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Imaging of hepatopancreatobiliary diseases 79
Figure 5.16 A 48-year-old woman with bile duct injury from laparoscopic cholecystectomy. Fluoroscopic spot image from ERCP
demonstrates amorphous contrast extravasation upon cannulation and injection of the common bile duct (a) consistent with bile
duct injury. Percutaneous transhepatic cholangiogram demonstrates opacification of the intrahepatic bile ducts on the right to the
level of the confluence of the right and left hepatic ducts where surgical clips are present (b). Incidentally noted is variant biliary
anatomy with right posterior sectional duct inserting on the left hepatic duct.
common symptomatic abnormality of the gallbladder is
acute cholecystitis. The most appropriate imaging options
for suspected acute cholecystitis are ultrasound or cholescintigraphy. Acute cholecystitis is typically manifest by
gallbladder wall thickening, pericholecystic fluid, stones,
and a positive sonographic Murphy’s sign (tendernesss
elicited by the ultrasound probe directly over the
gallbladder). Two separate meta-analyses compared cholescintigraphy with ultrasound and found that ultrasound
had a sensitivity of 81–88% and specificity of 80–83% and
cholescintigraphy a sensitivity of 96–97% and specificity
of 90% [58,59]. Ultrasound is generally more easily
accessible and avoids the need for radiation, making it
a good choice for initial evaluation. Cholecscintigraphy
may be used in the setting of equivocal ultrasound findings (see Figure 5.5).
In addition to acute cholecystitis, adenomyomatosis is a
frequently encountered benign gallbladder process. This
is often seen as an incidental imaging finding of focal wall
thickening with characteristic cystic spaces on MRI or
with classic comet tail artifact on ultrasound related to
crystal formation within intramural mucosal diverticula
Figure 5.17 Perihepatic collection following cholecystectomy. Axial CT image through the abdomen (a) demonstrates large
perihepatic fluid collection. Postcontrast axial MR image through the abdomen obtained 40 minutes after injection of Eovist
intravenous contrast (b) demonstrates Eovist hepatobiliary contrast excretion through the bile duct layering in the nondependent
portion of the perihepatic fluid collection, confirming that this fluid collection represents a biloma.
80 Chapter 5
Figure 5.18 Adenomyomatosis. Axial T2-weighted MR image demonstrates luminal narrowing of the fundus of the gallbladder with
thickened wall containing small T2 bright cystic spaces in the gallbladder wall which correspond to Rokitansky–Aschoff sinuses.
These findings are consistent with fundal adenomyomatosis. The remainder of the gallbladder is normal. These same findings are
redemonstrated on a thick slab MRCP image (b).
known as Rokitansky–Aschoff sinuses [60] (Figure 5.18).
Adenomyomatosis is a benign process that has no malignant potential, and when the classic imaging features are
present, no further work-up is required. The more focal
mass-like presentation of adenomyomatosis may mimic
malignancy and can be difficult to differentiate on preoperative imaging.
Gallbladder carcinoma has a poor prognosis a nd
often presents with advanced disease. The most common imaging presentation is of a large intraluminal
mass with invasion of the adjacent liver followed by
the less common presentation of intraluminal polyp or
diffuse/focal wall thickening [61]. No prospective
studies have compared MR, CT, and PET/CT for preoperative staging. CT provides accurate information
regarding liver involvement, nodal enlargement, and
presence of distant metastases [62]. MR/MRCP may
provide supplemental information regarding involvement of the bile duct in cancers that involve the
gallbladder neck [63].
5.2.4 Pancreas
5.2.4.1 Cystic pancreatic lesions
Focal pancreatic lesions are best assessed by CT or MRI,
and both modalities have similar diagnostic accuracy [64–66]. Although there are classic radiological
appearances of solid tumors and cystic tumors of the
pancreas, there may also be overlap in the imaging
appearance of some cystic entities [65], and ultimately
the lesions may require aspiration and analysis of fluid
contents under endoscopic ultrasound [67,68].
