Value of Laparoscopy in the Staging

Diego Camacho, Dan Reichenbach, Georg D Duerr, Tammy L Venema, John F Sweeney,
William E Fisher
The Elkins Pancreas Center, Michael E DeBakey Department of Surgery,
Baylor College of Medicine. Houston, Texas, USA
Summary
Pancreatic cancer is a devastating disease that
swiftly robs patients of both quality and
quantity of life. It is the fourth leading cause
of cancer death in the United States. In 2003,
there were 31,860 reported new cases with
31,270 deaths occurring due to lack of
effective therapy. Eighty percent of patients
present with either advanced local or
metastatic disease. Dynamic contrast-
enhanced computed tomography (CT) has
become the current staging test of choice.
Laparoscopic staging of pancreatic tumors
with the addition of ultrasound can reveal
intraparenchymal hepatic metastases, small
peritoneal metastases, and critical retro-
peritoneal
tumor-vessel
relationships
approaching the accuracy of open exploration
to
determine
resectability
without
significantly increasing morbidity or
mortality. However, given the current
accuracy of high-quality CT, the routine use
of diagnostic laparoscopy in pancreatic cancer
is not warranted. Diagnostic laparoscopy is
recommended in select patients with primary
tumors greater than 4 cm, tumors in the body
or tail of the pancreas, patients with equivocal
findings of metastasis on CT, ascites, or
clinical or laboratory findings suggesting
advanced disease such as marked weight loss,
hypoalbuminemia, and elevated CA 19-9.
Introduction
Pancreatic cancer is a devastating disease that
swiftly robs patients of both quality and
quantity of life. It is the fourth leading cause
of cancer death in the United States. In 2003,
there were 31,860 reported new cases with
31,270 deaths occurring due to lack of
effective therapy [1]. At least 80% of patients
with pancreatic cancer present with either
locally advanced or metastatic disease and are
unresectable at the time of diagnosis.
Pancreatic cancer tends to recur after surgery
and is relatively resistant to adjuvant therapy
thus contributing to a poor overall survival
[2]. The overall 5-year survival after resection
is somewhere between 15-20%. In patients
that fall into the better prognostic groups
(such as small tumors, negative lymph nodes,
favorable molecular genetics) the 5-year
survival can approach 40-50%. However,
surgery is currently the only treatment
available that offers a meaningful
improvement in survival. Therefore, it is
critical that we identify patients who might
benefit from resection, and avoid a surgical
approach in unresectable patients who will be
better served with palliative treatment.
Despite recent advances in imaging and non-
operative techniques to relieve biliary
obstruction, many patients still undergo an
exploratory laparotomy for accurate staging
and palliation [3, 4, 5, 6, 7]. A negative

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laparotomy is associated with significant
perioperative morbidity and diminishes
quality of life postoperatively [6, 8]. Many
older studies demonstrate that laparoscopic
staging is superior to radiological staging
especially with detection of small peritoneal
and hepatic disease [9, 10, 11]. With recent
advances in minimally invasive surgery, a
thorough surgical staging procedure for
pancreatic cancer is now possible.
In this review, we identify the limitations of
current staging modalities used in pancreatic
adenocarcinoma and evaluate the advantages
and disadvantages of routine laparoscopy as a
staging tool as well as for palliative treatment.
Computerized Tomography (CT)
CT scan has undergone a revolutionary
evolution over the last 20 years with new
developments that have improved data
acquisition, processing and image handling
[10, 12, 13, 14, 15]. Conventional CT has
been replaced by dynamic thin section CT,
spiral CT, multidetector CT (MDCT), and
three-dimensional reconstruction.
The criteria predictive for unresectability
based upon CT scanning are: 1) extra-
pancreatic metastases (hepatic, serosal, or
peritoneal); 2) extrapancreatic extension of
the tumor beyond bile duct, duodenum or
gastric antrum; 3) celiac axis or hepatic hilar
lymph nodes; 4) invasion or encasement of
the celiac axis, hepatic, or superior mesenteric
arteries; or, 5) involvement of the portal or
superior mesenteric vein with thrombosis [3,
16]. CT is accurate in assessing extra-
pancreatic involvement, but it is limited in
assessing local vascular invasion (portal vein
and superior mesenteric artery involvement).
