are considered potential candidates for resection.86 With few exceptions, hepatic resection is indicated only in patients with no extrahepatic disease and a controlled primary tumor, in whom a complete tumor resection can be achieved while leaving a sufficient remnant of liver for adequate recovery and function. As with other gastrointestinal malignancies, imaging modalities such as CT, magnetic resonance imaging, and PET scanning are used as preoperative staging modalities. Despite improvements in imaging technology, a significant number of patients continue to have unresectable disease at laparotomy.87–89

Similar to gastric and pancreas cancer, MIS techniques have been used as a staging procedure before open exploration. The perceived benefits of MIS staging of hepatic malignancies are similar to those observed in other tumors: more accurate assessment of disease extent, a reduced hospital stay, decreased morbidity, and a decreased delay in initiation of adjuvant or alternative therapies.

Table 4 lists some of the contemporary studies that have examined the role of MIS staging in hepatic malignancies. John et al.,49 in a series of 50 patients, demonstrated that a nontherapeutic laparotomy was avoided in 64%. Similarly, in a report from our institution, Jarnagin et al.90 examined 104 patients who underwent MIS staging. In this series, 25% of patients, despite negative radiological studies, were found to have unresectable disease at laparoscopy. Overall, laparoscopy was successful at determining unresectability in 68% of patients and avoided a nontherapeutic laparotomy in 45% of cases. The yield was greatest in detecting peritoneal disease, additional hepatic tumors, and unsuspected hepatic cirrhosis but often failed to identify unresectability due to extensive biliary involvement, extrahepatic nodal disease, or vascular involvement. Laparoscopic staging significantly improved the resectability rate and reduced the length of hospital stay and hospital-related charges. When patients undergoing laparoscopic staging alone (n = 17) were compared with those who underwent an open exploration (n = 19), no difference in operating room time was noted. However, the laparoscopic group had a significant reduction in both hospital stay and total hospital charges. The hospital room and board charges were 60% less in the laparoscopic group.


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  		TABLE 4. Summary of staging laparoscopy studies in hepatic malignancies
 
In a subsequent report, Jarnagin et al.91 used a previously described preoperative clinical risk score (CRS) scoring system92 to identify those patients with potentially resectable hepatic colorectal metastases who would benefit from MIS staging. Criteria such as the presence of positive lymph nodes, a disease-free interval of <12 months, more than one hepatic lesion, size >5 cm, and a carcinoembryonic antigen level of >200 ng/mL were scored. In patients with a CRS <2, occult metastatic disease was noted in 12%, compared with 42% in those with a CRS >2 (P = .001).

Other authors have emphasized the added value of LUS in staging. Callery et al.93 described their experience with 50 consecutive patients with hepatobiliary and pancreatic malignancy. Laparoscopy alone demonstrated previously unrecognized occult metastases in 11 patients. In 11 other patients in whom the laparoscopy was considered normal, the addition of LUS identified disease that precluded resection. Barbot et al.94 noted that laparoscopy staging alone had a specificity of 40%. However, the addition of LUS increased this to 75%. In 11 of 15 patients, the preoperative plan was changed solely on the basis of the intraoperative LUS findings. Similar results were reported by Rahusen et al.,95 who examined the role of LUS in patients with CRC metastasis to the liver who were considered to have resectable disease by conventional imaging modalities. With standard laparoscopic staging, 13% of patients were found to have disease that precluded resection. The addition of LUS increased the unresectability rate to 25%. In a prospective study, Foroutani et al.96 compared triphasic CT with LUS. Fifty-five patients were noted to have 222 lesions. LUS detected all 201 lesions seen on CT and identified 21 additional tumors in 11 patients. The authors suggested that their experience argued for more widespread use of LUS in laparoscopic staging procedures.

The role of staging laparoscopy in potentially resectable noncolorectal nonneuroendocrine liver metastasis was evaluated by D’Angelica et al.97 After imaging studies, 30 consecutive patients considered to have resectable disease underwent staging laparoscopy. Despite prior surgery, staging was completed in 80% and correctly identified six of the nine patients eventually found to have unresectable disease. The authors concluded that the addition of staging laparoscopy identified the majority of patients with unresectable disease in the setting of noncolorectal nonneuroendocrine liver metastasis.