Classically, a rim-enhancing peripancreatic cystic
lesion containing nonenhancing debris, in the setting
of prior pancreatitis, will represent a pseudocyst [69]
(Figure 5.19a,b). This is in contradistinction to intrapancreatic cystic lesions, which in the setting of prior
pancreatitis may represent walled-off necrosis. In the
absence of prior pancreatitis, cystic lesions should raise
concern for neoplasm. While there is considerable overlap in the imaging appearance of cystic lesions, there are
some features that help to differentiate them [70]. A
multilobulated, “sponge-like” lesion will represent a
serous cystic neoplasm (Figure 5.19c,d). Intraductal papillary mucinous neoplasms (IPMN) will demonstrate
communication with the pancreatic duct and may appear
tubular or like a “cluster of grapes.” A cystic lesion with a
thick wall and no or only a few septations, usually in the
body or tail of the pancreas, will represent a mucinous
cystic neoplasm (Figure 5.19e). These features provide a
general framework but there are exceptions such as the
following: Some serous neoplasms may be oligocystic and
mimic mucinous neoplasms. Neuroendocrine tumors can
present with primarily cystic appearance. The communication with the pancreatic duct in the setting of IPMN may
not be discernible on imaging. When there is doubt as to
the diagnosis, endoscopic US with cytology and fluid
sampling may be indicated.
5.2.4.2 Solid pancreatic lesions
Pancreatic adenocarcinomas account for the vast majority
of pancreatic malignancies. These tumors are often infiltrative hypoenhancing masses which can occur in any
Imaging of hepatopancreatobiliary diseases 81
Figure 5.19 Classic examples of select cystic pancreatic lesions including pseudocyst (a,b), serous cystadenoma (c,d) and mucinous
cystic neoplasm (e). Axial T2-weighted images through a T2 hyperintense cystic lesion in the pancreatic head (a,b) demonstrate T2
hypointense debris within the dependent portion of the lesion which did not demonstrate contrast enhancement, consistent with
pseudocyst. Thick slab MRCP (c) and thin section T2 fat sat coronal (d) images demonstrate a large lobulated lesion in the pancreatic
head which contains innumerable thin septations consistent with a serous cystadenoma, confirmed on EUS with fluid sampling.
Axial CT image through the pancreatic tail (e) demonstrates a cystic lesion with several thick septations, confirmed as mucinous
cystic neoplasm on aspiration and distal pancreatectomy.
portion of the pancreas and are equally well evaluated for
potential surgical resection by CT and MRI [71]. These
tumors classically produce pancreatic duct and/or common bile duct obstruction (Figure 5.20) and are locally
advanced at presentation in about three quarters of
patients [72]. Other solid lesions in the pancreas include
neuroendocrine tumors which are usually distinguished
from pancreatic adenocarcinoma by their hyperenhancement on arterial phase imaging. Other solid lesions to
consider in the pancreas include solid pseudopapillary
tumor, metastases, and lymphoma, in addition to mimics
of tumor such as focal pancreatitis.
82 Chapter 5
Figure 5.20 A 58-year-old man with right upper quadrant pain and elevated liver function tests. Axial arterial phase CT image
through the pancreatic head demonstrates pancreatic and common bile duct dilatation secondary to ill-defined hypoenhancing mass
in the pancreatic head. These findings are consistent with pancreatic adenocarcinoma with “double duct sign,” better depicted on a
curved multiplanar reformatted image (b). The patient underwent a successful Whipple procedure.
KEY POINTS
• Various imaging modalities are available for the assessment of HPB diseases, and modalities are often complementary.
Discussion with the radiologist can help with determination of modality and customizing an examination, if necessary.
• CT contrast can be nephrotoxic and should generally not be administered to patients with acute renal failure; patients with endstage renal disease on hemodialysis may receive contrast which can then be dialyzed.
• MR contrast agents are not nephrotoxic and generally can be administered to patients with eGFR greater than 30 mL/min.
However, contrast administration policies vary by institution.
• While ultrasound is an acceptable modality for focal liver lesion screening in patients with chronic liver disease, the
characterization of focal liver lesions is best performed with contrast-enhanced liver CT or MRI.