It is frequently difficult to distinguish whether
the tumor is touching vascular structures or
actually invading them; a distinction that can
often only be made at the time of surgery.
In a study by Velanovich et al., the accuracy
of conventional CT scanning alone in
predicting unresectable disease was 92%, but
the accuracy of CT scanning for predicting
resectable disease was only 45% [17]. In a
similar study by Ross et al., the accuracy of
predicting unresectable disease was 93%, and
the accuracy of predicting resectable disease
was 38% [15]. A study by Fuhrman et al. has
shown that thin section contrast enhanced CT
predicted resectability in 88% of patients [16].
Although this study reports a high predictive
value of CT scanning in determining
resectability, it includes peri-pancreatic
malignancies that are known to have a limited
incidence of peritoneal metastases.
Several authors have shown spiral CT to be
accurate for staging pancreatic cancer and
particularly for predicting resectability [18,
19, 20]. Bluemke et al., using single-phase
spiral CT, correctly predicted resectability in
70% of patients with pancreatic cancer [19].
Diehl et al. correctly predicted unresectable
disease in 96% of patients and resectable
disease in 79% using dual-phase spiral CT
[20]. Gmeinwieser et al. showed that spiral
CT was 93% and 100% accurate in detecting
portal venous and arterial involvement,
respectively [18].
The current staging test of choice is multi-
detector 3D CT scan that allows acquisition of
three-dimensional data and imaging of the
entire pancreas in a single breath-hold. With
reconstruction of overlapping images and
elimination of artifacts from movement with
inspiration, the detection of small lesions and
arterial and venous involvement is markedly
improved.
A recent study correlated findings of MDCT
with actual resectability determined at surgery
in 25 patients. Two patients (8%) were
considered not resectable because of vascular
invasion which was confirmed in one at
surgery. Of the 23 patients deemed resectable
by CT, 20 were resected yielding a negative
predictive value of 87% (20/23). In these
three patients, small metastases to the liver
and peritoneum were discovered at surgery
[21]. In another recent study, 44 patients
underwent thin-section dual-phase MDCT to
stage their tumor, followed by open surgery.
Of the 44 patients, 23 were resectable. The
sensitivity for CT in predicting resectability
was 96% (22/23) but the specificity was only
33% (7/21). Only the degree of arterial
involvement was a significant predictor of

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resectability. The authors concluded that even
modern CT remains relatively nonspecific for
predicting resectability and diagnostic
laparoscopy continues to have an important
role in staging of pancreatic cancer [22].
Preliminary data involving multi-detector row
CT (MDCT) and curved planar reconstruction
show that the reformation images are
equivalent to the transverse images obtained
from MDCT. In a study by Prokesch et al., 43
patients underwent MDCT for suspected
pancreatic tumors. Subsequently, curved
planar reformations were generated along the
pancreatic duct, common bile duct, and major
mesenteric vessels. The two modalities were
then compared for presence of tumor,
resectability, and vascular involvement. When
assessing the ability to detect pancreatic
cancer, MDCT had a sensitivity of 95% and
specificity of 90%, compared to
reconstruction images of 98% and 91%
respectively. For the ability to determine
tumor resectability, MDCT had a sensitivity
of 86% and specificity of 85%, compared to
71% and 84% respectively for reconstruction
images [23].
Although advances in CT have improved the
ability to predict resectability, limitations
remain including the sensitivity of CT to
detect tumors less than 1 cm in diameter, thus
limiting the detection of peritoneal metastatic
deposits, small liver metastases, and
peritoneal micrometastases [24, 25, 26]. CT
scan also cannot distinguish between reactive
lymphadenopathy and malignant deposits.
