Staging of Intra-Abdominal Malignancy Kevin C. Conlon, MD, FACS, and Sean M. Johnston, MD, FRCSI (gen)
n current clinical practice, management strategies for intra-abdominal malignancies have become increasingly sophisticated. As a result, it is critically important that disease staging be accurate and effective. Despite the many preoperative radiological staging modalities available such as computerized tomographic scanning (CT), magnetic resonance imaging (MRI), and positron emission tomography (PET), there often exists a small but significant margin of error between preoperative diagnosis and surgical findings at laparotomy. Since the mid1990s a significant amount of data has been produced to suggest, that the use of laparoscopy and laparoscopic ultrasound in the staging of intra-abdominal malignancies has the ability to reduce this margin of error and have a positive impact on overall management.1-4 The aim of laparoscopic staging is to mimic open exploration while avoiding unnecessary intervention, and allowing for quicker administration of adjuvant therapies if required. Laparoscopic staging should be viewed as complementary and not as a replacement for other modalities such as CT and MRI. With respect to intra-abdominal malignancies, such as gastric, pancreaticobiliary and hepatic, recent data has suggested a continued role for laparoscopic staging in the assessment of patients with these diseases. Laparoscopy and laparoscopic ultrasound is now commonly utilized in these malignancies to assess: 1. Resectability 2. Staging of locally advanced disease before chemoradiation 3. Diagnosis and histological conformation of radiologically suspected metastatic disease As with laparoscopy for benign disease there are few absolute contra-indications for the procedure apart from the patient who is deemed unfit for general anesthesia or has an ongoing bleeding diathesis. The main relative contraindications to laparoscopic staging for upper gastrointestinal malignancy include:
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From the Department of Surgery, The Adelaide and Meath Hospital, Incorporating the National Children’s Hospital, Dublin; and the University of Dublin Trinity College Dublin, Dublin, Ireland. Address reprint requests to Kevin C. Conlon, MD, FACS, Chair of Surgery, Professorial Surgical Unit, The Adelaide and Meath Hospital, Tallaght, Dublin 24 Ireland. © 2004 Elsevier Inc. All rights reserved. 1524-153X/04/0601-0003$30.00/0 doi:10.1053/j.optechgensurg.2004.01.002
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1. Multiple previous upper abdominal operations 2. Ongoing intra-abdominal sepsis 3. Pregnancy The following equipment is considered necessary for laparoscopic staging: 1. 30 degree angled laparoscope either 10 mm or 5 mm in diameter 2. 5 mm laparoscopic instruments including a. Maryland dissector b. Blunt tip dissecting forceps c. Cup-Biopsy forceps d. Atraumatic grasping forceps e. Liver retractor f. Scissors 3. 5 mm or 10 mm suction device 4. A laparoscopic ultrasound probe is optional (see below)
OPERATIVE TECHNIQUE In general, for intra-abdominal staging the patient is positioned supine on the operating table. A warming blanket is placed underneath the patient who is secured appropriately to the table with pressure points appropriately padded. Laparoscopy is performed under general anesthesia using a multiport technique. An open technique for placement of the initial trocar usually in the infra-umbilical area is preferred. However, for patients with a history of a prior laparotomy an open cut-down in either the right or left upper quadrant may be performed. This is particularly useful in patients with hepatic disease who have had a prior open colectomy. A Verres needle can also be used to obtain initial pneumoperitoneum. If using such a technique in patients with a history of prior abdominal surgery, care is required to avoid visceral injury. In these cases in particular, it is our preference to use an open technique allowing the peritoneum to be opened under direct vision. A blunt port is inserted and secured in place with two stay sutures. Pneumoperitoneum is achieved with CO2 gas. Initial insufflation should be at low flow rates until peritoneal entry is confirmed. An intraperitoneal pressure of 10 to 12 mmHg is considered optimal for the examination. Occasionally in elderly patients a lower maximum pressure will be set. A 30° telescope is inserted and an initial examination of the peritoneal cavity performed. Additional trocars are then inserted. The size and actual position of these trocars is determined by the site of
Operative Techniques in General Surgery, Vol 6, No 1 (March), 2004: pp 4-12
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left upper quadrant allowing for assessment of the ligament of Treitz, proximal jejunum, and transverse mesocolon as demonstrated in Fig 5. Following examination of the mesenteric root and the ligament of Treitz, the patient is returned to the supine position. For patients with gastric or pancreatic lesions, attention is turned to the gastro-hepatic omentum. The left lateral segment of the liver is elevated by use of a retractor inserted through the left upper quadrant port. Operating instruments are inserted via the right upper quadrant ports and the gastro-hepatic omentum is incised allowing entry into the lesser sac (Fig 6). If present, an aberrant left hepatic artery should be identified and preserved. The caudate lobe of the liver is clearly seen; further posteriorly lies the inferior vena cava. The neck and body of the pancreas and posterior gastric wall can also be inspected. Often adhesions between the stomach and pancreas require division to facilitate this part of the examination. By elevating the stomach the “gastric pillar” can clearly be appreciated as shown in Fig 6. This pillar contains the left gastric artery and vein. By following this
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Port position for Pancreatic and Gastric Cancer staging (10 mm subumbilical blunt camera port, 10 mm port in the right upper quadrant placed laterally). This port is utilized for liver retraction and for insertion of the laparoscopic ultrasound. Additional, 5 mm ports are placed in the left upper quadrant midclavicular line and in the right upper quadrant as demonstrated.