• Detailed anatomical information regarding HPB diseases is best achieved with CT or MRI, but nuclear scintigraphy examinations
can provide valuable complementary physiological information.
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Videos 1–26 will be of interest to readers of this chapter.
Visit the companion website at:
www.wiley.com\go\conrad\liver-pancreas-biliary-laparoscopic-surgery
CHAPTER 6
Role of staging laparoscopy in
hepatopancreatobiliary malignancies
Anil K. Agarwal, Raja Kalayarasan, and Amit Javed
Department of Gastrointestinal Surgery and Liver Transplant, Govind Ballabh Pant Hospital and Maulana Azad Medical College, Delhi University,
New Delhi, India
EDITOR COMMENT
In this comprehensive chapter on staging laparoscopy for HPB diseases, the authors report the technique and respective evidence for
performing staging laparoscopy, extended staging laparoscopy, and regional lymph node sampling to avoid non-therapeutic
laparotomies. The chapter summarizes the available data for pancreatic cancer, intra- and extrahepatic biliary cancer, hepatocellular
carcinoma, gallbladder cancer, and metastatic colorectal cancer. The value of including palliative biliary and enteric bypass in pancreatic
cancer patients with positive staging laparoscopy is reviewed. Further, the technique and value of peritoneal lavage are shown and the
optimal timing (prior to planned resection or as a separate procedure) is explored. The authors expand on how the yield of staging
laparoscopy could be increased through optimal indications, performing regional lymph node sampling, and staging laparoscopic
ultrasound.
Keywords: carcinomatosis, extended staging laparoscopy, minimally invasive lymph node staging, minimally invasive palliation, occult
metastases, peritoneal lavage, staging laparoscopic ultrasound, staging laparoscopy, staging of hepatopancreatobiliary disease,
timing of staging laparoscopy
The objective of preoperative evaluation for any malignancy, including pancreatic and hepatobiliary malignancy, is to identify patients who would benefit from
surgical exploration and exclude those with metastatic or
locally advanced unresectable disease. Despite significant
advancements in imaging technology for preoperative
assessment of accurate stage of pancreatic and hepatobiliary tumors, some patients with metastatic disease
are not diagnosed preoperatively and are detected for
the first time after surgical exploration, resulting in a
nontherapeutic laparotomy. Staging laparoscopy (SL) is
a minimally invasive tool that has conventionally been
used to detect these radiologically occult metastatic diseases in various gastrointestinal malignancies to avoid
unnecessary laparotomies [1,2]. Avoidance of a nontherapeutic laparotomy results in decreased morbidity related
Laparoscopic Liver, Pancreas, and Biliary Surgery: Textbook and Illustrated Video Atlas, First Edition.
Edited by Claudius Conrad and Brice Gayet.
© 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd.
to the incision and the procedure, faster recovery, shorter
hospital stay, and reduced time to initiation of chemotherapy/radiotherapy [1,2].
The concept of SL was introduced in the era when all
definitive procedures were being performed by an open
approach. Staging laparoscopy enabled direct visualization of the peritoneal cavity to detect small peritoneal and
surface liver metastases which precluded a curative surgical resection. Over the years, there has been a significant
change in the role of staging laparoscopy. On one hand,
there have been significant improvements in crosssectional imaging (computed tomography [CT] and magnetic resonance imaging [MRI]), widespread use of
newer modalities like positron emission tomography
(PET) scans, endoscopic ultrasound (EUS), and increasing
role of tumor markers. This has led to increased
85
86 Chapter 6
preoperative detection of metastatic disease with a resultant decrease in the overall yield of staging laparoscopy [3,4]. On the other hand, the procedure of SL
itself has evolved and it is not just limited to the detection
of radiologically occult metastases (like peritoneal and
surface liver deposits). It is now often performed in
conjunction with laparoscopic ultrasound (LUS) and
has become a valuable tool in determining not just metastatic disease but also locoregional resectability of the
tumor [5]. Additional dissection can be performed to
better assess inaccessible areas, determine locoregional
extent, and sample distant lymph nodes. In addition, it
has gained a new role in the era of portal vein embolization and neoadjuvant treatment protocols for downstaging hepatopancreatobiliary tumors.