Concern remains about the potential for a
false positive diagnosis of unresectability
resulting in an inappropriate denial of surgery
and a false positive diagnosis or resectability
resulting in an unnecessary trip to the
operating room. These limitations can
potentially be overcome with the assistance of
other imaging modalities particularly
diagnostic laparoscopy with the use of
laparoscopic ultrasonography and biopsy [27].
Endoscopic
Retrograde
Cholangio-
pancreatography (ERCP)
ERCP is often used as a diagnostic tool in
pancreatic cancer but is rarely of any benefit
[28, 29]. Most surgeons agree that ERCP is
not a useful test in pancreatic cancer. Pre-
operative relief of bile duct obstruction is of
benefit only when the patient has severe
jaundice or cholangitis. It has been clearly
shown that preoperative biliary stenting to
relieve jaundice is unnecessary in most cases.
ERCP to delineate duct anatomy and to obtain
cytological brushings may be useful when
pancreatic cancer is suspected but no mass is
seen on CT [10]. However, a normal
pancreatogram does not completely exclude
malignancy [24]. The differentiation between
chronic pancreatitis and pancreatic cancer can
also be difficult on ERCP. In one study,
ERCP was misleading in the diagnosis of
pancreatic cancer in 13% of patients [30].
Further, diagnostic ERCP always carries the
risk of pancreatitis and can induce cholangitis
[31, 32] and thus is not recommended as a
routine diagnostic test in pancreatic cancer;
however, the use of ERCP with biliary
decompression is appropriate in selected
patients with profound jaundice and hepatic
dysfunction or when there will be a delay in
surgical treatment.
Magnetic Resonance Imaging (MRI)
Abdominal MRI is rapidly evolving but
currently provides essentially the same
information as CT scanning [27]. Its initial
limitations involve image artifacts from
respiration, aortic pulsation, bowel peristalsis,
and a lack of ideal contrast material for the
gut lumen. Recent advances have improved
abdominal imaging with MRI but it has not
replaced high-quality CT-scanning at this
time. In recent studies from Steiner et al., T2-
weighted images were comparable with and
in 22% of cases superior to the CT scan
because it showed a difference in the signal
intensity between the tumor and the normal
pancreatic tissue [33]. MRI was also slightly
superior to CT in visualizing larger tumor
masses but overall no significant advantage
was offered over a high-quality CT. A
prospective study comparing CT, MRI,
angiography and EUS in 62 patients
determined that CT had the highest accuracy
in predicting resectability (83%). The authors

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suggested that the most cost-effective strategy
is to use CT as the initial test followed by
other confirmatory techniques in potentially
resectable cases [34].
Endoscopic Ultrasonography (EUS)
Endoscopic ultrasound (EUS) can be used to
detect small pancreatic masses when there is a
high suspicion for pancreatic cancer but no
mass is clearly identified by CT scan. With
the probe placed in the stomach or duodenum
right next to the pancreas, interference from
overlying bowel gas is eliminated and allows
for higher frequency waves, which improve
image resolution [27]. EUS is also a sensitive
test for portal vein invasion and is superior to
abdominal US and CT in determining tumor
size, extent, and lymph node status. EUS is
somewhat less effective at detecting superior
mesenteric artery invasion. As with all
ultrasound applications, EUS of the pancreas
is limited by the experience and expertise of
the ultrasonographer.
Endoscopic–Ultrasound-Guided Fine-Needle
Aspiration (EUS-FNA)
Fine needle aspiration (FNA) can be
performed using EUS as a guide. Several
authors have reported highly sensitive and
specific results for percutaneous FNA with
minimal morbidity [35, 36, 37]. Initially there
was concern that malignant cells could seed
the peritoneal cavity along the needle tract
during percutaneous biopsy of pancreatic
cancers and EUS-FNA would avoid this
problem [38]. However, many biopsies have
been performed percutaneously without the
appearance of this complication. The role of
preoperative EUS-FNA, or percutaneous
biopsy, is limited because a negative biopsy
does not rule out cancer and does not preclude
the need for surgical exploration. However,
this technique is very useful if a protocol
involving neoadjuvant treatment is under
consideration. In expert hands, adequate
specimens are obtained in about 95% of cases
and the results often expedite therapy and
influence clinical decisions [39, 40, 41]. The
sensitivity of EUS-FNA is 84% along with a
specificity of 96%, giving this technique a
reported accuracy of 85% [41].
