The staging of gastrointestinal malignancies aims to ensure that each
patient receives the most appropriate treatment with minimal
morbidity and in a cost-effective manner. Thus, the goal of staging
is to distinguish patients who have a potentially resectable
localized tumor from those with advanced disease and/or distant
metastases. Accurate staging has become increasinglyimportant in view
of the increasing alternatives for neoadjuvant therapy and
nonoperative palliative procedures.
The options available for the evaluation of patients suspected of
having a gastrointestinal tract malignancy are numerous and often
expensive. To identify and stage a solid organ malignancy,
noninvasive tests, such as ultrasonography or computed tomography
(CT), are rational initial studies. Since a tissue diagnosis is
nearly always necessary, endoscopy is clearly the first line of
investigation for patients who may have a carcinoma originating in a
hollow viscus. Once a malignancy is identified, a multitude of
additional studies may be obtained to determine the stage and
resectability of the disease.
Despite current technologic sophistication, preoperative imaging
methods are still far from optimal. Significant disparity often
exists between the results of preoperative investigations and
findings at exploratory laparotomy. Preoperative understaging may
result in the termination of a planned "curative"
resection, thereby subjecting the patient to some additional physical
and psychological morbidity. It is clear that the ideal staging
modality approaches the sensitivity and specificity of exploratory
laparotomy and yet is less invasive and has minimal risks.
With the resurgence and improvement of laparoscopy over the past 10
years, this technology is evolving as an ideal tool for staging
intraabdominal malignancies. Laparoscopy may be useful in procuring
tissue for the definitive diagnosis of malignancy, as well as in
determining the extent of disease following the identification of a
tumor. Although laparoscopy is more invasive than other imaging
modalities, it has better sensitivity and specificity. Moreover, with
the advent of laparoscopic ultrasonography, the accuracy of
laparoscopy in the assessment of solid organs is even greater.
Enthusiasm for laparoscopic staging should be tempered by the view
that it should be performed only if the information provided will
influence the treatment plan, however. Any patient in whom a
laparotomy must be performed, regardless of the findings of
laparoscopy should not be considered a candidate for this staging technique.
This article reviews the current status of laparoscopy in the staging
of gastrointestinal malignancies and attempts to demonstrate how the
advancement of this technology is beneficial to the field of oncology
and, most importantly, to the cancer patient. New developments and
future applications are also discussed, since the rapid progression
of laparoscopic techniques will undoubtedly lead to many future
improvements in the diagnosis, staging, and treatment of cancer.
Table 1 lists the basic instruments
needed to perform laparoscopic staging procedures.
The periumbilical area is the usual insertion site of the initial
trocar for the creation of a pneumoperitoneum. Although a history of
prior abdominal surgery is not a contraindication to laparoscopy, an
alternate initial trocar site may be necessary if there are surgical
scars, masses, or organomegaly. The Veress needle may be used for
most patients, but insertion of a blunt cannula under direct vision
using the "open" technique is the preferred method for
patients who have undergone a previous laparotomy.
In patients with ascites, the Trendelenburg position should not be
used for the establishment of a pneumoperitoneum since, in this
position, loops of the small intestine are likely to be located
adjacent to the anterior wall of the lower abdomen. Instead, the
patient should be placed in the reverse Trendelenburg position to
allow the small intestine to float cephalad to the surface of the
ascitic fluid, thereby limiting the possibility of intestinal injury
when the Veress needle is introduced.
Inspection of the Peritoneal Cavity
The initial step in staging laparoscopy is meticulous inspection of
the four quadrants of the peritoneal cavity, which, if done properly,
can identify serosal implants as small as 1 mm. To facilitate
visualization, any ascitic fluid should be aspirated and sent for
cytology prior to inspection. However, if laparoscopic
ultrasonography is planned during the evaluation, it should be
performed before aspiration, as the ascitic fluid is an excellent
medium for the transduction of ultrasonic sound waves.
Changing the position of the operating table facilitates
visualization of most areas of the peritoneal cavity, including the
paracolic gutters, esophageal hiatus, greater curvature of the
stomach, spleen, and pelvis. The insertion of two or three additional
trocars permits the manipulation of the stomach and transverse colon
so that the lesser sac can be entered and the retrogastric area,
including the body and tail of the pancreas, can be inspected. The
remainder of the retroperitoneum and pouch of Douglas are also
assessed at this time.