the tumor and the initial examination findings. In general, ports are placed along the planned open incision line as shown in Figs 1 and 2. After the initial visual examination, a detailed examination of the abdominal cavity is performed which mimics that performed during open exploration. The principle of this examination is to identify and biopsy any overt metastatic disease within the peritoneal cavity as shown in Fig 3A,B. Following initial inspection, the patient is tilted approximately 10° head up. Examination of the liver begins with the anterior aspect of the left lateral segment (segments 2 and 3) as shown in Fig 4A,B. Despite the absence of tactile sensation “indirect” palpation of the liver surface can be achieved by using two instruments as shown in Fig 4A. The blunt suction device is particularly useful for compressing liver tissue. Small metastases can be detected in this manner. On completion of the liver examination, the patient is placed in approximately 10° Trendelenberg position. The omentum and transverse colon are elevated toward the
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Port placement for staging Hepatic malignancy. Metastatic colorectal disease to the liver is the commonest indication for laparoscopic staging of liver tumors in the United States. As these patients in general have had prior open surgery a right subcostal cut down is the preferred means of access to the peritoneal cavity. Additional ports are inserted along the line of incision as shown.
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10-mm port. In general, we prefer to use the lateral port in the right upper quadrant. This allows for excellent examination of the liver (Fig 8), hepatoduodenal ligament (Figs 9 and 10), stomach and pancreas. To examine the stomach, 500 mL of warmed saline is inserted into the stomach. The resultant distention facilitates examination of the anterior and posterior walls. The liver is examined sequentially with particular attention paid to the areas not seen on the standard laparoscopic examination. Suspicious lesions can be biopsied either by fine needle aspiration (FNA) or with a percutaneously inserted Tru-cut needle. Duplex scanning is useful to enable identification of vessels particularly in the hepato-duodenal ligament and around the pancreas (Fig 10). The relationship of the primary tumor to the surrounding vessels can be determined.
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(A) Peritoneal metastases (blue arrow). Biopsy of suspicious peritoneal lesion (blue arrow). (B) Note also ascitic fluid present at hepatic flexure (red arrow).
structure down the celiac axis is appreciated and any suspicious nodal tissue can be biopsied. The hepatic artery is also identified and followed to the hepato-duodenal ligament. Again, any suspicious nodal tissue can be biopsied if required. In the case of both gastric and pancreatic cancer it is our practice to perform peritoneal lavage for cytological analysis. In general, specimens are taken at the start of the laparoscopic examination to avoid potential contamination from tumor manipulation or dissection. Between 200 mL and 400 mL of saline is placed into the peritoneal cavity. The abdomen is gently agitated before aspiration. In pancreatic cases samples are taken from the right and left upper quadrants (Fig 7). An additional sample is taken from the pelvis in patients with gastric cancer as this has been shown to increase the diagnostic yield. If available, laparoscopic ultrasonography (LUS) can be performed at this stage. The probe can be inserted via a
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(A) Examination of the left lateral hepatic sector (segments 2 and 3). (B) Examination of inferior aspect of the right hepatic lobe. GB ⫽ gallbladder, HDL ⫽ hepatoduodenal ligament, TC ⫽ Transverse colon. A metastastic lesion can be seen lateral to the hepatoduodenal ligament.