Cytology
Diagnostic laparoscopy provides the
opportunity to obtain peritoneal washings for
cytology. This can be helpful as a prognostic
indicator because negative cytology is
correlated with improved survival even in the
presence of metastases [42, 43, 44, 45]. In
contrast, positive peritoneal cytology is
usually correlated with metastatic disease and
poor survival. Peritoneal washings for
cytology can easily be performed at the time
of diagnostic laparoscopy. However, the
results are not available at the time of surgery,
which mandates a second anesthetic for this
information to be utilized in clinical decision-
making regarding need for open exploration.
One report indicated that cytology will be
positive and exclude 10% of patients from
exploration despite a CT and simple
laparoscopy (without ultrasound) consistent
with resectable disease [46].
Diagnostic Laparoscopy
Computers and microchip technology have
led to a trend towards minimally invasive
surgery. Modern surgeons strive to
manipulate anatomy and provide surgical care
in the least invasive method possible. In
addition, wide acceptance of laparoscopic
cholecystectomy has brought laparoscopic
surgery into the mainstream of general
surgical practice. These new techniques are
now being applied to a wider spectrum of
general surgical problems. Most patients with
pancreatic cancer have metastatic disease and
cannot benefit from surgery. However, even
with the advancement of radiographic
imaging, it can be difficult to determine
which patients are candidates for resection
and minimally invasive surgery may help
avoid unnecessary diagnostic laparotomies.
Several studies have demonstrated the value
of laparoscopy in the staging of abdominal
malignancies [3, 9, 10, 11, 47, 48, 49].

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Laparoscopic examination allows for direct
visualization of intra-abdominal contents and
has been reported to identify hepatic and
peritoneal metastases that were not shown by
other modalities. Diagnostic laparoscopy
involves a general exploration of the
abdominal surfaces including palpation of the
liver with two instruments. The hilum of the
liver is visualized and the foramen of
Winslow is examined and periportal lymph
nodes are biopsied if enlarged. The transverse
colon and omentum are reflected cephalad
and the base of the transverse mesocolon is
examined for tumor with particular attention
to the mesocolic vessels. The gastrocolic
ligament/omentum is incised and the lesser
sac is examined [3].
A critical appraisal of the literature reveals
that the percentage of patients with
unresectable disease found at diagnostic
laparoscopy has decreased over time as the
sensitivity of CT scanning has improved.
Conlon et al. examined 115 patients with
pancreatic cancer using abdominal CT and
diagnostic laparoscopy [3]. Sixty-seven
patients out of 115 were considered to have
resectable disease on completion of the
laparoscopic examination. A resection was
performed in 61 patients, so the correct
assessment of resectability was (91%). Six
patients (9%) did not undergo resection
because of disease that was missed at
laparoscopy. In five cases, laparoscopy failed
to identify hepatic metastases, and
encasement of the portal vein was not
appreciated in one patient. Unresectable
disease was identified in 41 patients. Open
exploration and resection were performed
under the same anesthetic upon completion of
the laparoscopy. There were no intraoperative
or postoperative complications related to the
laparoscopic procedure. The positive
predictive index, negative predictive index
and accuracy of the procedure were 100%,
91% and 94%, respectively. This study
showed that use of laparoscopy significantly
reduces the percentage of patients undergoing
open exploration without resection, with an
overall resectability rate of 76%.
In 1998 Merchant and Conlon reported their
results using a laparoscopic technique to
evaluate 442 consecutive patients with
pancreatic and periampullary malignancies
[45]. Preoperative radiographic evaluation
included a contrast-enhanced CT in all
patients (n=420), and selective use of
ultrasonography (n=194), ERCP (n=195), and
visceral angiography (n=22). Based on this
assessment, 339 patients (77%) were
considered to have resectable disease with
303 patients subsequently undergoing
laparoscopic staging. After laparoscopic
evaluation, only 199 patients were still
considered to have resectable disease and 104
were determined to be unresectable with
findings of liver metastases (n=48),
extrapancreatic disease (n=41), nodal disease
(n=20), and vascular invasion (n=37). One
patient was found to have benign disease.