The studies cited previously have mainly focused on metastatic disease to the liver. However, Lo et al.98 examined the role of LUS in the staging of patients with HCC. In this study, 1741 patients with HCC were seen over a 10-year period. The authors compared the prelaparoscopic (before 1994) and postlaparoscopic eras. The addition of LUS significantly improved resectability rates, avoiding exploratory laparotomy in 63% of patients with unresectable disease. In common with the experience noted previously for metastatic disease, operative time and hospital stay were noted to be significantly reduced.

Radiofrequency Ablation
Tissue ablation by means of either cryotherapy or interstitial radiofrequency ablation (RFA) has been described. Laparoscopic cryoablation has been proposed for both primary and metastatic disease.99–104 This technique has been demonstrated to be feasible and safe. However, technical difficulties related to image guidance and the maintenance of hemostasis after creation of the ice ball have limited application of the laparoscopic technique. Increasing attention has been focused on thermal energy sources.

RFA, which was first demonstrated by d’Arsonval in 1891, has undergone recent refinement, making it a viable modality for the treatment of hepatic metastases. The thermal effect produced from the alternating current of high-frequency radio waves (460–480 kHz) emitted from electrodes placed in an array leads to local tissue destruction. Precise control of tissue destruction can be achieved by controlling local temperature and electrical resistance. Technological advances have allowed the delivery of the RFA probe to be performed laparoscopically under LUS guidance.

An initial report by Cuschieri et al.100 examined the safety and efficacy of LUS-guided laparoscopic RFA. In this series, two patients with an isolated HCC and eight patients with multiple lesions from metastatic CRC were included. Total ablation with at least a .5-cm margin was achieved in all HCC patients and in seven of eight of the metastatic CRC patients. No complications were observed. At the time of the article, one patient had died of disease, eight were without evidence of disease, and one had developed new metastatic deposits. Siperstein et al.103 described their experience with laparoscopic RFA of primary and metastatic liver tumors. In this retrospective study, 250 lesions were treated in 66 patients. There were 79 neuroendocrine metastases, 64 metastatic adenocarcinomas, 27 other metastases, and 11 primary hepatic tumors. A partial radiological response was noted in 156 (88%) of 178 lesions in patients observed for at least 3 months. Of 22 local recurrences, 14 lesions increased in size, and 8 lesions showed multifocal recurrence that encroached on ablated foci. Variables such as histology (adenocarcinoma or sarcoma [18 of 22 treatment failures, P < .05]), larger tumors, and vascular invasion on LUS were considered poor prognostic variables. Most treatment failures were apparent by 6 months.

The technique of laparoscopic RFA has also been applied to patients with cirrhosis. Montorsi et al.105 reported a pilot study of laparoscopic RFA in patients with HCC and documented cirrhosis who were not eligible for resection. The majority of patients had Child’s class A disease. More extensive disease was seen at laparoscopy in 19%. A total of 44 lesions were treated with postprocedure CT scanning at 1 month, demonstrating a complete radiological response in 89%. There was no procedure-related mortality, and complications were minor, including trocar site hematoma (14%) and mild ascites (7%). Whether laparoscopic tumor ablation offers any advantages over the percutaneous route remains to be seen and awaits further study.

Resection
An interesting development has been recent articles detailing early experience with laparoscopic hepatic resection. As with other laparoscopic solid-organ resection, concerns exist concerning the adequacy of the resection and the possibility of inadvertent tumor dissemination. In addition, hepatic resection has been hampered by anatomical and size considerations. Although evidence regarding safety and efficacy awaits ongoing prospective trials, early data are intriguing, suggesting that in selected cases an MIS approach has potential applicability.106–116

The use of a hand-assisted technique and improved instrumentation has partially overcome some of the technical concerns regarding the procedure (Fig. 6). Tactile sense is restored and dissection facilitated by use of the surgeon’s hand. Instrumentation such as the US dissector and the development of angled staplers have greatly assisted parenchymal dissection and control of large vessels. However, despite these improvements, laparoscopic hepatectomy is generally limited to segments II, III, IVb, V, and VI, with inferior and peripheral lesions most amenable to resection.