Staging of Intra-Abdominal Malignancy
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The transverse colon has been elevated caudally revealing the mesenteric root and ligament of Trietz.
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Examination of the lesser sac.
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Sites for aspiration cytology (pancreas 1, 2, gastric 1, 2, 3).
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Laparoscopic ultrasound of the Liver. A 10 mm linear array laparoscopic ultrasound probe is placed over the surface of the live in similar fashion to the initial palpation described in Fig 4A,B.
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Staging of Intra-Abdominal Malignancy
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LUS assessment of hepato-duodenal ligament and pancreas.
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LUS image (reversed image) of the hepatoduodenal ligament showing a distended common bile duct (red arrow), cystic duct (blue arrow), portal vein (yellow arrow) and abnormal right hepatic artery (purple arrow).
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RESULTS No randomized control trials exist to assess the utility of laparoscopic staging for gastrointestinal malignancy. However, recent published data can be used to suggest possible benefits and define the limitation for the modality.
Gastric Cancer Traditionally, the majority of patients with gastric cancer underwent some form of operative procedure. However, recent experience has suggested that those patients with metastatic disease at presentation do not require a gastrectomy for palliation. Laparoscopic staging can identify patients with subradiological disease allowing them to avoid laparotomy and proceed to systemic therapies. The issue of subradiological disease has been addressed by a number of authors.5-7 Gross and co-workers, reported that laparoscopy identified metastatic disease in 57% of patients that had a prelaparoscopic staging status of M0. In an early study, Possik noted in a series of 360 patients who underwent laparoscopic staging an accuracy of 89% and 96%, respectively, for the detection of peritoneal and hepatic metastases. More recently Stell8 and others reported a prospective study evaluating the efficacy of laparoscopy, US, and CT in the staging of gastric cancer. Laparoscopy had an accuracy rate of 99% for the detection of hepatic metastases compared with 76% and 79% for CT and US, respectively. The sensitivity for laparoscopy was 96% versus 37% and 53% for US and CT. With regard to the diagnosis of peritoneal metastases, the accuracy rate was 94% for laparoscopy, 84% for US and 81% for CT. D’Ugo and co-workers prospectively assessed the diagnostic accuracy of laparoscopy compared with CT and US in 100 patients. Laparoscopy demonstrated 21 unsuspected metastases (21%) in 100 patients with M0 disease. Laparoscopy demonstrated 100% accuracy for M staging with an over all TMN staging accuracy of 72% compared with 38% for US/CT.9 A recent study by Lehnert10 and colleagues looked at 120 consecutive patients with gastric cancer. There were 15 patients who underwent laparoscopy because of an inconclusive preoperative diagnosis regarding liver metastases, peritoneal metastases, or local infiltration. In 6/15 patients unconfirmed liver or peritoneal metastases were identified and laparotomy prevented. Walkelin and co-workers11 examined 36 patients with adenocarcinoma of the proximal stomach or esophageal junction who were considered to have potentially resectable localized disease. Preoperative evaluation included contrast-enhanced CT, EUS, and laparoscopy with LUS. Locally advanced (T3/T4) tumors were accurately identified by CT in 94% of cases while EUS and LUS accurately identified tumor in 88% and 83%, respectively, in those tumors that could be traversed by the endoscope (14/16) and were below the diaphragm (10/12). Tumors above
the diaphragm were not visualized by LUS. In common with other published reports, EUS in this study remained the best modality for identifying early tumors compared with CT or LUS (64%, 38%, and 57%). The identification of occult nodal disease remains problematic. CT has a reported accuracy of 25% to 70%. With respect to EUS Wakelin and co-workers report an overall accuracy rate of EUS in nodal staging for proximal or EG junction tumors of 72%. If nontraversable tumors are excluded this increases by approximately 10%. Similar results have been reported for LUS with accuracy rates of 60% to 90% reported. LUS can also direct biopsy of suspicious nodes, which improves the utility of the modality.