There were 18 patients considered resectable
upon laparoscopic exploration, who were not
resected during laparotomy. In fact, 181
patients out of 199 (91%) considered
resectable after laparoscopic assessment were
resected. Of 104 patients considered to be
unresectable at laparoscopy, none underwent
resection. Consequently the laparoscopic
assessment provided a positive predictive
index of 100%, a negative predictive index of
91%, and an accuracy of 94%.
Laparoscopic Ultrasonography
Despite the aforementioned results achieved
by laparoscopy alone, this procedure still has
limitations in the staging of pancreatic cancer,
including only two-dimensional inspection of
the surface of the liver and the peritoneal
cavity and a lack of tactile sensation. These
factors limit the identification of small intra-
parenchymal hepatic metastases and make it
difficult to evaluate the critical retroperitoneal
tumor-vessel relationships [45, 50].
Laparoscopic ultrasound (LUS) probes offer a
possible solution allowing the surgeon to
examine the liver, the porta hepatis, and the
portal vein and superior mesenteric artery.
Diagnostic laparoscopy with the use of

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ultrasound improves the accuracy of
predicting resectability up to as high as 98%
in some studies [50, 51, 52, 53, 54].
Bemelman et al. staged seventy patients with
pancreatic cancer with laparoscopy and LUS.
Twenty-one patients were found to have
metastatic disease. Of 49 patients undergoing
laparotomy, 21 of 22 considered resectable
after LUS examination were resected. Also, 6
of 13 patients that were considered “probably
resectable” as well as 2 of 14 that were
deemed unresectable, were, in fact, resected.
The overall sensitivity and specificity for
determining resectability were 67% and 96%,
respectively. Unnecessary laparotomy was
avoided in 14 patients (19%) and the
therapeutic approach was changed in 18
patients (25%) using the combination of
laparoscopy and LUS [55].
John et al. evaluated 40 patients with
potentially resectable pancreatic cancer [51].
Metastatic disease was identified with
laparoscopy alone in 14 patients (35%). The
addition of LUS revealed factors that
increased the number of patients deemed
unresectable (59%). The overall accuracy in
predicting resectability with the addition of
LUS was 89% compared with only 65% with
laparoscopy alone.
Merchant and Conlon reported a prospective
evaluation of 90 patients with pancreatic
tumors undergoing laparoscopy with LUS
[45]. Conventional imaging techniques such
as CT scan identified 65 patients as being
resectable, 17 as unresectable, and 8 as
equivocal. Laparoscopy showed 36 patients to
be resectable, 13 to be equivocal and 41 to be
unresectable. The use of LUS in addition to
laparoscopy revealed a primary tumor in 88
patients, involvement of the portal vein in 87
patients, the superior mesenteric vein in 85
patients, and the hepatic and superior
mesenteric artery in 84 patients. LUS
confirmed the resectable and unresectable
cases determined by laparoscopy alone. Of 13
patients with equivocal findings at
laparoscopy, LUS identified 8 with
unresectable disease. Five patients with
equivocal findings at laparoscopy were
considered resectable with LUS. Four of those
underwent resection and only one was found
to be unresectable because of celiac axis
involvement not identified by LUS. Taken all
together, this study provided a positive
predictive index of 100%, a negative
predictive index of 98%, and an accuracy of
98% in determining resectability.
Initial CT scans obtained in patients with
pancreatic cancer often are of a suboptimal
quality and therefore do not properly reveal
metastatic disease that would be evident on a
high-quality CT scan. In some studies,
diagnostic laparoscopy with the use of
ultrasound improves the accuracy of
predicting resectability to about 98% [50, 51,
53, 54]. The true yield of laparoscopy cannot
be assessed from studies that do not use a
state of the art CT scan prior to laparoscopy.