In female patients, transvaginal insertion of a uterine manipulator
may be necessary for complete inspection of the pelvis. As in open
operations, the small intestine and its mesentery are routinely
inspected from the ligament of Treitz to the ileocecal valve.
Recently introduced flexible-tip laparoscopes now permit
visualization of the hepatic surface up to the dome of the diaphragm.
Peritoneal washings should be obtained, especially if the patient is
being evaluated for pancreatic cancer, as the presence of malignant
cells has been shown to influence resectability and prognosis.
Approximately 100 mL of 0.9% normal saline is instilled into the
subhepatic space, and the fluid is dispersed by agitating the
abdomen. The right side of the table is then tilted downward, and the
fluid is aspirated and sent for cytologic analysis.
When a parenchymal lesion, peritoneal implant, or suspicious lymph
node is identified, laparoscopic biopsy can be done with great
precision. Depending on the size and location, tissue may be obtained
by a variety of techniques, including fine-needle, core-needle,
forceps, and incisional or excisional biopsy. If bleeding develops,
it is usually easily controlled using electrosurgery, clip
application, or laparoscopic suture ligation.
Table 2 summarizes the laparoscopic
staging procedures that are applicable to the various regions of the
Laparoscopic techniques are well-suited to confirm the diagnosis of
hepatocellular carcinoma or metastatic liver lesions, in that they
can be used to visualize a surface lesion and perform a biopsy.
Laparoscopic techniques have the additional advantage of permitting
direct control of hemorrhage, if necessary. Specimens for cytologic
analysis can also be obtained by laparoscopic methods.
Furthermore, laparoscopy is a reliable method for detecting
additional small lesions and peritoneal seeding, which are usually
missed by other imaging methods. For example, transcutaneous
abdominal ultrasonography is known to have a false-negative rate for
liver metastasis that exceeds 50% in some studies. Moreover, a
multi-institution study demonstrated that 42% of patients with
hepatic metastases from colorectal carcinoma who were deemed
resectable by CT scan were, in fact, un-resectable at the time of laparotomy.
Primary Liver Tumors
In the 1980s, the potential benefits of staging laparoscopy for
primary liver tumors were reported by Lightdale and Jeffers et al,
who, using laparoscopy, identified unresectability due to multifocal
tumors and peritoneal implantation in 83% of the 41 patients in their
combined series.[4,5] Thus, staging laparoscopy spared these patients
an unnecessary laparotomy. In a recent series of 50 consecutive
patients diagnosed with potentially resectable liver tumors,
laparoscopy alone demonstrated unresectability in 46%, and
nontherapeutic laparotomy was avoided in these patients.
Despite these data, laparoscopic evaluation alone has been the
subject of continued criticisms. These include the inability of
laparoscopy to: (1) palpate the liver parenchyma, (2) assess
perihilar lymph nodes and retroperitoneal structures, and (3) exclude
portal vein thrombosis, all of which are critical to accurate tumor staging.
These objections can be addressed by considering the additional
contributions of intraoperative ultrasonography to the staging of
hepatic malignancies. Numerous studies have shown that intraoperative
ultrasound during open operations is more sensitive for the detection
of liver lesions than preoperative imaging modalities, including
ultrasound, CT, CT portography, and magnetic resonance imaging (MRI).[8,9]
When Clarke and colleagues compared intraoperative ultrasonography to
preoperative ultrasonography, CT, and angiography in 54 patients,
intraoperative ultrasound showed 25% to 35% of additional liver
lesions. Moreover, 40% of the 167 lesions detected by intraoperative
ultrasound were not visible or palpable at the time of exploratory
laparotomy. Based on the results of intraoperative ultrasonography,
the operative plan was altered in one-third of the study group.
Intraoperative ultrasonography also may be used to evaluate
surrounding structures, including the portal vein and perihilar structures.