Pancreatic Cancer Patients with pancreatic cancer have potentially the most to benefit from accurate staging. As with gastric cancer the notion that all patients require an operative procedure for palliation no longer is true. Our understanding of the natural history of the disease coupled with improvement in endoscopic and laparoscopic palliative techniques means that effective palliation does not require an open operation. Proponents of laparoscopic staging suggest that in combination with contrast-enhanced CT and/or MRI laparoscopic staging can prevent needless open surgery for those who would not benefit while not precluding resection for appropriate candidates. An early report from the Memorial Sloan-Kettering Cancer Center experience with laparoscopic staging of peri-pancreatic malignancy cited an improvement in resectability from 50% based on CT scanning alone, to over 90% when staging laparoscopy was added.12 While recent improvements in CT technique, better patient selection and refinements in surgical technique have reduced the benefit somewhat, the added value of laparoscopic staging remains between 15% to 20% for patients with adenocarcinoma of the pancreas. The utility of laparoscopic ultrasound remains unclear. Early work suggested that combined with multiport laparoscopic staging the added value was less than 10%. However, Vollemer and coworkers have recently reported an improvement in resection rates using LUS (84% with lap staging vs. 58% without).13 Further data are required before the true utility of this modality is understood. With respect to other pancreatic tumors such as neuroendocrine tumors, intraductal papillary mucinous neoplasm, and cystadenocarcinoma, the data are sparse for laparoscopic staging. Hockwald14 and co-workers examined a group of patients with islet cell tumors and found a high incidence of occult metastases at laparoscopy. CT followed by laparoscopy was significantly more sensitive than CT alone in predicting resectability (93% vs. 50%). CT failed in particular to identify low volume hepatic disease. The predictive value for resectability was also
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much higher for CT in combination with laparoscopy than for CT alone (95% vs. 74%). Patients with distal bile duct tumors also appear to benefit from laparoscopic staging both in terms of determining respectability and avoiding unnecessary surgery.15 In contrast those patients with known duodenal or ampullary tumors gain little added value from laparoscopy as the incidence of occult disease is low and overall resectability rates high.
Hepatic Disease Regarding the issue of colorectal metastases to the liver, Rahusan16 studied the role of LUS in patients who were considered by preoperative imaging studies to have resectable disease. Laparoscopy determined that 13% of patients had previously occult disease that precluded resection. The added value of LUS in this study was 12%. The addition of LUS to the staging armamentarium appeared to increase resectability rates from 46% to 71% thus sparing approximately one-third of patients an unnecessary open procedure. Similar results were reported by Metcalfe and co-workers who suggested that laparoscopic staging detects the majority of disease, which would preclude an experienced surgeon performing an hepatic resection.17 In an attempt to improve the selectivity of laparoscopic staging, Jarnagin and colleagues attempted to identify a group of high-risk patients who would benefit from the procedure.18 Patients were assigned a clinical risk score (CRS) based on five factors related to the primary tumor and the hepatic disease. The likelihood of finding occult unresectable disease and the yield of laparoscopy were analyzed. The authors determined that the likelihood of occult unresectable disease in those patients with a score ⬍ or ⫽ 2 was 12%. If the score was ⬎2 the yield increased to 42%. The authors concluded that if laparoscopy was performed only in high-risk patients (CRS ⬎ 2) the number of laparoscopic staging procedures could be reduced and net savings doubled. Laparoscopy has also been used in hepatocellular carcinoma. An early study by Lo19 and co-workers using laparoscopy and LUS to stage patients with hepatocellular carcinoma has shown that the use of these two techniques reduced the rate of unnecessary laparotomy by 60%. In a more recent report from Jarnigan and co-workers20 in which 104 patients underwent MIS staging, 25% of patients with potentially resectable disease were found to have disease at laparoscopy which precluded resection. Overall, laparoscopy predicted unresectablity in 68% of patients and avoided unnecessary laparotomy in 54%. This study demonstrated increased resectability rates and reduced hospital costs for the group who underwent laparoscopic staging. Other groups have emphasized the added value of LUS in this patient population. Fortoutani21 noted that LUS offered increased sensitivity over
CT. The added yield of LUS was approximately 10% over CT in detecting hepatic lesions. In a heterogenous patient population with malignant liver disease from the United Kingdom, Hartley and co-workers demonstrated that LUS was equivalent to MRI in determining resectability.22 Vascular involvement or extensive biliary involvement despite the use of LUS, however, proved difficult to evaluate. This benefit was more apparent in primary hepatic tumors compared with metastatic tumors.
SUMMARY Laparoscopy is no longer a tool of limited use and now has widespread indications within surgical oncological practice. It now has proven benefit in the detection and staging of gastrointestinal malignancies, saving a small but significant number of patients with unresectable disease from unnecessary laparotomy. In selected patients combined with state of the art radiological modalities, it appears safe and cost-efficient.
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