Advances in the quality of preoperative
imaging have led to accurate radiographic
prediction of resectability in at least 80% of
cases. This fact does diminish the usefulness
of laparoscopy and LUS as a routine
diagnostic technique prior to laparotomy
(particularly if performed under separate
anesthesia) [56].
Clinical data suggests that laparoscopy may
be important in the prevention of unnecessary
laparotomy in selected patients that are at
higher risk for contraindications to resection
despite a CT scan consistent with resectable
disease [50]. Selective use of staging
laparoscopy may be of benefit to avoid a non-
therapeutic laparotomy in up to 13% of
patients that come to surgery for pancreatic
cancer. The addition of LUS during
laparoscopic staging enhances the ability of
laparoscopy to determine resectability of
these tumors. The experience at the
Massachusetts General Hospital with staging
laparoscopy and peritoneal cytology over an
8-year period in 239 patients indicates that
approximately 30% of patients without
metastases by CT harbor occult metastatic
disease detectable at laparoscopy [46].
Currently, there is no data addressing factors
found on a CT scan or clinically that will
predict a positive laparoscopy in conjunction
with LUS. However, we would suggest that
patients with a tumor measuring greater than

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4 cm, tumors found in the body or tail of the
pancreas, weight loss greater than 9 kg,
hypoalbuminemia, or a markedly elevated CA
19-9 would suggest a positive laparoscopy
with LUS. In some studies, the accuracy of
laparoscopy in combination with LUS for the
assessment of resectability approaches that of
open laparotomy without significantly
increasing morbidity or mortality.
Conclusion
In 2005, the accuracy of CT scanning in
predicting resectability in patients with
pancreatic cancer has improved to about 90%.
Approximately one in ten patients brought to
the operating room with the intent of a
curative resection will be found at the time of
surgery to have unresectable cancer.
Diagnostic laparoscopy is more sensitive than
CT in detecting small superficial liver and
peritoneal metastases. As with all ultrasound
techniques, laparoscopic ultrasound is limited
by the skills of the ultrasonographer.
However, in experienced hands, it seems to
improve the detection of intraparenchymal
liver metastases and involvement of the portal
vein, superior mesenteric vein and superior
mesenteric artery. The addition of peritoneal
washings for cytology improves the detection
of stage IV disease but this requires the
laparoscopic examination to be performed
under a separate anesthetic. The increased
costs of diagnostic laparoscopy with
laparoscopic ultrasound cannot be justified for
the small subset that will benefit from its
routine use. A selective use in cases where
detection of unresectable disease is more
likely seems to be a rational approach. Factors
that suggest a higher yield with diagnostic
laparoscopy include a large primary tumor
(greater than 4 cm), a tumor in the body or tail
of the pancreas, equivocal findings of
metastasis on CT, the presence of ascites,
severe weight loss (greater than 9 kg),
hypoalbuminemia, and a markedly elevated
CA 19-9.
The ability of minimally invasive surgeons
and endoscopists to diagnose and palliate
unresectable pancreatic cancer is likely to
continue to improve and these techniques will
play an increasingly important role in the care
of patients with pancreatic cancer. Likewise,
the accuracy of radiological imaging
techniques to detect unresectable disease will
also continue to advance and further decrease
the incidence of nontherapeutic laparotomies.
Thus, the optimal application of conventional
surgery and minimally invasive approaches
for the diagnosis and palliation of pancreatic
cancer will continue to evolve.
Received June 14
th
, 2005 - Accepted August
1
st
, 2005
Keywords Laparoscopy; Neoplasm Staging;
Pancreatic Neoplasms
Abbreviations LUS: laparoscopic ultra-
sonography; MDCT: multidetector computed
tomography
Acknowledgements The authors would like
to acknowledge grant support from the
National Cancer Institute (1 K08 CA85822-
01A1)
Correspondence
William E Fisher
1709 Dryden, Suite 1500
Houston, Texas 77030
USA
Phone: +1-713.798.8070
Fax: +1-713.798.4530
E-mail: wfisher@bcm.tmc.edu
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