With the advent of laparoscopic ultrasound (Figure
1), accuracy comparable to that of intraoperative ultrasound can
be obtained without a major abdominal incision. Preliminary data
suggested that, in 48% of patients undergoing a planned hepatic
resection for malignancy, the combination of
laparoscopy and laparoscopic ultrasonography averted a nontherapeutic
laparotomy. In a study of 50 patients by John and colleagues,
laparoscopic staging using ultrasound significantly increased the
resectability rate of hepatic malignancies from 58% to 93%, when
compared with as-sessment without laparoscopy. More recent small
series in the literature have reported similar promising results.[12,13]
Intraoperative ultrasound may also be used during primary resection
of colorectal cancer to identify liver metastases that are not
detected by preoperative ultrasound or CT. In a prospective analysis
of 189 patients with colorectal carcinoma, Machi et al[14,15]
demonstrated that intraoperative ultrasound had a 82% sensitivity for
the identification of lesions that went undetected by preoperative
studies. These lesions later progressed to a size detectable by
abdominal ultrasound and/or CT.
Early identification of patients with liver metastasis may serve to
direct adjuvant therapy or earlier surgical treatment for metastatic
disease (Figure 2). An obvious
extension of this is the use of laparoscopic ultrasonography of the
liver during laparoscopic surgery for colorectal cancer. At the
Cleveland Clinic, we have demonstrated that laparoscopic
ultrasonography is a safe and rapid technique that permits systematic
scanning of all eight hepatic segments through a single cannula site.
In order to better evaluate the efficacy of this technique, we are
currently conducting a prospective, blindedinvestigation comparing
laparoscopic ultrasonography to conventional preoperative imaging
modalities in patients undergoing resection of colorectal malignancies.
1. Fernández-del Castillo C, Rattner DW, Warshaw AL: Further
experience with laparoscopy and peritoneal cytology in the staging of
pancreatic cancer. Br J Surg 82:1127-1129, 1995.
2. Ferrucci JT: Liver tumor imaging: Current concepts. Am J
Roentgenol 155:473-484, 1990.
3. Steele G Jr, Bleday R, Mayer RJ, et al: A prospective evaluation
of hepatic resection for colorectal carcinoma metastases to the
liver: Gastrointestinal tumor study group protocol 6584 J Clin Oncol
4. Lightdale CJ: laparoscopy and biopsy in malignant liver disease.
Cancer 50:2672-2675, 1982.
5. Jeffers L, Spieglman G, Reddy R, et al: Laparoscopically directed
fine needle aspiration for the diagnosis of hepatocellular carcinoma;
a safe and accurate technique. Gastrointest Endosc 34:235-237, 1988.
6. John TG, Greig JD, Crosbie JL, et al: Superior staging of liver
tumors with laparoscopy and laparoscopic ultrasound. Ann Surg
7. Bismuth H, Castaing D, Garden OJ: The use of operative ultrasound
in surgery of primary liver tumors. World J Surg 11:610-614, 1987.
8. Ravikumar TS: Laparoscopic staging and intraoperative
ultrasonography for liver tumor management. Surg Oncol Clin North Am
9. Hagspiel KD, Neidl KFW, Eichenberger AC: Detection of liver
metastases: Comparison of superparamagnetic iron oxide-enhanced and
unenhanced MR imaging at 1.5 T with dynamic CT, intraoperative US,
and percutaneous US. Radiology 196:471-478, 1995.
10. Clarke MP, Kane RA, Steele G Jr, et al: Prospective comparison of
preoperative imaging and intraoperative ultrasonography in the
detection of liver tumors. Surgery 106:849-855, 1989.
11. Babineau TJ, Lewis D, Jenkins RL, et al: Role of staging
laparoscopy in the treatment of hepatic malignancy. Am J Surg
12. Feld RI, Liu J-B, Nazarian L, et al: Laparoscopic liver
sonography: Preliminary experience in liver metastasis compared with
CT portography. J Ultrasound Med 15:289-295, 1996.