Widespread adoption of laparoscopy for tumor ablation
(like radiofrequency ablation) and curative surgical resection has redefined the role of staging laparoscopy [6,7]. As
more and more complex surgical resections for cancers
are performed laparoscopically, SL has become an integral initial part of the procedure itself and its role is thus
not limited to the avoidance of a nontherapeutic laparotomy. While newer techniques like PET scans have the
potential to decrease the yield of SL, it may be associated
with false-positive and -negative rates which would need
further confirmation [8]. This chapter aims to highlight
the current status of SL in the management of pancreatic
and hepatobiliary malignancies.
6.1 Indications for staging
laparoscopy
The principal indication for SL has been detection of
radiologically occult metastatic disease [9]. This is done
with the primary aim of preventing a nontherapeutic
laparotomy. Occult intra-abdominal metastatic disease
could be in the form of liver metastases (surface/deep
intraparenchymal), peritoneal carcinomatosis or distant
metastatic lymph nodes. While the presence of peritoneal
and distant lymph nodal metastases may contraindicate a
surgical resection, detection of additional tumors in the
liver (primary and secondary) may alter the magnitude of
proposed resection or change the management plan
altogether.
Another important aim of SL is assessment of locoregional extent of disease [3,4]. This is important because of
a change in philosophy as more and more centers perform
increasingly radical operations to achieve complete resection. Locoregional resectability can be ascertained by
direct visualization or a limited laparoscopic dissection.
The accuracy is further improved by combining laparoscopic ultrasound [10]. Laparoscopic ultrasound Doppler
probes not only help to assess involvement of locoregional vessels (e.g. portal vein/hepatic veins in hepatobiliary malignancies; superior mesenteric/portal vein and
superior mesenteric artery in pancreatic malignancies)
but also to qualify the extent of involvement (limited/
circumferential/tumor thrombus, etc.).
Recently, SL has also been used to exclude metastatic
disease in patients with borderline resectable/locally
advanced tumors before planning neoadjuvant therapy
or an invasive interventional procedure such as portal
vein embolization [11]. This approach may be used to
plan neoadjuvant therapy for downstaging such tumors.
If axial imaging is indeterminate, a second-look SL can
then be performed after completion of such treatment to
assess locoregional tumor response or disease progression. Patients especially with colorectal cancer liver
metastases who receive neaodjuvant chemotherapy
may develop chemotherapy-associated steatohepatitis [9]. A SL with a liver biopsy may be useful in these
cases in addition to evaluation of the extent of tumor. A SL
with a liver biopsy may also be performed to evaluate the
extent of fibrosis/cirrhosis in patients with hepatocellular
carcinoma (HCC) [12]. In tumors necessitating extended
liver resections (hilar cholangiocarcinoma/gallbladder
cancer [GBC]), SL has also been proposed to exclude
metastatic disease prior to performing portal vein embolization [3]. A repeat SL may then be performed after four
to six weeks (at the time of surgery), which helps to rule
out disease progression (new lesions that may contraindicate the planned resection) and assess the adequacy of
the hypertrophy of the future liver remnant. In very
selected cases, laparoscopic portal vein ligation can be
performed during SL, which combines the benefits of SL
and portal vein embolization in a single procedure but has
the downsides of facing a dissected porta during the actual
resection and some concerns as to the same degree of liver
hypertrophy resulting from portal vein embolization and
ligation [13].
Staging laparoscopy may also have a role in differentiating benign from malignant lesions. In certain thick-walled
gallbladders (on cross-sectional imaging), the differential
diagnosis includes cancer and other malignant masqueraderssuchaschroniccholecystitisorxanthogranulomatous
Role of staging laparoscopy in hepatopancreatobiliary malignancies 87
cholecystitis [14]. A SL in such patients may provide additional clues that may help in making a diagnosis. If the
probability of the lesion being benign in such a scenario is
higher, the gallbladder with a wedge of adjacent liver may
be resected laparoscopically and sent for frozen section. In
the current era of significant advancements in complex
laparoscopic surgery, a SL in such situations is useful and
often an inseparable part of the surgical plan.