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  		FIG. 6. Hand-assisted hepatectomy. Reprinted with permission from Archives of Surgery; Copyright © American Medical Association 2000. All rights reserved.113

 
Our initial institutional experience with a hand-assisted technique was reported by Fong et al.113 Eleven patients underwent laparoscopic evaluation and attempted resection over a 12-month period. Resection was successfully completed in five patients. For these patients, the median operative time was 248 minutes, and the median hospital stay was 5 days. Failure was due to anatomical location, extensive adhesions, or an inability to adequately palpate the lesion. A hand-assisted technique was used in all completed cases. The hand port was usually placed ipsilateral to the tumor, such that the hand could be used for lateral retraction of the liver and to assist in parenchymal transection. Ligamentous attachments were divided, and a Pringle maneuver was accomplished by using a bulldog clamp inserted through the hand port. The capsule of the liver along the line of transection was scored with cautery, and the parenchymal dissection was accomplished by using a combination of finger fracture and harmonic and sharp dissection. Endoscopic clips were placed on biliary and vascular structures, and major vessels were controlled by use of an endoscopic vascular stapler. Hemostasis along the raw liver surface was achieved by use of a laparoscopic argon beam coagulator. The specimen was placed in an extraction device and removed from the abdomen via the hand port site. Two patients had a postoperative complication (bile leak and Clostridium difficile colitis). Resection margins were negative in all cases.

Our early experience suggests that resection is both feasible and safe in selected cases. Others have reported similar results. In a prospective study, Cherqui et al.111 examined the results of laparoscopic liver resection in 30 patients, representing 19% of all liver resections performed in their institution during the study period. In general, tumors were small (<5 cm) and peripheral. A multiport laparoscopic technique was described. Segmental or nonanatomical resections were performed. Clear margins were obtained in all cases, and perioperative morbidity was low (20%). There were no deaths. Twelve patients had malignant disease. At a mean follow-up of 12 months, no evidence of port-site metastases were seen in this group of patients. The feasibility of the technique was also noted by Descottes et al.,117 who described 15 patients who underwent 16 laparoscopic liver resections for benign and malignant disease. Most patients (93%) underwent minor hepatic resections (segmentectomies, subsegmentectomies, or nonanatomical resections), with only one patient requiring open conversion to obtain a negative resection margin. Rau et al.115 compared 17 patients who underwent laparoscopic resection with a closely matched control group who underwent conventional open surgery. One patient in the laparoscopic group required open conversion. The operative time was significantly increased in the laparoscopic group; however, hospital stay was reduced.

Hashizume et al.112 presented one of the largest reports to date, including 70 liver resections performed laparoscopically or laparoscopically assisted. Although not rigorously reported, the majority of patients selected seemed to have HCC with mild cirrhosis or chronic hepatitis and CRC metastasis. A total of 32.2% were for benign conditions, 43% had formal lobectomies, and most the remaining patients had segmentectomies. One death was reported because of liver failure on day 1. CO2 embolism was documented in one patient, and biliary fistula occurred in one patient.

SUMMARY AND FUTURE DIRECTIONS

MIS has now become an integral part of the surgical oncologist’s armamentarium. In esophagogastric and hepatic malignancy, there is little argument as to the efficacy of laparoscopic staging before open exploration. In pancreatic cancer, controversy still exists as to its true role. In centers such as ours, in which a nonoperative approach is preferred for biliary obstruction and prophylactic gastric bypass is not recommended, the added value of laparoscopy seems compelling. Modern state-of-the-art imaging studies do not as yet have the resolution to detect the small-volume metastases seen in up to 20% patients at either laparoscopic or open exploration. Multiple studies have demonstrated that laparoscopy can avoid laparotomy in this group of patients. What is unclear, however, is whether this affects either quality-of-life measures or the use of adjuvant therapies. Studies are ongoing to help answer these questions.

With regard to therapeutic intervention, it is probable that advances in technology will only increase the utility of MIS. Improved optics and advances in image guidance and robotics, coupled with the development of novel therapeutic agents derived from our increased knowledge of the biology of cancer, will affect the field. It is not too far-fetched to envision combined interventional radiology and MIS techniques that allow us perform treatments and resections considered technically impossible today.

But what should we do today? Nonrandomized studies suggest that laparoscopic surgery is oncologically sound, but randomized data are lacking. It is reasonable to suggest that while we await the results of the studies in colon and endometrial cancer, patients with these diseases should undergo curative resection under protocol. However, level I evidence will never be available for most other tumor types. For patients with these tumors, a cautious approach is currently warranted. Individuals should be counseled on existing basic science and clinical data, and a decision should be made on whether or not to proceed on a case-by-case basis.

Received for publication February 22, 2002. Accepted for publication April 25, 2002.

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