13. Barbot DJ, Marks JH, Feld RI, et al: Improved staging of liver
tumors using laparoscopic intraoperative ultrasound. J Surg Oncol
14. Machi J, Iomoto H, Yanashita Y, et al: Intraoperative
ultrasonography in screening for liver metastases form colorectal
cancer: Comparative accuracy with traditional procedures. Surgery
15. Machi J, Isomoto H, Kurohiji T, et al: Accuracy of intraoperative
ultrasonography in diagnosing liver metastasis from colorectal
cancer: Evaluation with postoperative follow-up results. World J Surg
16. Marchesa P, Milsom JW, Hale JC, et al: Intraoperative
laparoscopic liver ultrasonography for staging of colorectal cancer:
Initial experience. Dis Colon Rectum 39(suppl):73-78, 1996.
17. Dagnini G, Marin G, Patella M, et al: Laparoscopy in the
diagnosis of primary carcinoma of the gallbladder: A study of 98
cases. Gastrointest Endosc 30:289-291, 1984.
18. van Delden OM, de Wit LTh, Nieveen van Dijkum EJM, et al: Value
of laparoscopic ultrasonography in staging of proximal bile duct
tumors. J Ultrasound Med 16:7-12, 1997.
19. Bartlett DL, Fong Y, Fortner JG, et al: Long-term results after
resection for gallbladder cancer. Ann Surg 224:639-646, 1996.
20. Cotlar AM, Mueller CR, Pettit JW, et al: Trocar site seeding of
inapparent gallbladder carcinoma during laparoscopic
cholecystectomy.J Laparoendosc Surg 6:35-45, 1996
. 21. Fernández-del Castillo C, Rattner DW, Warshaw AL:
Peritoneal metastases in pancreatic carcinoma. Hepatogastroenterology
22. John TG, Greig JD, Carter DC: Carcinoma of the pancreatic head
and periampullary region: Tumor staging with laparoscopy and
laparoscopic ultrasonography. Ann Surg 221:156-164, 1995.
23. Weiss SM, Skibber JM, Mohiuddin M, et al: Rapid intra-abdominal
spread of pancreatic cancer. Arch Surg 203:644-651, 1986.
24. Moosa AR, Gamagami RA: Diagnosis and staging of pancreatic
neoplasms. Surg Clin North Am 75:871-890, 1995.
25. Warshaw AL: Implications of peritoneal cytology for staging of
early pancreatic cancer. Am J Surg 161:26-30, 1991.
26. Bemelman WA, de Wit LTh, van Delden OM, et al: Diagnostic
laparoscopy combined with laparoscopic ultrasonography in staging of
cancer of the pancreatic head region. Br J Surg 82:820-824, 1995.
27. Fein J, Gerdes H, Karpeh M, et al: Overstaging of ulcerated
gastric cancers by endoscopic ultrasonography. Gastrointest Endosc
28. Stell DA, Carter CR, Stewart I, et al: Prospective comparison of
laparoscopy, ultrasonography, and computed tomography in the staging
of gastric cancer. Br J Surg 83:1260-1262, 1996.
29. Conlon KCP, Karpeh MS: Laparoscopy and laparoscopic ultrasound in
the staging of gastric cancer. Semin Oncol 23:347-351, 1996.
30. Lowy AM, Mansfield PF, Leach SD: Laparoscopic staging for gastric
cancer. Surgery 119:611-614, 1996.
31. Bartlett DL, Conlon KCP, Gerdes H, et al: Laparoscopic
ultrasonography: The best pretreatment staging modality in gastric
adenocarcinoma? Case report. Surgery 118:562-566, 1995.
32. Molloy RG, McCourtney JS, Anderson JR: Laparoscopy in the
management of patients with cancer of the gastric cardia and
oesophagus. Br J Surg 82:352-354, 1995.
33. Nieveen van Dijkum EJM, de Wit LTh, van Delden OM, et al: The
efficacy of laparoscopic staging in patients with upper
gastrointestinal tumors. Cancer 79:1315-1319, 1997.
34. OBrien MG, Fitzgerald EF, Lee G, et al: A prospective
comparison of laparoscopy and imaging in the staging of
esophagogastric cancer before surgery. Am J Gastroenterol
35. Finch MD, John TG, Garden OJ, et al: Laparoscopic ultrasonography
for staging gastroesophageal cancer. Surgery 121:10-17, 1997.
36. Manayan RC, Hart MJ, Friend WG: Radioimmunoguided surgery for
colorectal cancer. Am J Surg 173:386-389, 1997.