6.2 Technique of staging
laparoscopy
In the simplest form, a SL is performed by inserting a
laparoscope (usually 30°) through an abdominal port and
systematically assessing the abdominal cavity [15]. This
can visualize peritoneal metastases and surface liver
metastases. We have defined these lesions as detectable
lesions (DLs), which can be seen by simple SL without any
additional dissection or gadgets [16]. If there are concerns
for metastatic disease, DLs are biopsied and frozen section
histopathological examination is performed. To biopsy a
suspected metastasis and to visualize hidden areas such as
the undersurface of the liver, SL is usually performed
using two ports [16]. Additional ports are inserted as
required for lysing adhesions, performing more complex
biopsies or when an extended SL is performed.
The first trocar may be inserted by open or closed
technique as per surgeon preference. While most surgeons insert the first trocar in the periumbilical region, the
site of the second trocar is usually chosen within the line
of the planned incision, should the disease be found to be
resectable. The second port needs to be 10 mm if laparoscopic ultrasound is to be performed. Any significant
ascites is aspirated and sampled for cytology examination.
To allow for a systematic examination of all four quadrants of the peritoneal cavity, obstructing adhesions are
divided [17]. Placement of additional ports facilitates
complete systematic examination of the peritoneal cavity.
After inspection of the peritoneum, the anterior and
posterior surfaces of the right and left lobes of the liver
are examined. The hepatoduodenal ligament, the foramen of Winslow, and hilum of the liver are examined for
lymphadenopathy.
The patient is then placed in 10–15° Trendelenburg
position. The omentum is retracted into the left upper
quadrant after inspection of its surface for any evidence of
omental deposits. The ligament of Treitz and the inferior
surface of the transverse mesocolon are then inspected for
evidence of metastatic deposits and for lymphadenopathy. In standard SL, no additional dissection is performed
except for minimal adhesiolysis to facilitate complete
examination of the peritoneal cavity. The term
“undetectable lesions” refers to those lesions which are
not detected by a simple SL alone and require additional
dissection to assess resectability and sample distant lymph
nodes or need the help of gadgetry like an intraoperative
ultrasound. Extended staging laparoscopy is performed to
assess resectability in situations where a “simple staging
laparoscopy” (SSL) does not reveal any metastatic lesions.
6.3 Extended staging laparoscopy
Extended SL is defined as an SL procedure which entails
more than a simple visualization of the peritoneal cavity.
It includes additional dissection to visualize inaccessible
areas, assess locoregional resectability, distant (celiac/
interaortocaval) lymph nodal sampling, addition of laparoscopic ultrasound, and/or peritoneal lavage cytology.
For examination of the lesser sac, the gastrohepatic
omentum is divided and the caudate lobe and inferior
vena cava are examined [17]. Division of the gastrohepatic omentum also facilitates the examination of
the anterior aspect of the head of the pancreas.
6.3.1 Lymph node biopsy
While biopsy of the nodes in the hepatoduodenal ligament
can be performed, it is not routinely recommended as
evidence of disease in this region does not contraindicate a
curative resection for primary pancreatic and hepatobiliary malignancies. Hence, it should be selectively performed (e.g. in patients with colorectal liver metastases)
where it can alter the management decision. However, it
may be advisable to assess the distantceliac and aortocaval
lymph nodes. Division of the gastrohepatic omentum and
superior traction on the stomach facilitate identification of
the left gastric artery. The left gastric artery can then be
followed to its origin to allow inspection of the celiac axis
and biopsy of any enlarged celiac nodes [17]. For aortocaval lymph node biopsy, a duodenal kocherization is
performed to adequately expose the aortocaval space.
Any enlarged lymph nodes in the aortocaval region below
the level of the left renal vein are excised and sent for
frozen section examination. Positive aortocaval/celiac
lymph nodes on frozen section analysis are considered
88 Chapter 6
as metastatic disease in the majority of the pancreatic and
hepatobiliary malignancies, and the planned surgical
resection is abandoned [18].
6.3.2 Peritoneal lavage cytology
Some authors have advocated peritoneal cytology to
further increase the yield in hepatic, biliary, and pancreatic cancers [19,20]. In this procedure, approximately
150–200 mL of normal saline is instilled and aspirated
in each of the following areas of the peritoneal cavity
sequentially: the right upper quadrant, the left upper
quadrant, and the pelvis. Specimens are then centrifuged
and stained using the Papanicolaou technique. Positive
peritoneal cytology is defined as peritoneal cytology that
is highly suspicious or positive for adenocarcinoma [19].
To avoid false-positive results, cytological washings are
taken prior to any biopsy. The principal drawback of
including peritoneal lavage cytology routinely as a part
of single stage SL is that the results are not immediately
available and usually take at least 24 hours [19]. This
precludes SL and operative exploration at the same sitting. Also, the increase in the yield above a standard SL
alone is unclear and therefore may not justify routine use.
6.3.3 Laparoscopic ultrasound
Laparoscopic ultrasound consists of placement of a
6–10 MHz linear or curvilinear array transducer through
a 10 mm port and systematic examination of the anterior,
lateral, and inferior surfaces of the liver for evidence of
intraparenchymal liver metastases [21]. The hepatoduodenal ligament, peripancreatic, aortocaval, and celiac axis
lymph nodes are then evaluated. Laparoscopic ultrasound is also used to assess the locoregional extent of
the tumor with respect to critical vascular structures. In
the case of HCC, intrahepatic cholangiocarcinoma (IHC),
and colorectal liver metastases, LUS is used to determine
the proximity of the tumor to major hepatic veins. In a
recent study, Viganò et al. reported that LUS is a reliable
tool for staging liver tumors with a performance similar to
that of open intraoperative ultrasound in detecting new
nodules [5]. For hilar cholangiocarcinoma, an LUS probe
is placed in a transverse direction over the hepatoduodenal ligament to determine portal vein invasion and
hepatic artery involvement. For pancreatic cancers, it is
used to determine the relationship of the tumor with the
portal vein, superior mesenteric veins–splenic vein confluence, superior mesenteric artery, and celiac axis. It is
also used to locate small pancreatic tumors and detect
additional lesions within the pancreas as in the case of islet
cell tumors [21]. Laparoscopic ultrasound Doppler flow
pattern also helps in the assessment of vascular involvement. Proper assessment of the hepatoduodenal ligament
and porta hepatis can be performed by filling the right
upper quadrant with saline or releasing most of the
pneumoperitoneum.
6.4 Yield of staging laparoscopy
Yield of staging laparoscopy refers to the probablity of
avoiding nontherapeutic laparotomy. The yield of SL is
calculated by dividing the number of patients detected to
have unresectable disease at SL by all patients undergoing
staging laparoscopy [16]. The accuracy of SL for unresectable disease is calculated by dividing the number of
patients detected to have unresectable disease at SL by all
those with unresectable disease [16]. This definition is
limited by varying assessments of unresectable disease.
For example, some centers will define nonlocoregional
metastatic lymph nodes as unsuitable for resection, and
there are various definitions of locally unresectable disease. These differences in definition should be taken into
consideration before making definitive conclusions
regarding the yield and utility of staging laparoscopy.
Over the years, there has been a decline in the reported
overall yield of SL [3,4] (Table 6.1). This is attributed to
the advancements in cross-sectional imaging (CT scan
and MRI) and the emergence of newer techniques like
PET and EUS which have the potential to detect both
metastatic disease and locally advanced disease [22,23].
Simultaneously, there have been advancements in
Table 6.1 Evolution in the yield of staging laparoscopy in
pancreatic and hepatobiliary malignancies with advancements in
imaging technology.
Malignancy type Yield of staging laparoscopy
Studies published
up to 2005
Pancreatic cancer 25–40% 2–34%
Hepatocellular 16–39% 7–40%
carcinoma
Hilar 25–53% 14–45%
cholangiocarcinoma
Gallbladder cancer 38–83% 23–62%
Studies published
after 2005
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